XVI. ORGANS OF VISION…

XVI. ORGANS OF VISION

In the lowest forms of animal life the whole surface is sensitive to light, and organs of vision have no doubt arisen in the first instance from limited areas becoming especially sensitive to light in conjunction with a deposit of pigment. Lens-like structures, formed either as a thickening of the cuticle, or as a mass of cells, were subsequently formed; but their function was not, in the first instance, to throw an image of external objects on the perceptive part of the eye, but to concentrate the light on it. From such a simple form of visual organ it is easy to pass by a series of steps to an eye capable of true vision.

There are but few groups of the Metazoa which are not provided with optic organs of greater or less complexity.

In a large number of instances these organs are placed on the anterior part of the head, and are innervated from the anterior ganglia. It is possible that many of the eyes so situated may be modifications of a common prototype. In other instances organs of vision are situated in different regions of the body, and it is clear that such eyes have been independently evolved in each instance.

The percipient elements of the eye would invariably appear to be cells, one end of each of which is continuous with a nerve, while the other terminates in a cuticular structure, or indurated part of the cell forming what is known as the rod or cone.

The presence of such percipient elements in various eyes is therefore no proof of genetic relationship between these eyes, but merely of similarity of function.

Embryological data as to the development of the eye do not exist except in the case of the Arthropoda, Mollusca and Chordata. From such data as there are, combined with study of the adult structure of the eye, it can be shewn that two types of development are found. In one of these the percipient elements are formed from the central nervous system, in the other from the epidermis. The former may be called cerebral eyes. It is probable however that this distinction is not, in all cases at any rate, so fundamental as might be supposed; but that in both instances the eye may have taken its origin from the epidermis. In the eyes in which the retina is continuous with the central nervous system, these two organs were probably evolved simultaneously as differentiations of the epidermis, and continue to develop together in the ontogenetic growth of the eye.

Some of the eyes in which the retina is formed from the epidermis have also probably arisen simultaneously with part of the central nervous system, while in other instances they have arisen as later formations subsequently to the complete establishment of a central nervous system.

Coelenterata. The actual evolution of the eye is best shewn in the Hydrozoa. The simplest types are those found in Oceania and Lizzia[182]. In Lizzia the eye is placed at the base of a tentacle and consists of (fig. 276) a lens (l) and a percipient bulb (oc). The lens is a simple thickening of the cuticle, while the percipient part of the eye is formed of three kinds of elements:--(1) pigment cells; (2) sense cells, forming the true retinal elements, and consisting of a central swelling with the nucleus, a peripheral process representing a hardly differentiated rod, and a central process continuous with (3) ganglion cells at the base of the eye. In this eye there is present a commencing differentiation of a ganglion as well as of a retina.

[182] O. and R. Hertwig. Das Nervensystem u. Sinnesorgane d. Medusen. Leipzig, 1878.

[FIG. 276. EYE OF LIZZIA KOELLIKERI. (From Lankester; after Hertwig.)

l. lens; oc. perceptive part of eye.]

The eye of Oceania is simpler than that of Lizzia in the absence of a lens. Claus has shewn that in Charybdea amongst the Acraspeda a more highly differentiated eye is present, with a lens formed of cells like the vertebrate eye.

Mollusca. In a large number of the odontophorous Mollusca eyes, innervated by the supraoesophageal ganglia, are present on the dorsal side of the head. These eyes exhibit very various degrees of complexity, but are shewn both by their structure and development to be modifications of a common prototype.

The simplest type of eye is that found in the Nautilus, and although the possibility of this eye being degenerated must be borne in mind, it is at the same time very interesting to note (Hensen) that it retains permanently the early embryonic structure of the eyes of the other groups.

It has (fig. 277 A) the form of a vesicle, with a small opening in the outer wall, placing the cavity of the vesicle in free communication with the exterior. The cells lining the posterior face of the vesicle form a retina (R); and are continuous with the fibres of the optic nerve (N.op). We have no knowledge of the development of this eye.

[FIG. 277. THREE DIAGRAMMATIC SECTIONS OF THE EYES OF MOLLUSCA. (After Grenacher.)

A. Nautilus. B. Gasteropod (Limax or Helix). C. Dibranchiate Cephalopod.

Pal. eyelid; Co. cornea; Co.ep. epithelium of ciliary body; Ir. iris; Int, Int^1 ... Int^4. different parts of the integument; l. lens; l^1. outer segment of lens; R. retina; N.op. optic nerve; G.op. optic ganglion; x. inner layer of retina; N.S. nervous stratum of retina.]

In the Gasteropods the eye (fig. 277 B) has the form of a closed vesicle: the cells lining the inner side form the retina, while the outer wall of the vesicle constitutes the cornea. A cuticular lens is placed in the cavity, on the side adjoining the cornea. This eye originates from the ectoderm, within the velar area, and close to the supraoesophageal ganglia, usually at the base of the tentacles. According to Rabl (Vol. II. No. 268) it is formed as an invagination, the opening of which soon closes; while according to Bobretzky (Vol. II. No. 242) and Fol it arises as a thickening of the epiblast, which becoming detached takes the form of a vesicle. It is quite possible that both types of development may occur, the second being no doubt abbreviated. The vesicle, however formed, soon acquires a covering of pigment, except for a small area of its outer wall, where the lens becomes formed as a small body projecting into the lumen of the vesicle. The lens seems to commence as a cuticular deposit, and to grow by the addition of concentric layers. The inner wall of the vesicle gives rise to the retina.

The most highly differentiated molluscan eye is that of the Dibranchiate Cephalopoda, which is in fact more highly organized than any other invertebrate eye.

A brief description of its adult structure[183] will perhaps render more clear my account of the development. The most important features of the eye are shewn in fig. 277 C. The outermost layer of the optic bulb forms a kind of capsule, which may be called the sclerotic. Posteriorly the sclerotic abuts on the cartilaginous orbit, which encloses the optic ganglion (G. op); and in front it becomes transparent and forms the cornea Co, which may be either completely closed, or (as represented in the diagram) perforated by a larger or smaller opening. Behind the cornea is a chamber known as the anterior optic chamber. This chamber is continued back on each side round a great part of the circumference of the eye, and separates the sclerotic from a layer internal to it.

[183] Vide Hensen, Zeit. f. wiss. Zool. Bd. XV.

In the anterior optic chamber there are placed (1) the anterior part of the lens (l^1) and (2) the folds of the iris (Ir). The whole chamber, except the part formed by the lens, is lined by the epidermis (Int^1 and Int^2). Bounding the inner side of the anterior optic chamber is a layer which is called the choroid (Int^1) which is continued anteriorly into the fold of the iris (Ir). The most superficial layer of the choroid is the epithelium already mentioned, next comes a layer of obliquely placed plates known as the argentea externa, then a layer of muscles, and finally the argentea interna. The argentea interna abuts on a cartilaginous capsule, which completely invests the inner part of the eye.

The lens is a nearly spherical body composed of concentric lamellæ of a structureless material. It is formed of a small outer (l^1) and large inner (l) segment, the two being separated by a thin membrane. It is supported by a peculiar projection of the wall of the optic cup, known as the ciliary body (Co.ep), inserted at the base of the iris, and mainly formed of a continuation of the retina. This body is however muscular, and presents a series of folds on its outer and inner surfaces, which are especially developed on the latter.

The membrane dividing the lens into two parts is continuous with the ciliary body. Within the lens is the inner optic chamber, bounded in front by the lens and the ciliary body, and behind by the retina.

The retina is formed of two main divisions, an anterior division adjoining the inner optic chamber, and a posterior division (N.S) adjoining the cartilage of the choroid. The two layers are separated by a membrane. Passing from within outwards the following layers in the retina may be distinguished:

(1) Homogeneous membrane. } Anterior division of (2) Layer of rods. } retina. (3) Layer of granules imbedded in pigment } (4) Cellular layer. } (5) Connective tissue layer. } Posterior layer of retina. (6) Layer of nerve-fibres. }

At the side of the optic ganglion is a peculiar body, known as the white body (not shewn in the figure), which has the histological characters of glandular tissue.

[FIG. 278. TWO SECTIONS THROUGH THE DEVELOPING EYE OF A CEPHALOPOD TO SHEW THE FORMATION OF THE OPTIC CUP. (After Lankester.)]

The first satisfactory account of the development of the eye is due to Lankester (No. 365). The more important features in it were also independently worked out by Grenacher (No. 363), and are beautifully illustrated in Bobretzky's paper (No. 362). The eye first appears as an oval pit of the epiblast, the edge of which is formed by a projecting rim (fig. 278 A). The epiblast layer lining the floor of the pit soon becomes considerably thickened. By the growth inwards of the rim the mouth of the pit is gradually narrowed (fig. 278 B), resembling at this stage the eye of Nautilus, and finally closed. There is thus formed a flattened sack, lined by epiblast, which may be called the primary optic vesicle. Its cavity eventually forms the inner optic chamber. The anterior wall of the sack is lined by a much less columnar layer than the posterior, the former giving rise to the epithelium on the inner side of the ciliary processes, the latter to the retina.

[FIG. 279. TRANSVERSE SECTION THROUGH THE HEAD OF AN ADVANCED EMBRYO OF LOLIGO. (After Bobretzky.)

gls. salivary gland; g.vs. visceral ganglion; gc. cerebral ganglion; g.op. optic ganglion; adk. optic cartilage; ak. and y. lateral cartilage or (?) white body; rt. retina; gm. limiting membrane of retina; vk. ciliary region of eye; cc. iris; ac. auditory sack (the epithelium lining the auditory sacks is not represented); vc. vena cava; ff. folds of funnel; x. epithelium of funnel.]

The cavity of the sack rapidly enlarges, and assumes a spherical form. At the same time a layer of mesoblast grows in between the walls of the sack and the external epiblast. Two new structures soon arise nearly simultaneously (fig. 279),--which become in the adult eye the iris (cc) and the posterior segment of the lens. The iris is formed as a circular fold of the skin in front of the optic vesicle. It consists both of epiblast and mesoblast, and gives rise to a pit lined by epiblast. The posterior segment of the lens arises as a structureless rod-like body, which is shewn in fig. 279 depending from the inner side of the anterior wall of the optic vesicle. Its exact mode of origin is somewhat obscure. The following is Lankester's account of it[184]: "It is formed entirely within the primitive optic chamber, and at first depends as a short cylindrical rod from the middle point of the anterior wall of that chamber, that is to say, from the point at which the chamber finally closed up. It grows subsequently by the deposition of concentric layers of a horny material round this cone. No cells appear to be immediately concerned in effecting the deposition, and it must be looked upon as an organic concretion, formed from the liquid contained in the primitive optic chamber."

[184] "Devel. of Cephalopoda." Q. J. Micro. Scien. 1875, p. 44.

The lens would thus appear to be a cuticular structure. It gradually assumes a nearly spherical form; and is then composed of concentrically arranged layers (fig. 280, hl).

While the lens is being formed, the ciliary epithelium of the optic vesicle becomes divided into two layers, an outer layer of large cells and an inner of small cells. Both layers are at first continuous across the anterior wall of the optic chamber in front of the lens, but soon become confined to the sides (fig. 280 A, cc and gz). The inner layer is stated by Lankester to give rise to the muscles present in the adult. The mesoblast cells also disappear from the region in front of the lens, and the outer epithelium is converted into a kind of cuticular membrane. By these changes the original layers of cells in front of the lens become reduced to mere membranes,--a change which appears to be preparatory to the appearance of the anterior segment of the lens. The formation of the latter has not been fully followed out by any investigator except Bobretzky. His figures would seem to indicate that it is formed as a cuticular deposit in front of the membrane already spoken of (fig. 280 B, vl). The two segments of the lens appear at any rate to be separated by a membrane continuous with the ciliary region of the optic vesicle.

Grenacher believes that the front part of the lens is formed in a pocket-like depression of the epiblastic layer covering the outer side of the optic cup; and Lankester thinks that the lens "pushes its way through the median anterior area of the primitive optic chamber, and projects into the second or anterior optic chamber where the iridian folds lie closely upon it."

While the lens is attaining its complete development there appears a fresh fold round the circumference of the eye, which gradually grows inwards so as to form a chamber outside the parts already present. This chamber is the anterior optic chamber of the adult. In most Cephalopods (fig. 277 C) the edges of the fold do not quite meet, but leave a larger or smaller aperture leading into the chamber containing the iris, outer segment of the lens, etc. In some forms however they meet and coalesce, and so shut off this chamber from communication with the exterior. The edge of the fold constitutes the cornea while the remainder of it gives rise to the sclerotic.

[FIG. 280. SECTIONS THROUGH THE DEVELOPING EYE OF LOLIGO AT TWO STAGES. (After Bobretzky.)

hl. inner segment of lens; vl. outer segment of lens; a and a´. epithelium lining the anterior optic chamber; gz. large epiblast cells of ciliary body; cc. small epiblast cells of ciliary body; ms. layer of mesoblast between the two epiblastic layers of the ciliary body; af. and if. fold of iris; rt. retina; rt´´. inner layer of retina; st. rods; aq. cartilage of the choroid.]

The retina is at first a thick layer of numerous rows of oval cells (fig. 279). When the inner segment of the lens is far advanced towards its complete formation pigment becomes deposited in the anterior part of the retina, and a layer of rods grows out from the surface turned towards the cavity of the optic vesicle (fig. 280 A, st). At a slightly later stage the retina becomes divided into two layers (Bobretzky), a thicker anterior layer, and a thinner posterior layer (fig. 280, rt and rt´´). The former is composed of two strata, (1) the rods and (2) a stratum with numerous rows of nuclei which becomes in the adult the granular layer with its pigment. The posterior layer gives rise to the cellular part of the posterior division of the retina, while layers of connective tissue around it give rise to the connective tissue of this portion of the retina (layer 6 in the scheme on p. 474). The nervous layer is derived from the optic ganglion which attaches itself to the inner side of the connective tissue layer.

The greater part of the choroid is formed from the mesoblast adjoining the retina, but the epithelium covering its outer wall is of epiblastic origin.

It is difficult to decide from development whether the Molluscan eyes, so far dealt with, originated in the first instance pari passu with the supraoesophageal ganglia or independently at a later period. On purely à priori ground I should be inclined to adopt the former alternative.

In addition to the above eyes there occur amongst Mollusca highly complicated eyes, of a very different kind, in two widely separated groups, viz. certain species of a genus of slug (Onchidium), and certain Lamellibranchiata. These eyes, though they have no doubt been evolved independently of each other, present certain remarkable points of agreement. In both of them the rods of the retina are turned away from the surface, and the nerve-fibres are placed, as in the Vertebrate eye, on the side of the retina which faces outwards.

The peculiar eyes of Onchidium, investigated by Semper[185], are scattered on the dorsal surface, there being normal eyes in the usual situation on the head. The eyes on the dorsal surface are formed of a cornea, a lens composed of 1-7 cells, and a retina surrounded by pigment; which is perforated in the centre by an optic nerve, the retinal elements being in the inverted position above mentioned.

[185] Ueber Sehorgane von Typus d. Wirbelthieraugen, etc., Wiesbaden, 1877, and Archiv f. mikr. Anat. Vol. XIV. pp. 118-122.

The development of these eyes has been somewhat imperfectly studied in the adult, in which they continue to be formed anew. They arise by a differentiation of the epidermis at the end of a papilla. At first a few glandular cells appear in the epidermis in the situation where an eye is about to be formed. Then, by a further process of growth, an irregular mass of epidermic cells becomes developed, which pushes the glandular cells to one side, and constitutes the rudiment of the eye. This mass, becoming surrounded by pigment, unites with the optic nerve, and its cells then differentiate themselves, in situ, into the various elements of the eye. No explanation is offered by Semper of the inverted position of the rods, nor is any suggested by his account of the development. As pointed out by Semper these eyes are no doubt modifications of the sensory epithelium of the papillæ.

The eyes of Pecten and Spondylus[186] are placed on short stalks at the edge of the mantle, and are probably modifications of the tentacular processes of the mantle edge. They are provided with a cornea, a cellular lens, a vitreous chamber, and a retina. The retinal elements are inverted, and the optic nerve passes in at the side, but occupies, in reference to its ramifications, the same relative situation as the optic nerve in the Vertebrate eye. The development has unfortunately not yet been studied.

[186] Vide Hensen (No. 364) and S. J. Hickson, "The Eye of Pecten," Quart. J. of Micr. Science, Vol. XX. 1880.

Our knowledge of the structure or still more of the development of the organ of vision of the Platyelminthes, Rotifera, and Echinodermata is too scanty to be of any general interest.

Chætopoda. Amongst the Chætopoda the cephalic eyes of Alciope (fig. 281) have been adequately investigated as to their anatomy by Greeff. These are provided with a large cuticular lens (l), separated from the retina by a wide cavity containing the vitreous humour. The retina is formed of a single row of cells, with rods at their free extremities, continuous at their opposite ends with nerve-fibres. The development of this eye has not been worked out. Eyes not situated on the head are found in Polyophthalmus, and have probably been evolved from the more indifferent type of sense-organ found by Eisig in the allied Capitellidæ.

Chætognatha[187]. The paired cephalic eyes of Sagitta are spherical bodies imbedded in the epidermis. They are formed of a central mass of pigment with three lenses partially imbedded in it. The outer covering of the eye is the retina, which is mainly composed of rod-bearing cells; the rods being placed in contact with the outer surface of each of the lenses. In the presence of three lenses the eye of Sagitta approaches in some respects the eye of the Arthropoda.

[187] O. Hertwig. "Die Chætognathen." Jenaische Zeitschrift, Vol. XIV. 1880.

Arthropodan eye. A satisfactory elucidation of the phylogeny of Arthropodan eyes has not yet been given.

All the types of eyes found in the group (with exception of that of Peripatus)[188] present marked features of similarity, but I am inclined to view this similarity as due rather to the character of the exoskeleton modifying in a more or less similar way all the forms of visual organs, than to the descent of all these eyes from a common prototype. In none of these eyes is there present a chamber filled with fluid between the lens and the retina, but the space in question is filled with cells. This character sharply distinguishes them from such eyes as those of Alciope (fig. 281). The types of eyes which are found in the Arthropoda are briefly the following:

[188] The eye of Peripatus is similar neither to the eye of the Arthropoda, nor to that of the Chætopoda, but resembles much more closely the Molluscan eye. The hypodermis and cuticle form together a highly convex cornea, within which is a large optic chamber, the posterior wall of which is formed by the retina. The optic chamber would appear to contain a structureless lens, but it is possible that what I regard as a lens may, on fuller investigation, turn out to be only a coagulum.

[FIG. 281. EYE OF AN ALCIOPID (NEOPHANTA CELOX). (From Gegenbaur; after Greef.)

i. cuticle; c. continuation of cuticle in front of eye; l. lens; h. vitreous humour; o. optic nerve; o´. expansion of the optic nerve; b. layer of rods; p. pigment layer.]

(1) Simple eyes. In all simple eyes the corneal lens is formed by a thickening of the cuticle. Such eyes are confined to the Tracheata.

There are three types of simple eyes. (a) A type in which the retinal cells are placed immediately behind the lens, found (Lowne) in the larvæ of some Diptera (Eristalis), and also in some Chilognatha.

(b) A type of simple eye found in some Chilopoda, and in some Insect larvæ (Dytiscus, etc.) (fig. 282), the parts of which are entirely derived from the epidermis. There is present a lens (l) formed as a thickening of the cuticle, a so-called vitreous humour (gl) formed of modified hypodermis cells, and a retina (r) derived from the same source. The outer ends of the retinal cells terminate in rods, and their inner ends are continuous with nerve-fibres.

(c) A type of simple eye found in the Arachnida, and apparently some Chilopoda, and forming the simple eyes of most Insects, which differs from type (a) in the cells of the retina forming a distinct layer beneath the hypodermis; the latter only obviously giving rise to the vitreous humour.

[FIG. 282. SECTION THROUGH THE SIMPLE EYE OF A YOUNG DYTISCUS LARVA. (From Gegenbaur; after Grenacher.)

l. corneal lens; g. vitreous humour; r. retina; o. optic nerve; h. hypodermis.]

The development of the simple eyes has not yet been studied.

The simple eyes so far described are always placed on the head, and are usually rather numerous.

(2) Compound eyes. Compound eyes are almost always present in the Crustacea, and are usually found in adult Insects. In both groups they are paired, though in the Crustacea a median much simplified compound eye may either take the place of the paired eyes in the Nauplius larva and lower forms, or be present together with them during a period in the development of higher forms.

The typical compound eye is formed (fig. 283) of a series of corneal lenses (c) developed from the cuticle; below which are placed bodies known as the crystalline cones, one to each corneal lens; and below the crystalline cones are placed bodies known as the retinulæ (r) constituting the percipient elements of the eye, each of them being formed of an axial rod, the rhabdom, and a number of cells surrounding it.

The crystalline cones are formed from the coalescence of cuticular deposits in several cells, the nuclei of which usually remain as Semper's nuclei. These cells are probably simple hypodermis cells, but in some forms, e.g. Phronima, there may be a continuous layer of hypodermis cells between them and the cuticle. In various Insect eyes the cells which usually give rise to a crystalline cone may remain distinct, and such eyes have been called by Grenacher aconous eyes, while eyes with incompletely formed crystalline cones are called by him pseudoconous eyes.

The rhabdom of the retinulæ is, like the crystalline cone, developed by the coalescence of a series of parts, which are primitively separate rods placed each in its own cell: this condition of the retinulæ is permanently retained in the eyes of the Tipulidæ.

The development of the compound eye has so far only been satisfactorily studied in some Crustacea by Bobretzky (No. 367); by whom it has been worked out in Palæmon and Astacus, but more fully in the latter, to which the following account refers:

The eye of Astacus takes its origin from two distinct parts, (1) the external epidermis of the procephalic lobes which will be spoken of as the epidermic layer of the eye, (2) a portion of the supraoesophageal ganglia, which will be spoken of as the neural layer of the eye. The mesoblast is moreover the source of some of the pigment between the two above layers. The epidermic layer gives rise to the corneal lenses, the crystalline cones, and the pigment around the latter. The neural layer on the other hand seems to give rise to the retinulæ with their rhabdoms, and to the optic ganglion.

[FIG. 283. DIAGRAMMATIC REPRESENTATIONS OF PARTS OF A COMPOUND ARTHROPOD EYE. (From Gegenbaur.)

A. Section through the eye. B. Corneal facets. C. Two segments of the eye.

c. corneal (cuticular) lenses; r. retinulæ with rhabdoms; n. optic nerve; g. ganglionic swelling of optic nerve.]

After the separation of the supraoesophageal ganglia from the superficial epiblast, the cells of the epidermis in the region of the future eye become columnar, and so form the above-mentioned epidermic layer of the eye. This layer soon becomes two or three cells deep. At the same time the most superficial part of the adjoining supraoesophageal ganglion becomes partially constricted off from the remainder as the neural layer of the eye, but is separated by a small space from the thickened patch of epidermis. Into this space some mesoblast cells penetrate at a slightly later period. Both the epidermic and neural layers next become divided into two strata. The outer stratum of the epidermic layer gives rise to the crystalline cones and Semper's nuclei; each crystalline cone being formed from four coalesced rods, developed as cuticular differentiations of four cells, the nuclei of which may be seen in the embryo on its outer side. The lower ends of the cones pass through the inner stratum of the epidermic disc, the cells of which become pigmented, and constitute the pigment cells surrounding the lower part of the crystalline cones in the adult. The outer end of each of the crystalline cones is surrounded by four cells, believed by Bobretzky to be identical with Semper's nuclei[189]. These cells give rise in a later stage (not worked out in Astacus) to the cuticular corneal lenses.

[189] There would appear to be some confusion as to the nomenclature of these parts in Bobretzky's account.

Of the two strata of the neural layer the outer is several cells deep, while the inner is formed of elongated rod-like cells. Unfortunately however the fate of the two neural layers has not been worked out, though there can be but little doubt that the retinulæ originate from the outer layer.

The mesoblast which grows in between the neural and epidermic layers becomes a pigment layer, and probably also forms the perforated membrane between the crystalline cones and the retinulæ.

The above observations of Bobretzky would appear to indicate that the paired compound eyes of Crustacea belong to the type of cerebral eyes. How far this is also the case with the compound eyes of Insects is uncertain, in that it is quite possible that the latter eyes may have had an independent origin.

The relation between the paired and median eye of the Crustacea is also uncertain.

In the genus Euphausia amongst the Schizopods there is present a series of eyes placed on the sides of some of the thoracic legs and on the sides of the abdomen. The structure of these eyes, though not as yet satisfactorily made out, would appear to be very different from that of other Arthropodan visual organs.

The Eye of the Vertebrata. In view of the various structures which unite to form it, the eye is undoubtedly the most complicated organ of the Vertebrata; and though its mode of development is fairly constant throughout the group, it will be convenient shortly to describe what may be regarded as its typical development, and then to proceed to a comparative view of the origin of its various parts, and to enter into greater detail with reference to some of them. At the end of the section there is an account of the accessory structures connected with the eye.

The formation of the eye commences with the appearance of a pair of hollow outgrowths from the anterior cerebral vesicle or thalamencephalon, which arise in many instances, even before the closure of the medullary canal. These outgrowths, known as the optic vesicles, at first open freely into the cavity of the anterior cerebral vesicle. From this they soon however become partially constricted, and form vesicles (fig. 284, a), united to the base of the brain by comparatively narrow hollow stalks, the rudiments of the optic nerves. The constriction to which the stalk or optic nerve is due takes place obliquely downwards and backwards, so that the optic nerves open into the base of the front part of the thalamencephalon (fig. 284, b).

[FIG. 284. SECTION THROUGH THE HEAD OF AN EMBRYO TELEOSTEAN, TO SHEW THE FORMATION OF THE OPTIC VESICLES, ETC. (From Gegenbaur; after Schenk.)

c. fore-brain; a. optic vesicle; b. stalk of optic vesicle; d. epidermis.]

After the establishment of the optic nerves, there take place (1) the formation of the lens, and (2) the formation of the optic cup from the walls of the primary optic vesicle.

The external or superficial epiblast which covers, and is in most forms in immediate contact with, the most projecting portion of the optic vesicle, becomes thickened. This thickened portion is then driven inwards in the form of a shallow open pit with thick walls (fig. 285 A, o), carrying before it the front wall (r) of the optic vesicle. To such an extent does this involution of the superficial epiblast take place, that the front wall of the optic vesicle is pushed close up to the hind wall, and the cavity of the vesicle becomes almost obliterated (fig. 285 B).

The bulb of the optic vesicle is thus converted into a cup with double walls, containing in its cavity the portion of involuted epiblast. This cup, in order to distinguish its cavity from that of the original optic vesicle, is generally called the secondary optic vesicle. We may, for the sake of brevity, speak of it as the optic cup; in reality it never is a vesicle, since it always remains widely open in front. Of its double walls the inner or anterior (fig. 285 B, r) is formed from the front portion, the outer or posterior (fig. 285 B, u) from the hind portion of the wall of the primary optic vesicle. The inner or anterior (r), which very speedily becomes thicker than the other, is converted into the retina: in the outer or posterior (u), which remains thin, pigment is eventually deposited, and it ultimately becomes the tesselated pigment-layer of the choroid.

[FIG. 285. DIAGRAMMATIC SECTIONS ILLUSTRATING THE FORMATION OF THE EYE. (After Remak.)

In A the thin superficial epiblast h is seen to be thickened at x, in front of the optic vesicle, and involuted so as to form a pit o, the mouth of which has already begun to close in. Accompanying this involution, which forms the rudiment of the lens, the optic vesicle is doubled in, its front portion r being pushed against the back portion u, and the original cavity of the vesicle thus reduced in size. The stalk of the vesicle is shewn as still broad.

In B the optic vesicle is still further doubled in so as to form a cup with a posterior wall u and an anterior wall r. In the hollow of this cup lies the lens l, now completely detached from the superficial epiblast xh.]

By the closure of its mouth the pit of the involuted epiblast becomes a completely closed sac with thick walls and a small central cavity (fig. 285 B, l). At the same time it breaks away from the external epiblast, which forms a continuous layer in front of it, all traces of the original opening being lost. There is thus left lying in the cup of the secondary optic vesicle, an isolated elliptical mass of epiblast. This is the rudiment of the lens. The small cavity within it speedily becomes still less by the thickening of the walls, especially of the hinder one.

At its first appearance the lens is in immediate contact with the anterior wall of the secondary optic vesicle (fig. 285 B). In a short time however, the lens is seen to lie in the mouth of the cup (fig. 288 D), a space (vh) (which is occupied by the vitreous humour) making its appearance between the lens and anterior wall of the vesicle.

In order to understand how this space is developed, the position of the optic vesicle and the relations of its stalk must be borne in mind.

The vesicle lies at the side of the head, and its stalk is directed downwards, inwards and backwards. The stalk in fact slants away from the vesicle. Hence, when the involution of the lens takes place, the direction in which the front wall of the vesicle is pushed in is not in a line with the axis of the stalk, as for simplicity's sake has been represented in the diagram (fig. 285), but forms an obtuse angle with that axis, after the manner of fig. 286, where s´ represents the cavity of the stalk leading away from the almost obliterated cavity of the primary vesicle.

Fig. 286 represents the early stage at which the lens fills the whole cup of the secondary vesicle. The subsequent condition is brought about through the rapid growth of the walls of the cup. This growth however does not take place equally in all parts of the cup. The walls of the cup rise up all round except that point of the circumference of the cup which adjoins the stalk. While elsewhere the walls increase rapidly in height, carrying so to speak the lens with them, at this spot, which in the natural position of the eye is on its under surface, there is no growth: the wall is here imperfect, and a gap is left. Through this gap, which afterwards receives the name of the choroidal fissure, a way is open from the mesoblastic tissue surrounding the optic vesicle and stalk into the interior of the cavity of the cup.

[FIG. 286. DIAGRAMMATIC SECTION OF THE EYE AND THE OPTIC NERVE AT AN EARLY STAGE. (From Lieberkühn.)

To shew the lens l occupying the whole hollow of the optic cup, the inclination of the stalk s to the optic cup, and the continuity of the cavity of the stalk s´ with that of the primary vesicle c; r. anterior, u. posterior wall of the optic cup.]

From the manner of its formation the gap or fissure is evidently in a line with the axis of the optic stalk, and in order to be seen must be looked for on the under surface of the optic vesicle. In this position it is readily recognised in the embryo seen as a transparent object (fig. 118, chs).

Bearing in mind these relations of the gap to the optic stalk, the reader will understand how sections of the optic vesicle at this stage present very different appearances according to the plane in which the sections are taken.

When the head is viewed from underneath as a transparent object the eye presents very much the appearance represented in the diagram (fig. 287).

A section of such an eye taken along the line y, perpendicular to the plane of the paper, would give a figure corresponding to that of fig. 288 D. The lens, the cavity and double walls of the secondary vesicle, the remains of the primary cavity, would all be represented (the superficial epiblast of the head would also be shewn); but there would be nothing seen of either the stalk or the fissure. If on the other hand the section were taken in a plane parallel to the plane of the paper, at some distance above the level of the stalk, some such figure would be obtained as that shewn in fig. 288 E. Here the fissure f is obvious, and the communication of the cavity vh of the secondary vesicle with the outside of the eye evident; the section of course would not go through the superficial epiblast. Lastly, a section, taken perpendicular to the plane of the paper along the line z, i.e. through the fissure itself, would present the appearances of fig. 288 F, where the wall of the vesicle is entirely wanting in the region of the fissure marked by the position of the letter f. The external epiblast has been omitted in this figure.

[FIG. 287. DIAGRAMMATIC REPRESENTATION OF THE EYE OF THE CHICK OF ABOUT THE THIRD DAY AS SEEN WHEN THE HEAD IS VIEWED FROM UNDERNEATH AS A TRANSPARENT OBJECT.

l. the lens; l´. the cavity of the lens, lying in the hollow of the optic cup; r. the anterior, u. the posterior wall of the optic cup; c. the cavity of the primary optic vesicle, now nearly obliterated. By inadvertence u has been drawn in some places thicker than r, it should have been thinner throughout. s. the stalk of the optic cup with s´ its cavity, at a lower level than the cup itself and therefore out of focus; the dotted line indicates the continuity of the cavity of the stalk with that of the primary vesicle.

The line z z, through which the section shewn in fig. 288 F is supposed to be taken, passes through the choroidal fissure.]

With reference to the above description, taken with very slight alterations from the Elements of Embryology, Pt. 1., two points require to be noticed. Firstly it is extremely doubtful whether the invagination of the secondary optic vesicle is to be viewed as an actual mechanical result of the ingrowth of the lens. Secondly it seems probable that the choroid fissure is not simply due to an inequality in the growth of the walls of the secondary optic cup, but is partly due to a doubling up of the primary vesicle from the side along the line of the fissure, at the same time that the lens is being thrust in in front. In Mammalia, the doubling up involves the optic stalk, which becomes flattened (whereby its original cavity is obliterated) and then folded in on itself, so as to embrace a new central cavity continuous with the cavity of the vitreous humour. And in other forms a partial phenomenon of the same kind is usually observable, as is more particularly described in the sequel.

Before describing the development of the cornea, aqueous humour, etc. we may consider the further growth of the parts, whose first development has just been described, commencing with the optic cup.

During the above changes the mesoblast surrounding the optic cup assumes the character of a distinct investment, whereby the outline of the eyeball is definitely formed. The internal portions of this investment, nearest to the retina, become the choroid (i.e. the chorio-capillaris, and the lamina fusca; the pigment epithelium, as we have seen, being derived from the epiblastic optic cup), and pigment is subsequently deposited in it. The remaining external portion of the investment forms the sclerotic.

The complete differentiation of these two coats of the eye does not however take place till a late period.

The cavity of the original optic vesicle was left as a nearly obliterated space between the two walls of the optic cup. By the end of the third day the obliteration is complete, and the two walls are in immediate contact.

The inner or anterior wall is, from the first, thicker than the outer or posterior; and over the greater part of the cup this contrast increases with the growth of the eye, the anterior wall becoming markedly thicker and undergoing changes of which we shall have to speak directly (fig. 289).

In the front portion however, along, so to speak, the lip of the cup, anterior to a line which afterwards becomes the ora serrata, both layers cease to take part in the increased thickening, accompanied by peculiar histological changes, which the rest of the cup is undergoing. Thus a hind portion or true retina is marked off from a front portion.

The front portion, accompanied by the mesoblast which immediately overlies it, is behind the lens thrown into folds, the ciliary ridges; while further forward it bends in between the lens and the cornea to form the iris. The original wide opening of the optic cup is thus narrowed to a smaller orifice, the pupil; and the lens, which before lay in the open mouth of the cup, is now inclosed in its cavity. While in the hind portion of the cup or retina proper no deposit of black pigment takes place in the layer formed out of the inner or anterior wall of the vesicle; in the front portion forming the region of the iris, pigment is largely deposited throughout both layers, though first of all in the outer one, so that eventually this portion seems to become nothing more than a forward prolongation of the pigment epithelium of the choroid.

[FIG. 288.

D. Diagrammatic section taken perpendicular to the plane of the paper, along the line yy, fig. 287. The stalk is not seen, the section falling quite out of its region. vh. hollow of optic cup filled with vitreous humour; other letters as in fig. 285 B. (After Remak.)

E. Section taken parallel to the plane of the paper through fig. 287, so far behind the front surface of the eye as to shave off a small portion of the posterior surface of the lens l, but not so far behind as to be carried at all through the stalk. Letters as before; f. the choroidal fissure.

F. Section along the line zz, perpendicular to the plane of the paper, to shew the choroidal fissure f, and the continuity of the cavity of the optic stalk with that of the primary optic vesicle. Had this section been taken a little to one side of the line zz, the wall of the optic cup would have extended up to the lens below as well as above. Letters as before. The external epiblast is omitted in this section.]

Thus, while the hind moiety of the optic cup becomes the retina proper, including the choroid-pigment in which the rods and cones are imbedded, the front moiety is converted into the ciliary portion of the retina, covering the ciliary processes, and into the uvea of the iris; the bodies of the ciliary processes and the substance of the iris, their vessels, muscles, connective tissue and ramified pigment, being derived from the mesoblastic choroid. The margin of the pupil marks the extreme lip of the optic vesicle, where the outer or posterior wall turns round to join the inner or anterior.

The ciliary muscle and the ligamentum pectinatum are both derived from the mesoblast between the cornea and the iris.

[FIG. 289. SECTION OF THE EYE OF CHICK AT THE FOURTH DAY.

e.p. superficial epiblast of the side of the head; R. true retina: anterior wall of the optic cup; p.Ch. pigment-epithelium of the choroid: posterior wall of the optic cup. b is placed at the extreme lip of the optic cup at what will become the margin of the iris. l. the lens. The hind wall, the nuclei of whose elongated cells are shewn at nl, now forms nearly the whole mass of the lens, the front wall being reduced to a layer of flattened cells el. m. the mesoblast surrounding the optic cup and about to form the choroid and sclerotic. It is seen to pass forward between the lip of the optic cup and the superficial epiblast.

Filling up a large part of the hollow of the optic cup is seen a hyaline mass, the rudiment of the hyaloid membrane, and of the coagulum of the vitreous humour, y. In the neighbourhood of the lens it seems to be continuous as at cl with the tissue a, which appears to be the rudiment of the capsule of the lens and suspensory ligament.]

The Retina. At first the two walls of the optic cup do not greatly differ in thickness. On the third day the outer or posterior becomes much thinner than the inner or anterior, and by the middle of the fourth day is reduced to a single layer of flattened cells (fig. 289, p.Ch). At about the 80th hour its cells commence to receive a deposit of pigment, and eventually form the so-called pigmentary epithelium of the choroid; from them no part of the true retina (or no other part of the retina, if the pigment-layer in question be supposed to belong more truly to the retina than to the choroid) is derived.

On the fourth day, the inner (anterior) wall of the optic cup (fig. 289, R) has a perfectly uniform structure, being composed of elongated somewhat spindle-shaped cells, with distinct nuclei. On its external (posterior) surface a distinct cuticular membrane, the membrana limitans externa, early appears.

As the wall increases in thickness, its cells multiply rapidly, so that it soon becomes several cells thick: each cell being however probably continued through the whole thickness of the layer. The wall at this stage corresponds closely in its structure with the brain, of which it may properly be looked upon as part. According to the usual view, which is not however fully supported by the development, the retina becomes divided in the subsequent growth into (1) an outer part, corresponding morphologically to the epithelial lining of the cerebrospinal canal, composed of what may be called the visual cells of the eye, i.e. the cells forming the outer granular (nuclear) layer and the rods and cones attached to them; and (2) an inner portion consisting of the inner granular (nuclear) layer, the inner molecular layer, the ganglionic layer and the layer of nerve-fibres corresponding morphologically to the walls of the brain. According to Löwe, however, only the outer limbs of the rods and cones, which he holds to be metamorphosed cells, correspond to the epithelial layer of the brain.

The actual development of the retina is not thoroughly understood. According to the usual statements (Kölliker, No. 298, p. 693) the layer of ganglion cells and the inner molecular layer are first differentiated, while the remaining cells give rise to the rest of the retina proper, and are bounded externally by the membrana limitans externa. On the inner side of the ganglionic layer the stratum of nerve-fibres is also very early established. The rods and cones are formed as prolongations (Kölliker, Babuchin), or cuticularizations (Schultze, W. Müller) of the cells which eventually form the outer granular layer. The layer of cells external to the molecular layer is not divided till comparatively late into the inner and outer granular (nuclear) layers, and the interposed outer molecular layer.

Löwe's account of the development of the retina in the Rabbit is in many points different from the above. He finds that three stages in the differentiation of the layers of the retina may be distinguished.

In the first stage, in an embryo of four or five millimetres, the following layers are present, commencing at the outer side, adjoining the external wall of the secondary optic cup.

(1) A membrane, which does not however, as usually believed, become the membrana limitans externa. (2) A layer of clear elements, derived from metamorphosed cells, constituting the outer limbs of the rods and cones. (3) A layer of dark rounded elements. (4) An indistinctly striated layer, the future layer of nerve-fibres.

The third of these layers gives rise to all the eventual strata of the retina proper, except the outer limbs of the rods and cones.

In the next stage, when the embryo has reached a length of 2 cm., this layer becomes divided into three strata: viz. an outer and inner layer of dark elements and a middle one of clearer elements. The two inner of these layers become respectively the inner molecular layer and the layer of ganglion cells, while the outer layer gives rise to the parts of the retina external to the inner molecular layer.

In the newly born animal the outer darker layer of the previous stage has become considerably subdivided. Its outermost part forms a stratum of darkly coloured elements, which develop into the inner limbs of the rods and cones. It is bounded internally by a membrane--the true membrana elastica externa. The part of the layer within this is soon divided into the outer and inner granular layers, separated from each other by the delicate outer molecular layer. Thus, shortly after birth, all the layers of the retina are established in the Rabbit. It is important to notice that, according to Löwe's views, the outer and inner limbs of the rods and cones are metamorphosed cells. The outer limbs at first form a continuous layer, in which separate elements cannot be recognised.

At a very early period there appears a membrane on the side of the retina adjoining the vitreous humour. This membrane is the hyaloid membrane. The investigations of Kessler and myself lead to the conclusion that it may be formed at a time when there is no trace of mesoblastic structures in the cavity of the vitreous humour, and that it is therefore necessarily developed as a cuticular deposit of the cells of the optic cup. Lieberkühn, Arnold, Löwe, and other authors regard it however as a mesoblastic product; and Kölliker believes that a primitive membrane is developed from the cells of the optic cup, and that a true hyaloid membrane is developed much later as a product of the mesoblast.

For fuller information on this subject the reader is referred to the authors quoted above.

The optic nerve. The optic nerves are derived, as we have said, from the at first hollow stalks of the optic vesicles. Their cavities gradually become obliterated by a thickening of the walls, the obliteration proceeding from the retinal end inwards towards the brain. While the proximal ends of the optic stalks are still hollow the rudiments of the optic chiasma are formed from fibres at the roots of the stalks, the fibres of the one stalk growing over into the attachment of the other. The decussation of the fibres would appear to be complete. The fibres arise in the remainder of the nerves somewhat later. At first the optic nerve is equally continuous with both walls of the optic cup; as must of necessity be the case, since the interval which primarily exists between the two walls is continuous with the cavity of the stalk. When the cavity within the optic nerve vanishes, and the fibres of the optic nerve appear, all connection is ruptured between the outer wall of the optic cup and the optic nerve, and the optic nerve simply perforates the outer wall, and becomes continuous with the inner one.

There does not appear to me any ground for doubting (as has been done by His and Kölliker) that the fibres of the optic nerve are derived from a differentiation of the epithelial cells of which the nerve is at first formed.

Choroid Fissure. With reference to the choroid fissure we may state that its behaviour varies somewhat in the different types. It becomes for the greater part of its extent closed, though its proximal end is always perforated by the optic nerve, and in many forms by a mesoblastic process also.

The lens when first formed is an oval vesicle with a small central cavity, the front and hind walls being of nearly equal thickness, and each consisting of a single layer of elongated columnar cells. In the subsequent stages the mode of growth of the hind wall is of precisely an opposite character to that of the front wall. The hind wall becomes much thicker, and tends to obliterate the central cavity by becoming convex on its front surface. At the same time its cells, still remaining as a single layer, become elongated and fibre-like. The front wall on the contrary becomes thinner and thinner and its cells flattened.

These modes of growth continue until, as shewn in fig. 289, the hind wall l is in absolute contact with the front wall el, and the cavity thus becomes entirely obliterated. The cells of the hind wall have by this time become veritable fibres, which, when seen in section, appear to be arranged nearly parallel to the optic axis, their nuclei nl being seen in a row along their middle. The front wall, somewhat thickened at either side where it becomes continuous with the hind wall, is now a single layer of flattened cells separating the hind wall of the lens, or as we may now say the lens itself, from the front limb of the lens-capsule; of the latter it becomes the epithelium.

The subsequent changes undergone consist chiefly in the continued elongation and multiplication of the lens-fibres, with the partial disappearance of their nuclei.

During their multiplication they become arranged in the manner characteristic of the adult lens of the various forms. The lens-capsule, as was originally stated by Kölliker, appears to be formed as a cuticular membrane deposited by the epithelial cells of the lens.

The views of Lieberkühn, Arnold, Löwe and others, according to which the lens-capsule is a mesoblastic structure, do not appear to be well founded. The contrary view, held by Kölliker, Kessler, etc., is supported mainly by the fact that at the time when the lens-capsule first appears there are no mesoblast cells to give rise to it. It should however be stated that W. Müller has actually found cellular elements in what he believes to be the lens-capsule of the Ammocoete lens. Considering the degraded character of the Ammocoete eye, evidence derived from its structure must be accepted with caution.

The vitreous humour. The vitreous humour is derived (except in Cyclostomata) from a vascular ingrowth, which differs considerably in different types, through the choroid slit. Its real nature is very much disputed. According to Kessler's view, it is of the nature of a fluid transudation, but the occasional presence in it of ordinary embryonic mesoblast cells, in addition to more numerous blood-corpuscles, gives it a claim to be regarded as intercellular substance. The number of cells in it is however at best extremely small and in many cases there is no trace of them. In Mammals there appear to be some mesoblast cells invaginated with the lens, which are not improbably employed in the formation of the vessels of the so-called membrana capsulo-pupillaris. In the Ammocoete the vitreous humour originates from a distinct mesoblastic ingrowth, though the cells which give rise to it subsequently disappear.

The development of the zonula of Zinn in Mammalia, which ought to throw some light on the nature of the vitreous humour, has not been fully investigated. According to Lieberkühn (No. 373, p. 43), this structure appears in half-grown embryos of the sheep and calf.

He says "At the point where the ciliary processes and the ciliary part of the retina are entirely removed, one sees in the meridian bundles of fine fibres, which correspond to the valleys between the ciliary processes and fill them; also between these bundles there extend, as a thin layer, similar finely striated masses, and these would have been on the top of the ciliary processes." He further states that these fibres may be traced to the anterior and posterior limb of the lens-capsule, and that amongst them are numerous cells. Kölliker confirms Lieberkühn's statements. There can be little doubt that the fibres of the zonula are of the nature of connective tissue: they are stated to be elastic. By Löwe they are believed to be developed out of the substance of the vitreous humour, but this does not appear to me to follow from the observations hitherto made. It seems quite possible that they arise from mesoblast cells which have grown into the cavity of the vitreous humour, solely in connection with their production.

The integral parts of the eye in front of the lens are the cornea, the aqueous humour, and the iris. The development of the latter has already been described, and there remain to be dealt with the cornea, and the cavity containing the aqueous humour.

The cornea. The cornea is formed by the coalescence of two structures, viz. the epithelium of the cornea and the cornea proper. The former is directly derived from the external epiblast, which covers the eye after the invagination of the lens. The latter is formed in a somewhat remarkable manner, first clearly made out by Kessler.

[FIG. 290. SECTION THROUGH THE EYE OF A FOWL ON THE EIGHTH DAY OF DEVELOPMENT, TO SHEW THE IRIS AND CORNEA IN THE PROCESS OF FORMATION. (After Kessler.)

ep. epiblastic epithelium of cornea; cc. corneal corpuscles growing into the structureless matrix of the cornea; dm. Descemet's membrane; ir. iris; cb. mesoblast of the iris (this reference letter points a little too high).

The space between the layers dm. and ep. is filled with the structureless matrix of the cornea.]

When the lens is completely separated from the epidermis its outer wall is directly in contact with the external epiblast (future corneal epithelium). At its edge there is a small ring-shaped space bounded by the outer skin, the lens and the edge of the optic cup. In the chick, which we may take as typical, there appears at about the time when the cavity of the lens is completely obliterated a structureless layer external to the above ring-like space and immediately adjoining the inner face of the epiblast. This layer, which forms the commencement of the cornea proper, at first only forms a ring at the border of the lens, thickest at its outer edge, and gradually thinning off to nothing towards the centre. It soon however becomes broader, and finally forms a continuous stratum of considerable thickness, interposed between the external skin and the lens. As soon as this stratum has reached a certain thickness, a layer of flattened cells grows in along its inner side from the mesoblast surrounding the optic cup (fig. 290, dm). This layer is the epithelioid layer of the membrane of Descemet. After it[190] has become completely established, the mesoblast around the edge of the cornea becomes divided into two strata; an inner one (fig. 290, cb) destined to form the mesoblastic tissue of the iris already described, and an outer one (fig. 290, cc) adjoining the epidermis. The outer stratum gives rise to the corneal corpuscles, which are the only constituents of the cornea not yet developed. The corneal corpuscles make their way through the structureless corneal layer, and divide it into two strata, one adjoining the epiblast, and the other adjoining the inner epithelium. The two strata become gradually thinner as the corpuscles invade a larger and larger portion of their substance, and finally the outermost portion of them alone remains as the membrana elastica anterior and posterior (Descemet's membrane) of the cornea. The corneal corpuscles, which have grown in from the sides, thus form a layer which becomes continually thicker, and gives rise to the main substance of the cornea. Whether the increase in the thickness of the layer is due to the immigration of fresh corpuscles, or to the division of those already there, is not clear. After the cellular elements have made their way into the cornea, the latter becomes continuous at its edge with the mesoblast which forms the sclerotic.

[190] It appears to me possible that Lieberkühn may be right in stating that the epithelium of Descemet's membrane grows in between the lens and the epiblast before the formation of the cornea proper, and that Kessler's account, given above, may on this point require correction. From the structure of the eye in the Ammocoete it seems probable that Descemet's membrane is continuous with the choroid.

The derivation of the original structureless layer of the cornea is still uncertain. Kessler derives it from the epiblast, but it appears to me more probable that Kölliker is right in regarding it as derived from the mesoblast. The grounds for this view are, (1) the fact of its growth inwards from the border of the mesoblast round the edge of the eye, (2) the peculiar relations between it and the corneal corpuscles at a later period. This view would receive still further support if a layer of mesoblast between the lens and the epiblast were really present as believed by Lieberkühn. It must however be admitted that the objections to Kessler's view of its epiblastic nature are rather a priori than founded on definite observation.

The observations of Kessler, which have been mainly followed in the above account, are strongly opposed by Lieberkühn (No. 374) and Arnold (No. 370), and are not entirely accepted by Kölliker. It is especially on the development of these parts in Mammalia (to be spoken of in the sequel) that the above authors found their objections. I have had through Kessler's kindness an opportunity of looking through some of his beautiful preparations, and have no hesitation in generally accepting his conclusions, though as mentioned above I cannot agree with all his interpretations.

The aqueous humour. The cavity for the aqueous humour has its origin in the ring-shaped space round the front of the lens, which, as already mentioned, is bounded by the external skin, the edge of the optic cup, and the lens. By the formation of the cornea this space is shut off from the external skin, and on the appearance of the epithelioid layer of Descemet's membrane a continuous cavity is developed between the cornea and the lens. This cavity enlarges and receives its final form on the full development of the iris.

Comparative view of the development of the Vertebrate Eye.

The organ of vision, when not secondarily aborted, contains in all Vertebrata the essential parts above described. The most interesting cases of partial degeneration are those of Myxine and the Ammocoete. The development of such aborted eyes has as yet been studied only in the Ammocoete[191], in which it resembles in most important features that of other Vertebrata.

[191] The most detailed account is that of W. Müller (No. 377).

[FIG. 291. HORIZONTAL SECTION THROUGH THE HEAD OF A JUST HATCHED LARVA OF PETROMYZON SHEWING THE DEVELOPMENT OF THE LENS OF THE EYE.

th.c. thalamencephalon; op.v. optic vesicle; l. lens of eye; h.c. head cavity.]

Eye of Ammocoetes. The optic vesicle arises as an outgrowth of the fore-brain, but the secondary optic cup is remarkable in the young larva for its small size (fig. 291, opv). The thicker outer wall gives rise to the retina, and the thinner inner wall to the choroid pigment. The lens is formed as an invagination of the single-layered epidermis (fig. 291, l). As development proceeds the parts of the eye gradually enlarge, and the mesoblast around the hinder and dorsal part of the optic cup becomes pigmented. There is at first no cavity for the vitreous humour, but eventually the growth of the optic cup gives rise to a space, into which a cellular process of mesoblast grows at a slight notch in the ventral edge of the optic cup (W. Müller, No. 377). This notch is the only rudiment of the choroid fissure of other types. The mesoblastic process is probably the homologue of the processus falciformis and pecten, and appears to give rise to the vitreous humour; for a long time it retains its connection with the surrounding mesoblast. Its cells eventually disappear, and it never contains any vascular structures.

The lens for a long time remains as an oval vesicle with a central cavity. In a later stage, when the Ammocoete is fully developed, the secondary optic cup forms a deep pit (fig. 292, r); in the mouth of which is placed the lens (l). The two walls of the retina have now the normal vertebrate structure, though the pigment is as yet imperfectly present in the choroid layer. The lens has the embryonic forms of higher types (cf. fig. 289), consisting of an inner thicker segment, the true lens, and an outer layer forming the epithelium of the lens capsule. The edge of the optic cup, which forms the rudiment of the epiblast of the iris, is imperfectly separated from the remainder of the optic cup; and a mesoblastic element of the iris, distinct from Descemet's membrane (dm), can hardly be spoken of.

There is no cavity for the aqueous humour in front of the lens; and there is no cornea as distinct from the epidermis and subepidermic tissues. The elements in front of the lens are (1) the epidermis (ep); (2) the dermis (dc); (3) the subdermal connective tissue (sdc) which passes without any sharp line of demarcation into the dermis; (4) a thick membrane, continuous with the mesoblastic part of the choroid, which appears to represent Descemet's membrane. The subdermal connective tissue is continued as an investment round the whole eye; and there is no differentiated sclerotic and only an imperfect choroid.

In a still later stage a distinct mesoblastic element for the iris is formed. When the Ammocoete is becoming a Lamprey, the eye approaches the surface; an anterior chamber is established; and the eye differs from that of the higher types mainly in the fact that the cornea is hardly distinguished from the remainder of the skin, and that a sclerotic is very imperfectly represented.

Optic vesicles. The development of the primitive optic vesicles, so far as is known, is very constant throughout the Vertebrata. In Teleostei and Lepidosteus alone is there an important deviation from the ordinary type, dependent however upon the mode of formation of the medullary keel, the optic vesicles arising while the medullary keel is still solid, and being at first also solid. They subsequently acquire a lumen and undergo the ordinary changes.

[FIG. 292. EYE OF AN AMMOCOETES LYING BENEATH THE SKIN.

ep. epidermis; d.c. dermal connective tissue continuous with the subdermal connective tissue (s.d.c), which is also shaded. There is no definite boundary to this tissue where it surrounds the eye.

m. muscles; dm. membrane of Descemet; l. lens; v.h. vitreous humour; r. retina; rp. retinal pigment.]

The lens. In the majority of groups, viz. Elasmobranchii, Reptilia, Aves, and Mammalia, the lens is formed by an open invagination of the epiblast, but in Amphibia, Teleostei and Lepidosteus, where the nervous layer of the skin is early established, this layer alone takes part in the formation of the lens (fig. 293, l). The lens is however formed even in these types as a hollow body by an invagination; but its opening remains permanently shut off from communication with the exterior by the epidermic layer of the epiblast. Götte describes the lens as formed by a solid thickening of the nervous layer in Bombinator. This is probably a mistake.

The cornea. The mode of formation of the cornea already described appears to be characteristic of most Vertebrata except the Ammocoete. It has been found by Kessler in Aves, Reptilia and Amphibia, and probably also occurs in Pisces. In Mammals it is not however so easy to establish. There are at first no mesoblast cells between the lens and the epiblast (fig. 295) but in many Mammals (vide Kessler, No. 372, pp. 91-94) a layer of rounded mesoblast cells, which forms Descemet's membrane, grows in between the two, at a time when it is not easy to recognise a corneal lamina, as distinct from a simple coagulum.

After the formation of this layer the mesoblast cells grow into the corneal lamina from the sides, and becoming flattened arrange themselves in rows between the laminæ of the cornea. The cornea continues to increase in thickness by the addition of laminæ on the side adjoining the epiblast.

We have already seen that in the Lamprey the cornea is nothing else but the slightly modified and more transparent epidermis and dermis.

The optic nerve and the choroid fissure. It will be convenient to consider together the above structures, and with them the vascular and other processes which pass into the cavity of the optic cup through the choroid fissure. These parts present on the whole a greater amount of variation than any other parts of the eye.

I commence with the Fowl which is both a very convenient general type for comparison, and also that in which these structures have been most fully worked out.

During the third day of incubation there passes in through the choroid slit a vascular loop, which no doubt supplies the transuded material for the growth of the vitreous humour. Up to the fifth day this vascular loop is the only structure passing through the choroid slit. On this day however a new structure appears, which remains permanently through life, and is known as the pecten. It consists of a lamellar process of the mesoblast cells round the eye, passing through the choroid slit near the optic nerve, and enveloping part of the afferent branch of the vascular loop above mentioned. The proximal part of the free edge of the pecten is somewhat swollen, and sections through this part have a club-shaped form. On the sixth day the choroid slit becomes rapidly closed, so that at the end of the sixth day it is reduced to a mere seam. There are however two parts of this seam where the edges of the optic cup have not coalesced. The proximal of these adjoins the optic nerve, and permits the passage of the pecten and at a later period of the optic nerve; and the second or distal one is placed near the ciliary edge of the slit, and is traversed by the efferent branch of the above-mentioned vascular loop. This vessel soon atrophies, and with it the distal opening in the choroid slit completely vanishes. In some varieties of domestic Fowl (Lieberkühn) the opening however persists. The seam which marks the original site of the choroid slit is at first conspicuous by the absence of pigment, and at a later period by the deep colour of its pigment. Finally, a little after the ninth day, no trace of it is to be seen.

[FIG. 293. SECTION THROUGH THE FRONT PART OF THE HEAD OF A LEPIDOSTEUS EMBRYO ON THE SEVENTH DAY AFTER IMPREGNATION.

al. alimentary tract; fb. thalamencephalon; l. lens of eye; op.v. optic vesicle. The mesoblast is not represented.]

Up to the eighth day the pecten remains as a simple lamina; by the tenth or twelfth day it begins to be folded or rather puckered, and by the seventeenth or eighteenth day it is richly pigmented and the puckerings have become nearly as numerous as in the adult, there being in all seventeen or eighteen. The pecten is almost entirely composed of vascular coils, which are supported by a sparse pigmented connective tissue; and in the adult the pecten is still extremely vascular. The original artery which became enveloped at the formation of the pecten continues, when the latter becomes vascular, to supply it with blood. The vein is practically a fresh development after the atrophy of the distal portion of the primitive vascular loop of the vitreous humour.

There are no true retinal blood-vessels.

In the formation of the optic cup the extreme peripheral part of the optic nerve, which is in immediate proximity with the artery of the pecten, becomes folded. The permanent opening in the choroid fissure for the pecten is intimately related to the entrance of the optic nerve into the eyeball; the fibres of the optic nerve passing in at the inner border of the pecten, coursing along its sides to its outer border, and radiating from it as from a centre to all parts of the retina.

In the Lizard the choroid slit closes considerably earlier than in the Fowl. The vascular loop in the vitreous humour is however more developed. The pecten long remains without vessels, and does not in fact become at all vascular till after the very late disappearance of the distal part of the vascular loop of the vitreous humour.

The arrangement of the ingrowth through the choroid slit in Elasmobranchii (Scyllium) has been partially worked out, and so far as is at present known the agreement between the Avian and Elasmobranch type is fairly close.

At the time when the cavity between the lens and the secondary optic cup is just commencing to be formed, a process of mesoblast accompanied by a vascular loop passes into the vitreous humour, through the choroid slit, close to the optic nerve. The vessel in this process is no doubt equivalent to the vascular loop in the Avian eye, but I have not made out that it projects beyond the mesoblastic process accompanying it. As the cavity of the vitreous humour enlarges and the choroid slit elongates, the process through it takes the form of a lamina with a somewhat swollen border, and projects for some distance into the cavity of the vitreous humour.

At a later stage, after the outer layer of the optic cup has become pigmented, the distal part of the choroid slit adjoining the border of the lens closes up; but along the line where it was present the walls of the optic cup remain very thin and are thrown into three folds, two lateral and one median, projecting into the cavity of the vitreous humour. The median fold is in contact with the lens, and the vascular mesoblast surrounding the eye projects into the space between the two laminæ of which it is formed. In passing from the region of the lens to that of the optic nerve the lateral folds of the optic cup disappear, and the median fold forms a considerable projection into the cavity of the vitreous humour. It consists of a core of mesoblast covered by a delicate layer derived from both strata of the optic cup. Still nearer the optic nerve the choroid slit is no longer closed, and the mesoblast, which in the neighbourhood of the lens only extended into the folds of the wall of the optic cup, now projects freely into the cavity of the vitreous humour, and forms the lamina already described. It is not very vascular, but close to the optic nerve there passes into it a considerable artery.

In the young animal the choroid slit is no longer perforated by a mesoblastic lamina. At its inner end it remains open to allow of the passage of the optic nerve. The line of the slit can easily be traced along the lower side of the retina; and close to the lens the retinal wall continues, as in the embryo, to be raised into a projecting fold. Traces of these structures are visible even in the fully grown examples of Scyllium.

As has been pointed out by Bergmeister the mesoblastic lamina projecting into the vitreous humour resembles the pecten at an early stage of development, and is without doubt homologous with it. The artery which supplies it is certainly equivalent to the artery of the pecten.

There can be no doubt that the mesoblastic lamina projecting into the vitreous humour is equivalent to the processus falciformis of Teleostei, and it seems probable that the whole of it, including the free part as well as that covered by epiblast, ought to be spoken of under this title. The optic nerve in Elasmobranchii is not included in the folding to which the secondary optic vesicle owes its origin, and would seem to perforate the walls of the optic cup only at the distal end of the processus falciformis.

[FIG. 294. HORIZONTAL SECTION THROUGH THE EYE OF A TELEOSTEAN EMBRYO. (From Gegenbaur; after Schenk.)

s. choroid fissure, with two folds forming part of the processus falciformis; a. choroid layer of optic cup; b. retinal layer of optic cup; c. cavity of vitreous humour; d. lens.]

In Teleostei there is at first a vascular loop like that in Birds, passing through the choroid fissure. This has been noticed by Kessler in the Pike, and by Schenk in the Trout. At a later period a mesoblastic ingrowth with a blood-vessel makes its way in many forms into the cavity of the vitreous humour, accompanied by two folds in the walls of the free edges of the choroid fissure (fig. 294). These structures, which constitute the processus falciformis, clearly resemble very closely the mesoblastic process and folds of the optic cup in Elasmobranchii. The processus falciformis comes in contact with, and perhaps becomes attached to the wall of the lens; and persists through life.

In Triton there is no vascular ingrowth through the choroid fissure, but a few mesoblastic cells pass in which represent the vascular ingrowth of other types. The optic nerve perforates the proximal extremity of the original choroid slit.

The absence of an embryonic blood-vessel does not however hold good for all Amphibia, as there is present in the embryo Alytes (Lieberkühn) an artery, which breaks up into a capillary system on the retinal border of the vitreous humour.

In the Ammocoete the choroid slit is merely represented by a slight notch on the ventral edge of the optic cup, and the mesoblastic process which passes through the choroid slit in most types is represented by a large cellular process, from which the vitreous humour would appear to be derived.

Mammalia differ from all the types already described in the immense foetal development of the blood-vessels of the vitreous humour. There are however some points in connection with the development of these vessels which are still uncertain. The most important of these points concerns the presence of a prolongation of the mesoblast around the eye into the cavity of the vitreous humour. It is maintained by Lieberkühn, Arnold, Kölliker, etc., that in the invagination of the lens a thin layer of mesoblast is carried before it; and is thus transported into the cavity of the vitreous humour. This is denied by Kessler, but the layer is so clearly figured by the above embryologists, that the existence of it in some Mammalia (the Rabbit, etc.) must I think be accepted.

In the folding in of the optic vesicle, which accompanies the formation of the lens, the optic nerve becomes included, and on the development of the cavity of the vitreous humour an artery, running in the fold of the optic nerve, passes through the choroid slit into the cavity of the vitreous humour (fig. 295, acr). The sides of the optic nerve subsequently bend over, and completely envelope this artery, which at a later period gives off branches to the retina, and becomes known as the arteria centralis retinæ. It is homologous with the arterial limb of the vascular loop projecting into the vitreous humour in Birds, Lizards, Teleostei, etc.

[FIG. 295. SECTION THROUGH THE EYE OF A RABBIT EMBRYO OF ABOUT TWELVE DAYS..

c. epithelium of cornea; l. lens; mec. mesoblast growing in from the side to form the cornea; rt. retina; a.c.r. arteria centralis retinæ; of.n. optic nerve.

The figure shews (1) the absence at this stage of mesoblast between the lens and the epiblast: the interval between the two has however been made too great; (2) the arteria centralis retinæ forming the vascular capsule of the lens and continuous with vascular structures round the edges of the optic cup.]

Before becoming enveloped in the optic nerve this artery is continued through the vitreous humour (fig. 295), and when it comes in close proximity to the lens it divides into a number of radiating branches, which pass round the edge of the lens, and form a vascular sheath which is prolonged so as to cover the anterior wall of the lens. In front of the lens they anastomose with vessels, coming from the iris, many of which are venous (fig. 295)--and the whole of the blood from the arteria centralis is carried away by these veins. The vascular sheath surrounding the lens receives the name of the membrana capsulo-pupillaris. The posterior part of it appears (Kessler, No. 372) to be formed of vessels without the addition of any other structures and is either formed simply by branches of the arteria centralis, or out of the mesoblast cells involuted with the lens. The anterior part of the vascular sheath is however inclosed in a very delicate membrane, the membrana pupillaris, continuous at the sides with the epithelium of Descemet's membrane. On the formation of the iris this membrane lies superficially to it, and forms a kind of continuation of the mesoblast of the iris over the front of the lens.

The origin of this membrane is much disputed. By Kessler, whose statements have been in the main followed, it is believed to appear comparatively late as an ingrowth of the stroma of the iris; while Kölliker believes it to be derived from a mesoblastic ingrowth between the front wall of the lens and the epiblast. According to Kölliker this ingrowth subsequently becomes split into two laminæ, one of which forms the cornea, and the other the anterior part of the vascular sheath of the lens with its membrana pupillaris. Between the two appears the aqueous humour.

The membrana capsulo-pupillaris is simply a provisional embryonic structure, subserving the nutrition of the lens. The time of its disappearance varies somewhat for the different Mammalia in which this point has been investigated. In the human embryo it lasts from the second to the seventh month and sometimes longer. As a rule it is completely absorbed at the time of birth. The absorption of the anterior part commences in the centre and proceeds outwards.

In addition to the vessels of the vascular capsule round the lens, there arise from the arteria centralis retinæ, just after its exit from the optic nerve, in many forms (Dog, Cat, Calf, Sheep, Rabbit, Man) provisional vascular branches which extend themselves in the posterior part of the vitreous humour. Near the ciliary end of the vitreous humour they anastomose with the vessels of the membrana capsulo-pupillaris.

In Mammals the choroid slit closes very early, and is not perforated by any structure homologous with the pecten. The only part of the slit which remains open is that perforated by the optic nerve; and in the centre of the latter is situated the arteria centralis retinæ as explained above. From this artery there grow out the vessels to supply the retina, which have however nothing to do with the provisional vessels of the vitreous humour just described (Kessler). On the atrophy of the provisional vessels the whole of the blood of the arteria centralis passes into the retina.

It is interesting to notice (Kessler, No. 372, p. 78) that there seems to be a blood-vessel supplying the vitreous humour in the embryos of nearly all vertebrate types, which is homologous throughout the Vertebrata. This vessel often exhibits a persisting and a provisional part. The latter in Mammalia is the membrana capsulo-pupillaris and other vessels of the vitreous humour; in Birds and Lizards it is the part of the original vascular loop, not included in the pecten, and in Osseous Fishes that part (?) not involved in the processus falciformis. The permanent part is formed by the retinal vessels of Mammalia, by the vessels of the pecten in Birds and Lizards, and by those of the processus falciformis in Fishes.

The Iris and Ciliary processes. The walls of the edge of the optic cup become very much thinner than those of the true retinal part. In many Vertebrates (Mammalia, Aves, Reptilia, Elasmobranchii, etc.) the thinner part, together with the mesoblast covering it, becomes divided into two regions, viz. that of the iris, and that of the ciliary processes. In the Newt and Lamprey this differentiation does not take place, but the part in question simply becomes the iris.

Accessory Organs connected with the Eye.

Eyelids. The most important accessory structures connected with the eye are the eyelids. They are developed as simple folds of the integument with a mesoblastic prolongation between their two laminæ. They may be three in number, viz. an upper and lower, and a lateral one--the nictitating membrane--springing from the inner or anterior border of the eye. Their inner face is lined by a prolongation of conjunctiva, which is the modified epiblast covering the cornea and part of the sclerotic.

In Teleostei and Ganoidei eyelids are either not present or at most very rudimentary. In Elasmobranchii they are better developed, and the nictitating membrane is frequently present. The latter is also usually found in Amphibia. In the Sauropsida all three eyelids are usually present, but in Mammalia the nictitating membrane is rudimentary.

In many Mammalia the two eyelids meet together during a period of embryonic life, and unite in front of the eye. A similar arrangement is permanent through life in Ophidia and some Lacertilia; and there is a chamber formed between the coalesced eyelids and the surface of the cornea, into which the lacrymal ducts open.

Lacrymal glands. Lacrymal glands are found in the Sauropsida and Mammalia. They arise (Remak, Kölliker) as solid ingrowths of the conjunctival epithelium. They appear in the chick on the eighth day.

Lacrymal duct. The lacrymal duct first appears in Amphibia, and is present in all the higher Vertebrates. Its mode of development in the Amphibia, Lacertilia and Aves has recently been very thoroughly worked out by Born (Nos. 380 and 381).

In Amphibia he finds that the lacrymal duct arises as a solid ridge of the mucous layer of the epidermis, continued from the external opening of the nasal cavity backwards towards the eye. It usually appears at about the time when the nasal capsule is beginning to be chondrified. As this ridge is gradually prolonged backwards towards the eye its anterior end becomes separated from the epidermis, and grows inwards in the mesoblast to become continuous with the posterior part of the nasal sack. The posterior end which joins the eye becomes divided into the two collecting branches of the adult. Finally the whole structure becomes separated from the skin except at the external opening, and develops a lumen.

In Lacertilia the lacrymal duct arises very much in the same manner as in Amphibia, though its subsequent growth is somewhat different. It appears as an internal ridge of the epithelium, at the junction of the superior maxillary process and the fold which gives rise to the lower eyelid. A solid process of this ridge makes its way through the mesoblast on the upper border of the maxillary process till it meets the wall of the nasal cavity, with the epithelium of which it becomes continuous. At a subsequent stage a second solid growth from the upper part of the epithelial ridge makes its way through the lower eyelid, and unites with the inner epithelium of the eyelid; and at a still later date a third growth from the lower part of the structure forms a second junction with the epithelium of the eyelid. The two latter outgrowths form the two upper branches of the duct. The ridge now loses its connection with the external skin, and, becoming hollow, forms the lacrymal duct. It opens at two points on the inner surface of the eyelid, and terminates at its opposite extremity by opening into the nasal cavity. It is remarkable, as pointed out by Born, that the original epithelial ridge gives rise directly to a comparatively small part of the whole duct.

In the Fowl the lacrymal duct is formed as a solid ridge of the epidermis, extending along the line of the so-called lacrymal groove from the eye to the nasal pit (fig. 120). At the end of the sixth day it begins to be separated from the epidermis, remaining however united with it on the inner side of the lower eyelid. After its separation from the epidermis it forms a solid cord, the lower end of which unites with the wall of the nasal cavity. The cord so formed gives rise to the whole of the duct proper and to the lower branch of the collecting tube. The upper branch of the collecting tube is formed as an outgrowth from this cord. A lumen begins to be formed on the twelfth day of incubation, and first appears at the nasal end. It arises by the formation of a space between the cells of the cord, and not by an absorption of the central cells.

In Mammalia Kölliker states that he has been unable to observe anything similar to that described by Born in the Sauropsida and Amphibia, and holds to the old view, originally put forward by Coste, that the duct is formed by the closure of a groove leading from the eye to the nose between the outer nasal process and the superior maxillary process. The upper extremity of the duct dilates to form a sack, from which two branches pass off to open on the lacrymal papillæ. In view of Born's discoveries Kölliker's statements must be received with some caution.

The Eye of the Tunicata.

The unpaired eye of the larva of simple Ascidians is situated somewhat to the right side of the posterior part of the dorsal wall of the anterior cephalic vesicle (fig. 296, O). It consists of a refractive portion, turned towards the cavity of the vesicle of the brain, and a retinal portion forming part of the wall of the brain. The refractive parts consist of a convex-concave meniscus in front, and a spherical lens behind, adjoining the concave side of the meniscus. The posterior part of this lens is imbedded in a layer of pigment. The retina is formed of columnar cells, with their inner ends imbedded in the pigment which encloses the posterior part of the lens. The retinal part of the eye arises in the first instance as a prominence of the wall of the cerebral vesicle: its cells become very columnar and pigmented at their inner extremities (fig. 8, V, a). The lens is developed at a later period, after the larva has become hatched, but the mode of its formation has not been made out.

[FIG. 296. LARVA OF ASCIDIA MENTULA. (From Gegenbaur; after Kupffer.) Only the anterior part of the tail is represented.

N´. anterior swelling of neural tube; N. anterior swelling of spinal portion of neural tube; n. hinder part of neural tube; ch. notochord; K. branchial region of alimentary tract; d. oesophageal and gastric region of alimentary tract; O. eye; a. otolith; o. mouth; s. papilla for attachment.]

General considerations on the Eye of the Chordata.

There can be but little doubt that the eye of the Tunicata belongs to the same phylum as that of the true Vertebrata, different as the two eyes are. The same may also be said with reference to the degenerate and very rudimentary eye of Amphioxus.

The peculiarity of the eye of all the Chordata consists in the retina being developed from part of the wall of the brain. How is this remarkable feature of the eye of the Chordata to be explained?

Lankester, interpreting the eye in the light of the Tunicata, has made the interesting suggestion[192] "that the original Vertebrate must have been a transparent animal, and had an eye or pair of eyes inside the brain, like that of the Ascidian Tadpole."

[192] Degeneration, London, 1880, p. 49.

This explanation may possibly be correct, but another explanation appears to me possible, and I am inclined to think that the vertebrate eyes have not been derived from eyes like those of Ascidians, but that the latter is a degenerate form of vertebrate eye.

The fact of the retina being derived from the fore-brain may perhaps be explained in the same way as has already been attempted in the case of the retina of the Crustacea; i.e. by supposing that the eye was evolved simultaneously with the fore part of the brain.

The peculiar processes which occur in the formation of the optic vesicle are more difficult to elucidate; and I can only suggest that the development of a primary optic vesicle, and its conversion into an optic cup, is due to the retinal part of the eye having been involved in the infolding which gave rise to the canal of the central nervous system. The position of the rods and cones on the posterior side of the retina is satisfactorily explained by this hypothesis, because, as may be easily seen from figure 285, the posterior face of the retina is the original external surface of the epidermis, which is infolded in the formation of the brain; so that the rods and cones are, as might be anticipated, situated on what is morphologically the external surface of the epiblast of the retina.

The difficulty of this view arises in attempting to make out how the eye can have continued to be employed during the gradual change of position which the retina must have undergone in being infolded with the brain in the manner suggested. If however the successive steps in this infolding were sufficiently small, it seems to me not impossible that the eye might have continued to be used throughout the whole period of change, and a transparency of the tissues, such as Lankester suggests, may have assisted in rendering this possible.

The difficulty of the eye continuing to be in use when undergoing striking changes in form is also involved in Lankester's view, in that if, as I suppose, he starts from the eye of the Ascidian Tadpole with its lenses turned towards the cavity of the brain; it is necessary for him to admit that a fresh lens and other optical parts of the eye became developed on the opposite side of the eye to the original lens; and it is difficult to understand such a change, unless we can believe that the refractive media on the two sides were in operation simultaneously. It may be noted that the same difficulty is involved in supposing, as I have done, that the eye of the Ascidian Tadpole was developed from that of a Vertebrate. I should however be inclined to suggest that the eye had in this case ceased for a period to be employed; and that it has been re-developed again in some of the larval forms. Its characters in the Tunicata are by no means constant.

Accessory eyes in the Vertebrata.

In addition to the paired eyes of the Vertebrata certain organs are found in the skin of a few Teleostei living in very deep water, which, though clearly not organs of true vision, yet present characters which indicate that they may be used in the perception of light. The most important of such organs are those found in Chauliodus, Stomias, etc., the significance of which was first pointed out by Leuckart, while the details of their structure have been recently worked out by Leydig[193] and Ussow. They are distributed not only in the skin, but are also present in the mouth and respiratory cavity, a fact which appears to indicate that their main function must be something else than the perception of light. It has been suggested that they have the function of producing phosphorescence.

Another organ, probably of the same nature, is found on the head of Scopelus.

The organs in Chauliodus are spherical or nearly spherical bodies invested in a special tunic. The larger of them, which alone can have any relation to vision, are covered with pigment except on their outer surface. The interior is filled with two masses, named by Leuckart the lens and vitreous humour. According to Leydig each of them is cellular and receives a nerve, the ultimate destination of which has not however been made out. According to Ussow the anterior mass is structureless, but serves to support a lens, placed in the centre of the eye, and formed of a series of crystalline cones prolonged into fibres, which in the posterior part of the eye diverge and terminate by uniting with the processes of multipolar cells, placed near the pigmented sheath. These cells, together with the fibres of the crystalline cones which pass to them, are held by Ussow to constitute a retina.

Eye of the Mollusca.

(362) N. Bobretzky. "Observations on the development of the Cephalopoda" (Russian). Nachrichten d. kaiserlichen Gesell. d. Freunde der Naturwiss. Anthropolog. Ethnogr. bei d. Universität Moskau.

(363) H. Grenacher. "Zur Entwicklungsgeschichte d. Cephalopoden." Zeit. f. wiss. Zool., Bd. XXIV. 1874.

(364) V. Hensen. "Ueber d. Auge einiger Cephalopoden." Zeit. f. wiss. Zool., Vol. XV. 1865.

(365) E. R. Lankester. "Observations on the development of the Cephalopoda." Quart. J. of Micr. Science, Vol. XV. 1875.

(366) C. Semper. Ueber Sehorgane von Typus d. Wirbelthieraugen. Wiesbaden, 1877.

Eye of the Arthropoda.

(367) N. Bobretzky. Development of Astacus and Palaemon. Kiew, 1873.

(368) A. Dohrn. "Untersuchungen üb. Bau u. Entwicklung d. Arthropoden. Palinurus und Scyllarus." Zeit. f. wiss. Zool., Bd. XX. 1870, p. 264 et seq.

(369) E. Claparède. "Morphologie d. zusammengesetzten Auges bei den Arthropoden." Zeit. f. wiss. Zool., Bd. X. 1860.

(370) H. Grenacher. Untersuchungen üb. d. Sehorgane d. Arthropoden. Göttingen, 1879.

Vertebrate Eye.

(371) J. Arnold. Beiträge zur Entwicklungsgeschichte des Auges. Heidelberg, 1874.

(372) Babuchin. "Beiträge zur Entwicklungsgeschichte des Auges." Würzburger naturwissenschaftliche Zeitschrift, Bd. 8.

(373) L. Kessler. Zur Entwicklung d. Auges d. Wirbelthiere. Leipzig, 1877.

(374) N. Lieberkühn. Ueber das Auge des Wirbelthierembryo. Cassel, 1872.

(375) N. Lieberkühn. "Beiträge z. Anat. d. embryonalen Auges." Archiv f. Anat. und Phys., 1879.

(376) L. Löwe. "Beiträge zur Anatomie des Auges" and "Die Histogenese der Retina." Archiv f. mikr. Anat., Vol. XV. 1878.

(377) V. Mihalkowics. "Untersuchungen über den Kamm des Vogelauges." Archiv f. mikr. Anat., Vol. IX. 1873.

(378) W. Müller. "Ueber die Stammesentwickelung des Schorgans der Wirbelthiere." Festgabe Carl Ludwig. Leipzig, 1874.

(379) S. L. Schenk. "Zur Entwickelungsgeschichte des Auges der Fische." Wiener Sitzungsberichte, Bd. LV. 1867.

Accessory organs of the Vertebrate Eye.

(380) G. Born. "Die Nasenhöhlen u. d. Thränennasengang d. Amphibien." Morphologisches Jahrbuch, Bd. II. 1876.

(381) G. Born. "Die Nasenhöhlen u. d. Thränennasengang d. amnioten Wirbelthiere. I. Lacertilia. II. Aves." Morphologisches Jahrbuch, Bd. V. 1879.

Eye of the Tunicata.

(382) A. Kowalevsky. "Weitere Studien üb. d. Entwicklung d. einfachen Ascidien." Archiv f. mikr. Anat., Vol. VII. 1871.

(383) C. Kupffer. "Zur Entwicklung d. einfachen Ascidien." Archiv f. mikr. Anat., Vol. VII. 1872.

[193] F. Leydig. "Ueber Nebenaugen d. Chauliodus Sloani." Archiv f. Anat. und Phys., 1879. M. Ussow. "Ueb. d. Bau d. augenähnlichen Flicken einiger Knochenfische." Bul. d. la Soc. d. Naturalistes de Moscou, Vol. LIV. 1879. Vide for general description and further literature, Günther, The Study of Fishes, Edinburgh, 1880.

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Chapter XVII

AUDITORY ORGAN, OLFACTORY ORGAN AND SENSE ORGANS OF THE LATERAL LINE.

Auditory Organs.

A great variety of organs, very widely distributed amongst aquatic forms, and also found, though less universally, in land forms, are usually classed together as auditory organs.

In the case of all aquatic forms, or of forms which have directly inherited their auditory organs from aquatic forms, these organs are built upon a common type; although in the majority of instances the auditory organs of the several groups have no genetic relations. All the organs have their origin in specialized portions of the epidermis. Some of the cells of a special region become provided at their free extremities with peculiar hairs, known as auditory hairs; while in other cells concretions, known as otoliths, are formed, which appear often to be sufficiently free to be acted upon by vibrations of the surrounding medium, and to be so placed as to be able in their turn to transmit their vibrations to the cells with auditory hairs[194]. The auditory regions of the epidermis are usually shut off from the surface in special sacks.

[194] The function of the otoliths is not always clear. There is evidence to shew that they sometimes act as dampers.

The actual function of these organs is no doubt correctly described, in the majority of instances, as being auditory; but it appears to me very possible that in some cases their function may be to enable the animals provided with them to detect the presence of other animals in their neighbourhood, through the undulatory movements in the water, caused by the swimming of the latter.

Auditory organs with the above characters, sometimes freely open to the external medium, but more often closed, are found in various Coelenterata, Vermes and Crustacea, and universally or all but universally in the Mollusca and Vertebrata.

In many terrestrial Insects a different type of auditory organ has been met with, consisting of a portion of the integument modified to form a tympanum or drum, and supported at its edge by a chitinous ring. The vibrations set up in the membranous tympanum stimulate terminal nerve organs at the ends of chitinous processes, placed in a cavity bounded externally by the tympanic membrane.

The tympanum of Amphibia and Amniota is an accessory organ added, in terrestrial Vertebrata, to an organ of hearing primitively adapted to an aquatic mode of life; and it is interesting to notice the presence of a more or less similar membrane in the two great groups of terrestrial forms, i.e. terrestrial Vertebrata and Insecta.

Nothing is known with reference to the mode of development or evolution of the tympanic type of auditory organ found in Insects, and, except in the case of Vertebrates, but little is known with reference to the development of what may be called the vesicular type of auditory organ found in aquatic forms. Some very interesting facts with reference to the evolution of such organs have however been brought to light by the brothers Hertwig in their investigations on the Coelenterata; and I propose to commence my account of the development of the auditory organs in the animal kingdom by a short statement of the results of their researches.

Coelenterata. Three distinct types of auditory organ have been recognised in the Medusæ; two of them resulting from the differentiation of a tentacle-like organ, and one from ectoderm cells on the under surface of the velum. We may commence with the latter as the simplest. It is found in the Medusæ known as the Vesiculata. The least differentiated form of this organ, so far discovered, is present in Mitrotrocha, Tiaropsis and other genera. It has the form of an open pit; and a series of such organs are situated along the attached edge of the velum with their apertures directed downwards. The majority of the cells lining the outer, i.e. peripheral side of the pit, contain an otolith, while a row of the cells on the inner, i.e. central side, are modified as auditory cells. The auditory cells are somewhat strap-shaped, their inner ends being continuous with the fibres of the lower nerve-ring, and their free ends being provided with bent auditory hairs, which lie in contact with the convex surfaces of the cells containing the otoliths.

[FIG. 297. AUDITORY VESICLE OF PHIALIDIUM AFTER TREATMENT WITH DILUTE OSMIC ACID. (From Lankester; after O. and R. Hertwig.)

d^1. epithelium of the upper surface of the velum; d^2. epithelium of the under surface of the velum; r. circular canal at the edge of the velum; nr^1. upper nerve-ring; h. auditory cells; hh. auditory hairs; np. nervous cushion formed of a prolongation of the lower nerve-ring. Close to the nerve-ring is seen a cell, shewn as black, containing an otolith.]

By the conversion of such open pits into closed sacks a more complicated type of auditory organ, which is present in many of the Vesiculata, viz. Æquorea, Octorchis, Phialidium, &c., is produced. A closed vesicle of this type is shewn in fig. 297. Such organs form projections on the upper surface of the velum. They are covered by a layer of the epithelium (d^1) of the upper surface of the velum, but the lining of the vesicle (d^2) is derived from what was originally part of the epithelium of the lower surface of the velum, homologous with that lining the open pits in the type already described. The general arrangement of the cells lining such vesicles is the same as that of the cells lining the open pits.

A second type of auditory organ, found in the Trachymedusæ, appears in its simplest condition as a modified tentacle. It is formed of a basal portion, covered by auditory cells with long stiff auditory hairs, supporting at its apex a club-shaped body, attached to it by a delicate stalk. An endodermal axis is continued through the whole structure, and in one or more of the endoderm cells of the club-shaped body otoliths are always present. The tails of the auditory cells are directly continued into the upper nerve-ring.

In more complicated forms of this organ the tentacle becomes enclosed in a kind of cup, by a wall-like upgrowth of the surrounding parts (fig. 298); and in some forms, e.g. Geryonia, by the closure of the cup, the whole structure takes the form of a completely closed vesicle, in the cavity of which the original tentacle forms an otolith-bearing projection.

[FIG. 298. AUDITORY ORGAN OF RHOPALONEMA. (From Lankester; after O. and R. Hertwig.)

The organ consists of a modified tentacle (hk) with auditory cells and concretions, partially enclosed in a cup.]

The auditory organs found in the Acraspedote Medusæ approach in many respects to the type of organ found in the Trachymedusæ. They consist of tentacular organs placed in grooves on the under surface of the disc. They have a swollen extremity, and are provided with an endodermal axis for half the length of which there is a diverticulum of the gastrovascular canal system. The terminal portion of the endoderm is solid, and contains calcareous concretions. The ectodermal cells at the base of these organs have the form of auditory cells.

Mollusca. Auditory vesicles are found in almost all Mollusca on the ventral side of the body in close juxtaposition to the pedal ganglia. Except possibly in some Cephalopods, these vesicles are closed. They are provided with free otoliths, supported by the cilia of the walls of the sack, but in addition some of the cells of the sack are provided with stiff auditory hairs.

In many forms these sacks have been observed to originate by an invagination of the epiblast of the foot (Paludina, Nassa, Heteropoda, Limax, Clio, Cephalopoda and Lamellibranchiata). In other instances (some Pteropods, Lymnæus, &c.) they appear, by a secondary modification in the development, to originate by a differentiation of a solid mass of epiblast.

According to Fol the otocysts in Gasteropods are formed by cells of the wall of the auditory sacks; and the same appears to hold good for Cephalopoda (Grenacher)[195] shewing that free otoliths have in these instances originated from otoliths originally placed in cells.

[195] For the somewhat complicated details as to the development of the auditory sacks of Cephalopods I must refer the reader to Vol. II., pp. 278, 279, and to Grenacher (Vol. I., No. 280).

Crustacea. In the decapodous Crustacea organs, which have been experimentally proved to be true organs of hearing, are usually present on the basal joint of the anterior antennæ. They may have (Hensen, No. 384) the form either of closed or of open sacks, lined by an invagination of the epidermis. They are provided with chitinous auditory hairs and free otoliths. In the case of the open sacks the otoliths appear to be simply stones transported into the interior of the sacks, but in the closed sacks the otoliths, though free, are no doubt developed within the sacks.

The Schizopods, which, as mentioned in the last chapter, are remarkable as containing a genus (Euphausia) with abnormally situated eyes, distinguish themselves again with reference to their auditory organs, in that another genus (Mysis) is characterized by the presence of a pair of auditory sacks in the inner plates of the tail. These sacks have curved auditory hairs supporting an otolith at their extremity.

The development of the auditory organs in the Crustacea has not been investigated.

The Vertebrata. The Cephalochorda are without organs of hearing, and the auditory organ of the Urochorda is constructed on a special type of its own. The primitive auditory organs of the true Vertebrata have the same fundamental characters as those of the majority of aquatic invertebrate forms. They consist of a vesicle, formed by the invagination of a patch of epiblast, and usually shut off from the exterior, but occasionally (Elasmobranchii) remaining open. The walls of this vesicle are always much complicated and otoliths of various forms are present in its cavity. To this vesicle accessory structures, derived from the walls of the hyomandibular cleft, are added in the majority of terrestrial Vertebrata.

The development of the true auditory vesicle will be considered separately from that of the accessory structures derived from the hyomandibular cleft.

[FIG. 299. SECTION THROUGH THE HEAD OF AN ELASMOBRANCH EMBRYO, AT THE LEVEL OF THE AUDITORY INVOLUTION.

aup. auditory pit; aun. ganglion of auditory nerve; iv.v. roof of fourth ventricle; a.c.v. anterior cardinal vein; aa. aorta; I.aa. aortic trunk of mandibular arch; pp. head cavity of mandibular arch; Ivc. alimentary pouch which will form the first visceral cleft; Th. rudiment of thyroid body].

In all Vertebrata the development of the auditory vesicle commences with the formation of a thickened patch of epiblast, at the side of the hind-brain, on the level of the second visceral cleft. This patch soon becomes invaginated in the form of a pit (fig. 299, aup), to the inner side of which the ganglion of the auditory nerve (aun), which as shewn in a previous chapter is primitively a branch of the seventh nerve, closely applies itself.

In those Vertebrata (viz. Teleostei, Lepidosteus and Amphibia) in which the epiblast is early divided into a nervous and epidermic stratum, the auditory pit arises as an invagination of the nervous stratum only, and the mouth of the auditory pit is always closed (fig. 300) by the epidermic stratum of the skin. Since the opening of the pit is retained through life in Elasmobranchii the closed form of pit in the above forms is clearly secondary.

In Teleostei the auditory pit arises as a solid invagination of the epiblast.

The mouth of the auditory vesicle gradually narrows, and in most forms soon becomes closed, though in Elasmobranchii it remains permanently open. In any case the vesicle is gradually removed from the surface, remaining connected with it by an elongated duct, either opening on the dorsal aspect of the head (Elasmobranchii), or ending blindly close beneath the skin.

[FIG. 300. SECTION THROUGH THE HEAD OF A LEPIDOSTEUS EMBRYO ON THE SIXTH DAY AFTER IMPREGNATION.

au.v. auditory vesicle; au.n. auditory nerve; ch. notochord; hy. hypoblast.]

[FIG. 301. SECTION THROUGH THE HIND-BRAIN OF A CHICK AT THE END OF THE THIRD DAY OF INCUBATION.

IV. fourth ventricle. The section shews the very thin roof and thicker sides of the ventricle. Ch. notochord; CV. anterior cardinal vein; CC. involuted auditory vesicle (CC points to the end which will form the cochlear canal); RL. recessus labyrinthi (remains of passage connecting the vesicle with the exterior); hy. hypoblast lining the alimentary canal; AO., AO.A. aorta, and aortic arch.]

In all Vertebrata the auditory vesicle undergoes further changes of a complicated kind. In the Cyclostomata these changes are less complicated than in other forms, though whether this is due to degeneration, or to the retention of a primitive state of the auditory organ, is not known. In the Lamprey the auditory vesicle is formed in the usual way by an invagination of the epiblast, which soon becomes vesicular, and for a considerable period retains a simple character. As pointed out by Max Schultze, a number of otoliths appears in the vesicle during larval life, and, although such otoliths are stated by J. Müller to be absent both in the full-grown Ammocoete and in the adult, they have since been found by Ketel (No. 387). The formation of the two semicircular canals has not been investigated.

In all the higher Vertebrates the changes of the auditory sacks are more complicated. The ventral end of the sack is produced into a short process (fig. 301, CC); while at the dorsal end there is the canal-like prolongation of the lumen of the sack (RL), derived from the duct which primitively opened to the exterior, and which in most cases persists as a blind diverticulum of the auditory sack, known as the recessus labyrinthi or aqueductus vestibuli. The parts thus indicated give rise to the whole of the membranous labyrinth of the ear. The main body of the vesicle becomes the utriculus and semicircular canals, while the ventral process forms the sacculus hemisphericus and cochlear canal.

The growth of these parts has been most fully studied in Mammalia, where they reach their greatest complexity, and it will be convenient to describe their development in this group, pointing out how they present, during some of the stages in their growth, a form permanently retained in lower types.

The auditory vesicle in Mammalia is at first nearly spherical, and is imbedded in the mesoblast at the side of the hind-brain. It soon becomes triangular in section, with the apex of the triangle pointing inwards and downwards. This apex gradually elongates to form the rudiment of the cochlear canal and sacculus hemisphericus (fig. 302, CC). At the same time the recessus labyrinthi (R.L) becomes distinctly marked, and the outer wall of the main body of the vesicle grows out into two protuberances, which form the rudiments of the vertical semicircular canals (V.B). In the lower forms (fig. 305) the cochlear process of the vestibule hardly reaches a higher stage of development than that found at this stage in Mammalia.

The parts of the auditory labyrinth thus established soon increase in distinctness (fig. 303); the cochlear canal (CC) becomes longer and curved; its inner and concave surface being lined by a thick layer of columnar epiblast. The recessus labyrinthi also increases in length, and just below the point where the bulgings to form the vertical semicircular canals are situated, there is formed a fresh protuberance for the horizontal semicircular canal. At the same time the central parts of the walls of the flat bulgings of the vertical canals grow together, obliterating this part of the lumen, but leaving a canal round the periphery; and, on the absorption of their central parts, each of the original simple bulgings of the wall of the vesicle becomes converted into a true semicircular canal, opening at its two extremities into the auditory vesicle. The vertical canals are first established and then the horizontal canal.

[FIG. 302. TRANSVERSE SECTION OF THE HEAD OF A FOETAL SHEEP (16 MM. IN LENGTH) IN THE REGION OF THE HIND-BRAIN. (After Böttcher.)

HB. the hind-brain.

The section is somewhat oblique, hence while on the right side the connections of the recessus vestibuli R.L., and of the commencing vertical semicircular canal V.B., and of the ductus cochlearis CC., with the cavity of the primary otic vesicle are seen; on the left side, only the extreme end of the ductus cochlearis CC, and of the semicircular canal V.B. are shewn.

Lying close to the inner side of the otic vesicle is seen the cochlear ganglion GC; on the left side the auditory nerve G and its connection N with the hind-brain are also shewn.

Below the otic vesicle on either side lies the jugular vein.]

Shortly after the formation of the rudiment of the horizontal semicircular canal a slight protuberance becomes apparent on the inner commencement of the cochlear canal. A constriction arises on each side of the protuberance, converting it into a prominent hemispherical projection, the sacculus hemisphericus (fig. 304, S.R).

[FIG. 303. SECTION OF THE HEAD OF A FOETAL SHEEP 20 MM. IN LENGTH. (After Böttcher.)

R.V. recessus labyrinthi; V.B. vertical semicircular canal; H.B. horizontal semicircular canal; C.C. cochlear canal; G. cochlear ganglion.]

The constrictions are so deep that the sacculus is only connected with the cochlear canal on the one hand, and with the general cavity of the auditory vesicle on the other, by, in each case, a narrow though short canal.

The former of these canals (fig. 304, b) is known as the canalis reuniens. At this stage we may call the remaining cavity of the original otic vesicle, into which all the above parts open, the utriculus.

Soon after the formation of the sacculus hemisphericus, the cochlear canal and the semicircular canals become invested with cartilage. The recessus labyrinthi remains however still enclosed in undifferentiated mesoblast.

Between the cartilage and the parts which it surrounds there remains a certain amount of indifferent connective tissue, which is more abundant around the cochlear canal than around the semicircular canals.

As soon as they have acquired a distinct connective-tissue coat, the semicircular canals begin to be dilated at one of their terminations to form the ampullæ. At about the same time a constriction appears opposite the mouth of the recessus labyrinthi, which causes its opening to be divided into two branches--one towards the utriculus and the other towards the sacculus hemisphericus; and the relations of the parts become so altered that communication between the sacculus and utriculus can only take place through the mouth of the recessus labyrinthi (fig. 305).

When the cochlear canal has come to consist of two and a half coils, the thickened epithelium which lines the lower surface of the canal forms a double ridge from which the organ of Corti is subsequently developed. Above the ridge there appears a delicate cuticular membrane, the membrane of Corti or membrana tectoria.

The epithelial walls of the utricle, the recessus labyrinthi, the semicircular canals, and the cochlear canal constitute together the highly complicated product of the original auditory vesicle. The whole structure forms a closed cavity, the various parts of which are in free communication. In the adult the fluid present in this cavity is known as the endolymph.

In the mesoblast lying between these parts and the cartilage, which at this period envelopes them, lymphatic spaces become established, which are partially developed in the Sauropsida, but become in Mammals very important structures.

They consist in Mammals partly of a space surrounding the utricle and semicircular canals, and partly of two very definite channels, which largely embrace between them the cochlear canal. The latter channels form the scala vestibuli on the upper side of the cochlear canal and the scala tympani on the lower. The scala vestibuli is in free communication with the lymphatic cavity surrounding the vestibule, and opens at the apex of the cochlea into the scala tympani. The latter ends blindly at the fenestra rotunda.

The fluid contained in the two scalæ, and in the remaining lymphatic cavities of the auditory labyrinth, is known as perilymph.

[FIG. 304. SECTION THROUGH THE INTERNAL EAR OF AN EMBRYONIC SHEEP 28 MM. IN LENGTH. (After Böttcher.)

D.M. dura mater; R.V. recessus labyrinthi; H.V.B. posterior vertical semicircular canal; U. utriculus; H.B. horizontal semicircular canal; b. canalis reuniens; a. constriction by means of which the sacculus hemisphericus S.R. is formed; f. narrowed opening between sacculus hemisphericus and utriculus; C.C. cochlea; C.C´. lumen of cochlea; K.K. cartilaginous capsule of cochlea; K.B. basilar plate; Ch. notochord.]

The cavities just spoken of are formed by an absorption of parts of the embryonic mucous tissue between the perichondrium and the walls of the membranous labyrinth.

The scala vestibuli is formed before the scala tympani, and both scalæ begin to be developed at the basal end of the cochlea: the cavity of each is continually being carried forwards towards the apex of the cochlear canal by a progressive absorption of the mesoblast. At first both scalæ are somewhat narrow, but they soon increase in size and distinctness.

The cochlear canal, which is often known as the scala media of the cochlea, becomes compressed on the formation of the scalæ so as to be triangular in section, with the base of the triangle outwards. This base is only separated from the surrounding cartilage by a narrow strip of firm mesoblast, which becomes the stria vascularis, etc. At the angle opposite the base the canal is joined to the cartilage by a narrow isthmus of firm material, which contains nerves and vessels. This isthmus subsequently forms the lamina spiralis, separating the scala vestibuli from the scala tympani.

The scala vestibuli lies on the upper border of the cochlear canal, and is separated from it by a very thin layer of mesoblast, bordered on the cochlear aspect by flat epiblast cells. This membrane is called the membrane of Reissner. The scala tympani is separated from the cochlear canal by a thicker sheet of mesoblast, called the basilar membrane, which supports the organ of Corti and the epithelium adjoining it. The upper extremity of the cochlear canal ends in a blind extremity called the cupola, to which the two scalæ do not for some time extend. This condition is permanent in Birds, where the cupola is represented by a structure known as the lagena (fig. 305, II. L). Subsequently the two scalæ join at the extremity of the cochlear canal; the point of the cupola still however remains in contact with the bone, which has now replaced the cartilage, but at a still later period the scala vestibuli, growing further round, separates the cupola from the adjoining osseous tissue.

The ossification around the internal ear is at first confined to the cartilage, but afterwards extends into the thick periosteum between the cartilage and the internal ear, and thus eventually makes its way into the lamina spiralis, etc.

The organ of Corti. In Mammalia there is formed from the epithelium of the cochlear canal a very remarkable organ known as the organ of Corti, the development of which is of sufficient importance to merit a brief description. A short account of this organ in the adult state may facilitate the understanding of its development.

[FIG. 305. DIAGRAMS OF THE MEMBRANOUS LABYRINTH. (From Gegenbaur.)

I. Fish. II. Bird. III. Mammal.

U. utriculus; S. sacculus; US. utriculus and sacculus; Cr. canalis reuniens; R. recessus labyrinthi; UC. commencement of cochlea; C. cochlear canal; L. lagena; K. cupola at apex of cochlear canal; V. cæecal sack of the vestibulum of the cochlear canal.]

The cochlear canal is bounded by three walls, the outer one being the osseous wall of the cochlea. The membrane of Reissner bounds it towards the scala vestibuli, and the basilar membrane towards the scala tympani. This membrane stretches from the margin of the lamina spiralis to the ligamentum spirale; the latter being merely an expanded portion of the connective tissue lining the osseous cochlea.

The lamina spiralis is produced into two lips, called respectively the labium tympanicum and labium vestibulare; it is to the former and longer of these that the basilar membrane is attached. At the margin of the junction of the labium tympanicum with the basilar membrane the former is perforated for the passage of the nervous fibres, and this region is called the habenula perforata.

The labium vestibulare, so called from its position, is shorter than the labium tympanicum and is raised above into numerous blunt teeth. Partly springing out from the labium vestibulare, and passing from near the inner attachment of the membrane of Reissner towards the outer wall of the cochlea, is an elastic membrane, the membrana tectoria. Resting on the basilar membrane is the organ of Corti.

Considering for the moment that a transverse section of the cochlear canal only one cell deep is being dealt with, the organ of Corti will be found to consist of a central part composed of two peculiarly shaped rods widely separated below, but in contact above. These are the rods or fibres of Corti. On their outer side, i.e. on the side towards the osseous wall of the canal, is a reticulate membrane which passes from the inner rod of Corti towards the osseous wall of the canal. With their upper extremities fixed in that membrane, and their lower resting on the basilar membrane are three (four in man) cells with auditory hairs known as the outer 'hair cells,' which alternate with three other cells known as Deiters' cells. Between these and the outer attachment of the basilar membrane is a series of cells gradually diminishing in height in passing outwards. On the inner side of the rods of Corti is one hair cell, and then a number of peculiarly modified cells which fill up the space between the two lips of the lamina spiralis.

It will not be necessary to say much in reference to the development of the labium tympanicum and the labium vestibulare.

The labium vestibulare is formed by a growth of the connective tissue which fuses with and passes up between the epithelial cells. The epithelial cells which line its upper (vestibular) border become modified, and remain as its teeth.

The labium tympanicum is formed by the coalescence of the connective tissue layer separating the scala tympani from the cochlear canal with part of the connective tissue of the lamina spiralis. At first these two layers are separate, and the nerve fibres to the organ of Corti pass between them. Subsequently however they coalesce, and the region where they are penetrated by the nervous fibres becomes the habenula perforata.

The organ of Corti itself is derived from the epiblast cells lining the cochlear canal, and consists in the first instance of two epithelial ridges or projections. The larger of them forms the cells on the inner side of the organ of Corti, and the smaller the rods of Corti together with the inner and outer hair cells and Deiters' cells.

At first both these ridges are composed of simple elongated epithelial cells one row deep. The smaller ridge is the first to shew any change. The cells adjoining the larger ridge acquire auditory hairs at their free extremities, and form the row of inner hair cells; the next row of cells acquires a broad attachment to the basilar membrane, and gives origin to the inner and outer rods of Corti.

Outside the latter come several rows of cells adhering together so as to form a compact mass which is quadrilateral in section. This mass is composed of three upper cells with nuclei at the same level, which form the outer hair cells, each of them ending above in auditory hairs, and three lower cells which form the cells of Deiters. Beyond this the cells gradually pass into ordinary cubical epithelial cells.

As just mentioned, the cells of the second row, resting with their broad bases on the basilar membrane, give rise to the rods of Corti. The breadth of the bases of these cells rapidly increases, and important changes take place in the structure of the cells themselves.

The nucleus of each cell divides; so that there come to be two nuclei or sometimes three which lie close together near the base of the cell. Outside the nuclei on each side a fibrous cuticular band appears. The two bands pass from the base of the cell to its apex, and there meet though widely separated below. The remaining contents of the cell, between the two fibrous bands, become granular, and are soon to a great extent absorbed; leaving at first a round, and then a triangular space between the two fibres. The two nuclei, surrounded by a small amount of granular matter, come to lie, each at one of the angles between the fibrous bands and the basilar membrane.

The two fibrous bands become, by changes which need not be described in detail, converted into the rods of Corti--each of their upper ends growing outwards into the processes which the adult rods possess.

Each pair of rods of Corti is thus (Böttcher) to be considered as the product of one cell; and the nuclei embedded in the granular mass between them are merely the remains of the two nuclei formed by the division of the original nucleus of that cell[196]. The larger ridge is for the most part not permanent, and from being the most conspicuous part of the organ of Corti comes to be far less important than the smaller ridge. Its cells undergo a partial degeneration; so that the epithelium in the hollow between the two lips of the lamina spiralis, which is derived from the larger ridge, comes to be composed of a single row of short and broad cells. In the immediate neighbourhood however of the inner hair cell, one or two of the cells derived from the larger ridge are very much elongated.

[196] It is not clear from Böttcher's description how it comes about that the inner rods of Corti are more numerous than the outer.

The membrana reticularis is a cuticular structure derived from the parts to which it is attached.

Accessory structures connected with the organ of hearing in Terrestrial Vertebrata.

In all the Amphibia, Sauropsida and Mammalia, except the Urodela and a few Anura and Reptilia, the first visceral or hyomandibular cleft enters into intimate relations with the organs of hearing, and from it and the adjoining parts are formed the tympanic cavity, the Eustachian tube, the tympanic membrane and the meatus auditorius externus. The tympanic membrane serves to receive from the air the sound vibrations, which are communicated to fluids contained in the true auditory labyrinth by one ossicle or by a chain of auditory ossicles.

The addition to the organ of hearing of a tympanic membrane to receive aerial sound vibrations is an interesting case of the adaptation of a structure, originally required for hearing in water, to serve for hearing in air; and as already pointed out, the similarity of this membrane to the tympanic membrane of some Insects is also striking.

There is much that is obscure with reference to the actual development of the above parts of the ear, which has moreover only been carefully studied in Birds and Mammals.

The Eustachian tube and tympanic cavity seem to be derived from the inner part of the first visceral or hyomandibular cleft, the external opening of which becomes soon obliterated. Kölliker holds that the tympanic cavity is simply a dorsally and posteriorly directed outgrowth of the median part of the inner section of this cleft; while Moldenhauer (No. 392) holds, if I understand him rightly, that it is formed as an outgrowth of a cavity called by him the sulcus tubo-tympanicus, derived from the inner aperture of the first visceral cleft together with the groove of the pharynx into which it opens; and Moldenhauer is of opinion that the greater part of the original cleft atrophies.

The meatus auditorius externus is formed at the region of a shallow depression where the closure of the first visceral cleft takes place. It is in part formed by the tissue surrounding this depression growing up in the form of a wall, and Moldenhauer believes that this is the whole process. Kölliker states however that the blind end of the meatus becomes actually pushed in towards the tympanic cavity.

The tympanic membrane is derived from the tissue which separates the meatus auditorius externus from the tympanic cavity. This tissue is obviously constituted of an hypoblastic epithelium on its inner aspect, an epiblastic epithelium on its outer aspect, and a layer of mesoblast between them, and these three layers give rise to the three layers of which this membrane is formed in the adult. During the greater part of foetal life it is relatively very thick, and presents a structure bearing but little resemblance to that in the adult.

A proliferation of the connective tissue-cells in the vicinity of the tympanic cavity causes in Mammalia the complete or nearly complete obliteration of the cavity during foetal life.

The tympanic cavity is bounded on its inner aspect by the osseous investment of the internal ear, but at one point, known as the fenestra ovalis, the bone is deficient in the Amphibia, Sauropsida and Mammalia, and its place is taken by a membrane; while in Mammalia and Sauropsida a second opening, the fenestra rotunda, is also present.

These two fenestræ appear early, but whether they are formed by an absorption of the cartilage, or by the nonchondrification of a small area, is not certainly known. The upper of the two, or fenestra ovalis, contains the base of a bone, known in the Sauropsida and Amphibia as the columella. The main part of the columella is formed of a stalk which is held by Parker to be derived from part of the skeleton of the visceral arches, but its nature is discussed in connection with the skeleton, while the base, forming the stapes, appears to be derived from the wall of the periotic cartilage.

In all Amphibia and Sauropsida with a tympanic cavity, the stalk of the columella extends to the tympanic membrane; its outer end becoming imbedded in this membrane, and serving to transmit the vibrations of the membrane to the fluid in the internal ear. In Mammalia there is a stapes not directly attached to the tympanic membrane by a stalk, and two additional auditory ossicles, derived from parts of the skeleton of the visceral arches, are placed between the stapes and the tympanic membrane. These ossicles are known as the malleus and incus, and the chain of the three ossicles replaces physiologically the single ossicle of the lower forms.

These ossicles are at first imbedded in the connective tissue in the neighbourhood of the tympanic cavity, but on the full development of this cavity, become apparently placed within it; though really enveloped in the mucous membrane lining it.

The fenestra ovalis is in immediate contiguity with the walls of the utricle, while the fenestra rotunda adjoins the scala tympani.

Hunt (No. 391) holds, from his investigations on the embryology of the pig, that "the Eustachian tube is an involution of the pharyngeal mucous membrane;" and that "the meatus is an involution of the integument" while "the drum is formed by the Eustachian tube overlapping the extremity of the meatus." Urbantschitsch also holds that the first visceral cleft has nothing to do with the formation of the tympanic cavity and Eustachian tube, and that these parts are derived from lateral outgrowths of the oral cavity.

The evolution of the accessory parts of the ear would be very difficult to explain on Darwinian principles if the views of Hunt and Urbantschitsch were correct; and the accepted doctrine, originally proposed by Huschke (No. 389), according to which these structures have originated by a 'change of function' of the parts of the first visceral cleft, may fairly be held till more conclusive evidence has been brought against it than has yet been done.

[FIG. 306. LARVA OF ASCIDIA MENTULA. (From Gegenbaur; after Kupffer.) Only the anterior part of the tail is represented.

N´. anterior swelling of neural tube; N. anterior swelling of spinal portion of neural tube; n. hinder part of neural tube; ch. notochord; K. branchial region of alimentary tract; d. oesophageal and gastric region of alimentary tract; O. eye; a. otolith; o. mouth; s. papilla for attachment.]

Tunicata. The auditory organ of the Tunicata (fig. 306) is placed on the under surface of the anterior vesicle of the brain. It consists of two parts (1) a prominence of the cells of the floor of the brain forming a crista acustica, and (2) an otolith projecting into the cavity of the brain, and attached to the crista by delicate hairs.

The crista acustica is formed of very delicate cylindrical cells, and in its most projecting part is placed a vesicle with clear contents. The otolith is an oval body with its dorsal half pigmented, and its ventral half clear and highly refractive. It is balanced on the highest point of the crista.

The crista acustica would seem to be developed from the cells of the lower part of the front vesicle of the brain. The otolith however is developed from a single cell on the dorsal and right side of the brain. This cell commences to project into the cavity of the brain and its free end becomes pigmented. It gradually grows inwards till it forms a spherical prominence in the cavity of the brain, to the wall of which it is attached by a stalk. At the same time it travels round the right side of the vesicle of the brain (in a way not fully explained) till it reaches the summit of the crista, which has become in the meantime established.

The auditory organ of the simple Ascidians can hardly be brought into relation with that of the other Chordata, and has most probably been evolved within the Tunicate phylum.

BIBLIOGRAPHY.

Invertebrata.

(384) V. Hensen. "Studien üb. d. Gehörorgan d. Decapoden." Zeit. f. wiss. Zool., Vol. XIII. 1863.

(385) O. and R. Hertwig. Das Nervensystem u. d. Sinnesorgane d. Medusen. Leipzig, 1878.

Vertebrata.

(386) A. Boettcher. "Bau u. Entwicklung d. Schnecke." Denkschriften d. kaiserl. Leop. Carol. Akad. d. Wissenschaft., Vol. XXXV.

(387) C. Hasse. Die vergleich. Morphologie u. Histologie d. häutigen Gehörorgane d. Wirbelthiere. Leipzig, 1873.

(388) V. Hensen. "Zur Morphologie d. Schnecke." Zeit. f. wiss. Zool., Vol. XIII. 1863.

(389) E. Huschke. "Ueb. d. erste Bildungsgeschichte d. Auges u. Ohres beim bebrüteten Küchlein." Isis von Oken, 1831, and Meckel's Archiv, Vol. VI.

(390) Reissner. De Auris internæ formatione. Inaug. Diss. Dorpat, 1851.

Accessory parts of Vertebrate Ear.

(391) David Hunt. "A comparative sketch of the development of the ear and eye in the Pig." Transactions of the International Otological Congress, 1876.

(392) W. Moldenhauer. "Zur Entwick. d. mittleren u. äusseren Ohres." Morphol. Jahrbuch, Vol. III. 1877.

(393) V. Urbantschitsch. "Ueb. d. erste Anlage d. Mittelohres u. d. Trommelfelles." Mittheil. a. d. embryol. Instit. Wien, Heft I. 1877.

Olfactory organ.

Amongst the Invertebrata numerous sense organs have been described under the title of olfactory organs. In aquatic animals they often have the form of ciliated pits or grooves, while in the Insects and Crustacea delicate hairs and other structures present on the antennæ are usually believed to be organs of smell. Our knowledge of all these organs is however so vague that it would not be profitable to deal with them more fully in this place. Amongst the Chordata there are usually well developed olfactory organs.

Amongst the Urochorda (Tunicata) it is still uncertain what organs (if any) deserve this appellation. The organ on the dorsal side of the opening of the respiratory pharynx may very possibly have an olfactory function, but it is certainly not homologous with the olfactory pits of the true Vertebrata, and as mentioned above (pp. 436 and 437), may perhaps be homologous with the pituitary body.

[FIG. 307. VIEWS OF THE HEAD OF ELASMOBRANCH EMBRYOS AT TWO STAGES AS TRANSPARENT OBJECTS.

A. Pristiurus embryo of the same stage as fig. 28 F. B. Somewhat older Scyllium embryo.

III. third nerve; V. fifth nerve; VII. seventh nerve; au.n. auditory nerve; gl. glossopharyngeal nerve; Vg. vagus nerve; fb. fore-brain; pn. pineal gland; mb. mid-brain; hb. hind-brain; iv.v. fourth ventricle; cb. cerebellum; ol. olfactory pit; op. eye; au.V. auditory vesicle; m. mesoblast at base of brain; ch. notochord; ht. heart; Vc. visceral clefts; eg. external gills; pp. sections of body cavity in the head.]

In the Cephalochorda (Amphioxus) there is a shallow ciliated pit, discovered by Kölliker, which is situated on the left side of the head, and is closely connected with a special process of the front end of the brain. It is most probably the homologue of the olfactory pits of the true Vertebrata.

In the true Vertebrata the olfactory organ has usually the form of a pair of pits, though in the Cyclostomata the organ is unpaired.

In all the Vertebrata with two olfactory pits these organs are formed from a pair of thickened patches of the epiblast, on the under side of the fore-brain, immediately in front of the mouth (fig. 307, ol). Each thickened patch of epiblast soon becomes involuted as a pit (fig. 308, N), the lining cells of which become the olfactory or Schneiderian epithelium. The surface of this epithelium is usually much increased by various foldings, which in the Elasmobranchii arise very early, and are bilaterally symmetrical, diverging on each side like the barbs of a feather from the median line. They subsequently become very pronounced (fig. 309), serving greatly to increase the surface of the olfactory epithelium. At a very early stage the olfactory nerve attaches itself to the olfactory epithelium.

In Petromyzon the olfactory organ arises as an unpaired thickening of the epiblast, which in the just hatched larva forms a shallow pit, on the ventral side of the head, immediately in front of the mouth. This pit rapidly deepens, and soon extends itself backwards nearly as far as the infundibulum (fig. 310, ol). By the development of the upper lip the opening of the olfactory pit is gradually carried to the dorsal surface of the head, and becomes at the same time narrowed and ciliated (fig. 47, ol). The whole organ forms an elongated sack, and in later stages becomes nearly divided by a median fold into two halves.

It is probable that the unpaired condition of the olfactory organ in the Lamprey has arisen from the fusion of two pits into one; there is however no evidence of this in the early development; but the division of the sack into two halves by a median fold may be regarded as an indication of such a paired character in the later stages.

In Myxine the olfactory organ communicates with the mouth through the palate, but the meaning of this communication, which does not appear to be of the same nature as the communication between the olfactory pits and the mouth by the posterior nares in the higher types, is not known.

The opening of the olfactory pit does not retain its embryonic characters. In Elasmobranchii and Chimæra it becomes enclosed by a wall of integument, often deficient on the side of the mouth, so that there is formed a groove leading from the nasal pit towards the angle of the mouth. This groove is usually constricted in the middle, and the original single opening of the nasal sack thus becomes nearly divided into two. In Teleostei and Ganoids the division of the nasal opening into two parts becomes complete, but the ventral opening is generally carried off some distance from the mouth, and placed, by the growth of the snout, on the upper surface of the head (figs. 54 and 68). In all these instances it is probable that the dorsal opening of the external nares, and the ventral opening with the posterior nares of higher types. Thus the posterior nares would in fact seem to be represented in all Fishes by a ventral part of the opening of the original nasal pit which either adjoins the border of the mouth (many Elasmobranchii) or is quite separate from the mouth (Teleostei and Ganoidei). In the Dipnoi, Amphibia and all the higher types the oral region becomes extended so as to enclose the posterior nares, and then each nasal pit acquires two openings; viz. one outside the mouth, the external nares, and one within the mouth, the internal or posterior nares. In the Dipnoi the two nasal openings are very similar to those in Ganoidei and Teleostei, but both are placed on the under surface of the head, the inner one being within the mouth, and the external one is so close to the outer border of the upper lip that it also has been considered by some anatomists to lie within the mouth.

[FIG. 308. SIDE VIEW OF THE HEAD OF AN EMBRYO CHICK OF THE THIRD DAY AS AN OPAQUE OBJECT. (Chromic acid preparation.)

C.H. cerebral hemispheres; F.B. vesicle of third ventricle; M.B. mid-brain; Cb. cerebellum; H.B. medulla oblongata; N. nasal pit; ot. auditory vesicle in the stage of a pit with the opening not yet closed up; op. optic vesicle, with l. lens and ch.f. choroidal fissure.

1 F. The first visceral fold; above it is seen the superior maxillary process.

2, 3, 4 F. Second, third and fourth visceral folds, with the visceral clefts between them.]

In all the higher types the nasal pits have originally only a single opening, and the ontogenetic process by which the posterior nasal opening is formed has been studied in the Amniota and Amphibia. Amongst the Amniota we may take the Chick as representing the process in a very simple form. The general history of the process was first made out by Kölliker.

[FIG. 309. SECTION THROUGH THE BRAIN AND OLFACTORY ORGAN OF AN EMBRYO OF SCYLLIUM. (Modified from figures by Marshall and myself.)

c.h. cerebral hemispheres; ol.v. olfactory vesicle; olf. olfactory pit; Sch. Schneiderian folds; I. olfactory nerve. The reference line has been accidentally taken through the nerve to the brain.]

[FIG. 310. DIAGRAMMATIC VERTICAL SECTION THROUGH THE HEAD OF A LARVA OF PETROMYZON.

The larva had been hatched three days, and was 4.8 mm. in length. The optic and auditory vesicles are supposed to be seen through the tissues.

c.h. cerebral hemisphere; th. optic thalamus; in. infundibulum; pn. pineal gland; mb. mid-brain; cb. cerebellum; md. medulla oblongata; au.v. auditory vesicle; op. optic vesicle; ol. olfactory pit; m. mouth; br.c. branchial pouches; th. thyroid involution; v.ao. ventral aorta; ht. ventricle of heart; ch. notochord.]

The opening of the nasal pit becomes surrounded by a ridge except on its oral side. The deficiency of this ridge on the side of the mouth gives rise to a kind of shallow groove leading from the nasal pit to the mouth. The ridge enveloping the opening of the nasal pit next becomes prolonged along the sides of this groove, especially on its inner one; and at the same time the superior maxillary process grows forwards so as to bound the lower part of its outer side. The inner and outer ridges, together with the superior maxillary process, enclose a deep groove, connecting the original opening of the nasal pit with the mouth. The process just described is illustrated by fig. 311 A, and it may be seen that the ridge on the inner side of the groove forms the edge of the frontonasal process (k).

[FIG. 311. HEAD OF A CHICK FROM BELOW ON THE SIXTH AND SEVENTH DAYS OF INCUBATION. (From Huxley.)

I^a. cerebral vesicles; a. eye, in which the remains of the choroid slit can still be seen in A; g. nasal pits; k. frontonasal process; l. superior maxillary process; 1. inferior maxillary process or first visceral arch; 2. second visceral arch; x. first visceral cleft.

In A the cavity of the mouth is seen enclosed by the frontonasal process, the superior maxillary processes and the first pair of visceral arches. At the back of it is seen the opening leading into the throat. The nasal grooves leading from the nasal pits to the mouth are already closed over.

In B the external opening of the mouth has become much constricted, but it is still enclosed by the frontonasal process and superior maxillary processes above, and by the inferior maxillary processes (first pair of visceral arches) below.

The superior maxillary processes have united with the frontonasal process, along nearly the whole length of the latter.]

On the sixth day (Born, 394) the sides of this groove unite together in the middle, and convert it into a canal open at both ends--the ventral openings of the canals of the two sides being placed just within the border of the mouth, and forming the posterior nares; while the external openings form the anterior nares. The upper part of the canal, together with the original nasal pit, is alone lined by olfactory epithelium; the remaining epithelium of the nasal cavity being indifferent epiblastic epithelium. Further changes subsequently take place in connection with the posterior nares, but these are described in the section dealing with the mouth.

In Mammalia the general formation of the anterior and posterior nares is the same as in Birds; but, as shewn by Dursy and Kölliker, an outgrowth from the inner side of the canal between the two openings arises at an early period; and becoming separate from the posterior nares and provided with a special opening into the mouth, forms the organ of Jacobson. The general relations of this organ when fully formed are shewn in fig. 312.

In Lacertilia the formation of the posterior nares differs in some particulars from that in Birds (Born). A groove is formed leading from the primitive nasal pit to the mouth, bordered on its inner side by the swollen edge of the frontonasal process, and on its outer by an outer-nasal process; while the superior maxillary process does not assist in bounding it. On the inner side of the narrowest part of this groove there is formed a large lateral diverticulum, which is lined by a continuation of the Schneiderian epithelium, and forms the rudiment of Jacobson's organ. The nasal groove continues to grow in length, but soon becomes converted into a canal by the junction of the outer-nasal process with the frontonasal process. This canal is open at both ends: at its dorsal end is placed the original opening of the nasal pit, and its ventral opening is situated within the cavity of the mouth. The latter forms the primitive posterior nares. The superior maxillary process soon grows inwards on the under side of the posterior part of the nasal passage, and assists in forming its under wall. This ingrowth of the superior maxillary process is the rudiment of the hard palate.

On the conversion of the nasal groove into a closed passage, the opening of Jacobson's organ into the groove becomes concealed; and at a later period Jacobson's organ becomes completely shut off from the nasal cavity, and opens into the mouth at the front end of an elongated groove leading back to the posterior nares.

[FIG. 312. SECTION THROUGH THE NASAL CAVITY AND JACOBSON'S ORGAN. (From Gegenbaur.)

sn. septum nasi; cn. nasal cavity; J. Jacobson's organ; d. edge of upper jaw.]

In Amphibia the posterior nares are formed in a manner very different from that of the Amniota. At an early stage a shallow groove is formed leading from the nasal pit to the mouth; but this groove instead of forming the posterior nares soon vanishes, and by the growth of the front of the head the nasal pits are carried farther away from the mouth.

The actual posterior nares are formed by a perforation in the palate, opening into the blind end of the original nasal pit.

Considering that the various stages in the formation of the posterior nares of the Amniota are so many repetitions of the adult states of lower forms, it may probably be assumed that the mode of formation of the posterior nares in Amphibia is secondary, as compared with that in the Amniota.

A diverticulum of the front part of the nasal cavity of the Anura is probably to be regarded as a rudimentary form of Jacobson's organ.

BIBLIOGRAPHY.

(394) G. Born. "Die Nasenhöhlen u. d. Thränennasengang d. amnioten Wirbelthiere." Parts I. and II. Morphiologisches Jahrbuch, Bd. V., 1879.

(395) A. Kölliker. "Ueber die Jacobson'schen Organe des Menschen." Festschrift f. Rienecker, 1877.

(396) A. M. Marshall. "Morphology of the Vertebrate Olfactory Organ." Quart. Journ. of Micr. Science, Vol. XIX., 1879.

Sense organs of the lateral line.

Although I do not propose dealing with the general development of various sense organs of the skin, there is one set of organs, viz. that of the lateral line, which, both from its wide extension amongst the Ichthyopsida and from the similarity of some of its parts to certain organs found amongst the Chætopoda[197], has a great morphological importance.

[197] The organs which resemble those of the lateral line are the remarkable sense organs found by Eisig in the Capitellidæ (Mittheil. a. d. Zool. Station zu Neapel, Vol. 1); but I am not inclined to think that there is a true homology between these organs and the lateral line of Vertebrata. It seems to me probable that the segmentally arranged optic organs of Polyophthalmus are a special modification of the more indifferent sense organs of the Capitellidæ. The close affinity of these two types of Chætopods is favourable to this view.

The organs of the lateral line consist as a rule of canals, partly situated in the head, and partly in the trunk. These canals open at intervals on the surface, and their walls contain a series of nerve-endings. The branches of the canal in the head are innervated for the most part by the fifth pair, and those of the trunk by the nervus lateralis of the vagus nerve. There is typically but a single canal in the trunk, the openings and nerve-endings of which are segmentally arranged.

Two types of development of these organs have been found. One of these is characteristic of Teleostei; the other of Elasmobranchii.

In just hatched Teleostei, Schulze (No. 402) found that instead of the normal canals there was present a series of sense bulbs, projecting freely on the surface and partly composed of cells with stiff hairs. In most cases each bulb is enclosed in a delicate tube open at its free extremity; while the bulbs correspond in number with the myotomes. In some Teleostei (Gobius, Esox, etc.) such sense organs persist through life; in most forms however each organ becomes covered by a pair of lobes of the adjacent tissue, one formed above and the other below it. The two lobes of each pair then unite and form a tube open at both ends. The linear series of tubes so formed is the commencement of the adult canal; while the primitive sense bulbs form the sensory organs of the tubes. The adjacent tubes partially unite into a continuous canal, but at their points of apposition pores are left, which place the canal in communication with the exterior.

Besides these parts, I have found that there is present in the just hatched Salmon a linear streak of modified epidermis on the level of the lateral nerve, and from the analogy of the process described below for Elasmobranchii it appears to me probable that these streaks play some part in the formation of the canal of the lateral line.

In Elasmobranchii (Scyllium) the lateral line is formed as a linear thickening of the mucous layer of the epidermis. This thickening is at first very short, but gradually grows backwards, its hinder end forming a kind of enlarged growing point. The lateral nerve is formed shortly after the lateral line, and by the time that the lateral line has reached the level of the anus the lateral nerve has grown back for about two-thirds of that distance. The lateral nerve would seem to be formed as a branch of the vagus, but is at first half enclosed in the modified cells of the lateral line (fig. 275, nl)[198], though it soon assumes a deeper position.

[198] Götte and Semper both hold that the lateral nerve, instead of growing in a centrifugal manner like other nerves, is directly derived from the epiblast of the lateral line. For the reasons which prevent me accepting this view I must refer the reader to my Monograph on Elasmobranch Fishes, pp. 141-146.

A permanent stage, more or less corresponding to the stage just described in Elasmobranchii, is retained in Chimæra, and Echinorhinus spinosus, where the lateral line has the form of an open groove (Solger, No. 404).

The epidermic thickening, which forms the lateral line, is converted into a canal, not as in Teleostei by the folding over of the sides, but by the formation of a cavity between the mucous and epidermic layers of the epiblast, and the subsequent enclosure of this cavity by the modified cells of the mucous layer of the epiblast which constitute the lateral line. The cavity first appears at the hind end of the organ, and thence extends forwards.

After its conversion into a canal the lateral line gradually recedes from the surface; remaining however connected with the epidermis at a series of points corresponding with the segments, and at these points perforations are eventually formed to constitute the segmental apertures of the system.

The manner in which the lumen of the canal is formed in Elasmobranchs bears the same relation to the ordinary process of conversion of a groove into a canal that the formation of the auditory involution in Amphibia does to the same process in Birds. In both Elasmobranchii and Amphibia the mucous layer of the epiblast behaves exactly as does the whole epiblast in the other types, but is shut off from the surface by the passive epidermic layer of the epiblast.

The mucous canals of the head and the ampullæ are formed from the mucous layer of the epidermis in a manner very similar to the lateral line; but the nerves to them arise as simple branches of the fifth and seventh nerves, which unite with them at a series of points, but do not follow their course like the lateral nerve.

It is clear that the canal of the lateral line is secondary, as compared with the open groove of Chimæra or the segmentally arranged sense bulbs of young Teleostei; and it is also clear that the phylogenetic mode of formation of the canal consisted in the closure of a primitively open groove. The abbreviation of this process in Elasmobranchii was probably acquired after the appearance of food-yolk in the egg, and the consequent disappearance of a free larval stage.

While the above points are fairly obvious it does not seem easy to decide à priori whether a continuous sense groove or isolated sense bulbs were the primitive structures from which the canals of the lateral line took their origin. It is equally easy to picture the evolution of the canal of the lateral line either from (1) a continuous unsegmented sense line, certain points of which became segmentally differentiated into special sense bulbs, while the whole subsequently formed a groove and then a canal; or from (2) a series of isolated sense bulbs, for each of which a protective groove was developed; and from the linear fusion of which a continuous canal became formed.

From the presence however of a linear streak of modified epidermis in larval Teleostei, as well as in Elasmobranchii, it appears to me more probable that a linear sense streak was the primitive structure from which all the modifications of the lateral line took their origin, and that the segmentally arranged sense bulbs of Teleostei are secondary differentiations of this primitive structure.

The, at first sight remarkable, distribution of the vagus nerve to the lateral line is probably to be explained in connection with the evolution of this organ. As is indicated both by its innervation from the vagus, as also from the region where it first becomes developed, the lateral line was probably originally restricted to the anterior part of the body. As it became prolonged backwards it naturally carried with it the vagus nerve, and thus a sensory branch of this nerve has come to innervate a region which is far beyond the limits of its original distribution.

BIBLIOGRAPHY.

(397) F. M. Balfour. A Monograph on the development of Elasmobranch Fishes, pp. 141-146. London, 1878.

(398) H. Eisig. "Die Segmentalorgane d. Capitelliden." Mittheil. a. d. zool. Station zu Neapel, Vol. I. 1879.

(399) A. Götte. Entwicklungsgeschichte d. Unke. Leipzig, 1875.

(400) Fr. Leydig. Lehrbuch d. Histologie des Menschen u. d. Thiere. Hamm. 1857.

(401) Fr. Leydig. Neue Beiträge z. anat. Kenntniss d. Hautdecke u. Hautsinnesorgane d. Fische. Halle, 1879.

(402) F. E. Schulze. "Ueb. d. Sinnesorgane d. Seitenlinie bei Fischen und Amphibien." Archiv f. mikr. Anat., Vol. VI. 1870.

(403) C. Semper. "Das Urogenitalsystem d. Selachier." Arbeit. a. d. zool.-zoot. Instit. Würzburg, Vol. II.

(404) B. Solger. "Neue Untersuchungen zur Anat. d. Seitenorgane d. Fische." Archiv f. mikr. Anat., Vol. XVII. and XVIII. 1879 and 1880.

Spotted a typo or a problem in this chapter? Tell us

Chapter XVIII

THE NOTOCHORD, THE VERTEBRAL COLUMN, THE RIBS AND THE STERNUM.

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Introduction

Amongst the products of that part of the mesoblast which constitutes the connective tissue of the body special prominence must be given to the skeleton of the Vertebrata, from its importance in relation to numerous phylogenetic and morphological problems.

The development of the skeleton is however so large a subject that it cannot be satisfactorily dealt with except in a special treatise devoted to it; and the following description must be regarded as a mere sketch, from which detail has been as far as possible excluded.

In the lowest Chordata the sole structure present, which deserves to be called a skeleton, is the notochord. Although the notochord often persists as an important organ in the true Vertebrata, yet there are always added to it various skeletal structures developed in the mesoblast. Before entering into a systematic description of these, it will be convenient to say a few words as to the general characters of the skeleton.

Two elements, distinct both in their genesis and structure, are to be recognized in the skeleton. The one, forming the true primitive internal skeleton or endoskeleton, is imbedded within the muscles and is originally formed in cartilage. In many instances it retains a cartilaginous consistency through life, but in the majority of cases it becomes gradually ossified, and converted into true bone. Bones so formed are known as cartilage bones.

The other element is originally formed by the fusion of the ossified bases of the dermal placoid scales already described in Chapter XIV., or by the fusion of the ossified bases of teeth situated in the mucous membrane of the mouth. In both instances the plates of bone so formed may lose the teeth or spines with which they were in the first instance covered, either by absorption in the individual, or phylogenetically by their gradually ceasing to be developed. The plates of bone, which originated by the above process, become in higher types directly developed in the connective tissue beneath the skin; and gradually acquire a deeper situation, and are finally so intimately interlocked with parts of the true internal skeleton, that the two sets of elements can only be distinguished by the fact of the one set ossifying in cartilage and the other in membrane.

It seems probable that in the Reptilia, and possibly the extinct Amphibia, dermal bones have originated in the skin without the intervention of superjacent spinous structures.

In cases where a membrane bone, as the dermal ossifications are usually called, overlies a part of the cartilage, it may set up ossification in the latter, and the cartilage bone and membrane bone may become so intimately fused as to be quite inseparable. It seems probable that in cases of this kind the compound bone may in the course of further evolution entirely lose either its cartilaginous element or its membranous element; so that cases occasionally occur where the development of a bone ceases to be an absolutely safe guide to its evolution.

As to the processes which take place in the ossification of cartilage there is still much to be made out. Two processes are often distinguished, viz. (1) a process known as ectostosis, in which the ossification takes place in the perichondrium, and either simply surrounds or gradually replaces the cartilage, and (2) a process known as endostosis, where the ossification actually takes place between the cartilage cells. It seems probable however (Gegenbaur, Vrolik) that there is no sharp line to be drawn between these two processes; but that the ossification almost always starts from the perichondrium. In the higher types, as a rule, the vessels of the perichondrium extend into the cartilage, and the ossification takes place around these vessels within the cartilage; but in the lower types (Pisces, Amphibia) ossification is often entirely confined to the perichondrium; and the cartilage is simply absorbed.

The regions where ossification first sets in are known as centres of ossification; and from these centres the ossification spreads outwards. There may be one or more centres for a bone.

The actual causes which in the first instance gave rise to particular centres of ossification, or to the ossification of particular parts of the cartilage, are but little understood; nor have we as yet any satisfactory criterion for determining the value to be attached to the number and position of centres of ossification. In some instances such centres appear to have an important morphological significance, and in other instances they would seem to be determined by the size of the cartilage about to be ossified.

There is no doubt that the membrane bones and cartilage bones can as a rule be easily distinguished by their mode of development; but it is by no means certain that this is always the case. It is necessarily very difficult to establish the homology between bones, which develop in one type from membrane and in another type from cartilage; but there are without doubt certain instances in which the homology between two bones would be unhesitatingly admitted were it not for the difference in their development. The most difficult cases of this kind are connected with the shoulder-girdle.

The possible sources of confusion in the development of bones are obviously two. (1) A cartilage bone by origin may directly ossify in membrane, without the previous development of cartilage, and (2) a membrane bone may in the first instance be formed in cartilage.

The occurrence of the first of these is much more easy to admit than that of the second; and there can be little doubt that it sometimes takes place. In a large number of cases it would moreover cause no serious difficulty to the morphologist.

BIBLIOGRAPHY of the origin of the Skeleton.

(405) C. Gegenbaur. "Ueb. primäre u. secundäre Knochenbildung mit besonderer Beziehung auf d. Lehre von dem Primordialcranium." Jenaische Zeitschrift, Vol. III. 1867.

(406) O. Hertwig. "Ueber Bau u. Entwicklung d. Placoidschuppen u. d. Zähne d. Selachier." Jenaische Zeitschrift, Vol. VIII. 1874.

(407) O. Hertwig. "Ueb. d. Zahnsystem d. Amphibien u. seine Bedeutung f. d. Genese d. Skelets d. Mundhöhle." Archiv f. mikr. Anat., Vol. XI. Supplementheft, 1874.

(408) O. Hertwig. "Ueber d. Hautskelet d. Fische." Morphol. Jahrbuch, Vol. II. 1876. (Siluroiden u. Acipenseriden.)

(409) O. Hertwig. "Ueber d. Hautskelet d. Fische (Lepidosteus u. Polypterus)." Morph. Jahrbuch, Vol. V. 1879.

(410) A. Kölliker. "Allgemeine Betrachtungen üb. die Entstehung d. knöchernen Schädels d. Wirbelthiere." Berichte v. d. königl. zoot. Anstalt z. Würzburg, 1849.

(411) Fr. Leydig. "Histologische Bemerkungen üb. d. Polypterus bichir." Zeit. f. wiss. Zool., Vol. V. 1858.

(412) H. Müller. "Ueber d. Entwick. d. Knochensubstanz nebst Bemerkungen, etc." Zeit. f. wiss. Zool., Vol. IX. 1859.

(413) Williamson. "On the structure and development of the Scales and Bones of Fishes." Phil. Trans., 1851.

(414) Vrolik. "Studien üb. d. Verknöcherung u. die Knochen d. Schädels d. Teleostier." Niederländisches Archiv f. Zoologie, Vol. I.

Notochord and Vertebral column.

The primitive axial skeleton of the Chordata consists of the notochord and its sheath. It persists as such in the adult in Amphioxus, and constitutes, in embryos of all Vertebrata, for a considerable period of their early embryonic life, the sole representative of the axial skeleton.

[FIG. 313. HORIZONTAL SECTION THROUGH THE TRUNK OF AN EMBRYO OF SCYLLIUM CONSIDERABLY YOUNGER THAN F IN FIG. 28.

The section is taken at the level of the notochord, and shews the separation of the cells to form the vertebral bodies from the muscle-plates.

ch. notochord; ep. epiblast; Vr. rudiment of vertebral body; mp. muscle-plate; mp´. portion of muscle-plate already differentiated into longitudinal muscles.]

The Notochord. The early formation of the notochord has already been described in detail (pp. 292-300). It is developed, in most if not all cases, as an axial differentiation of the hypoblast, and forms at first a solid cord of cells, without a sheath, placed between the nervous system and the dorsal wall of the alimentary tract, and extending from the base of the front of the mid-brain to the end of the tail. The section in the region of the brain will be dealt with by itself. That in the trunk forms the basis round which the vertebral column is moulded.

The early histological changes in the cells of the notochord are approximately the same in all the Craniata. There is formed by the superficial cells of the notochord a delicate sheath, which soon thickens, and becomes a well-defined structure. Vacuoles (one or more to each cell) are formed in the cells of the notochord, which enlarge till the whole notochord becomes almost entirely formed of large vacuoles separated by membranous septa which form a complete sponge-like reticulum (fig. 313). In the Ichthyopsida most of the protoplasm with the nuclei is carried to the periphery, where it forms a special nucleated layer sometimes divided into definite epithelial-like cells (fig. 314), while in the meshes of the reticulum a few nuclei surrounded by a little protoplasm still remain. In the Amniotic Vertebrata, probably owing to the early atrophy of the notochord, the distribution of the nuclei in the spaces of the mesh-work remains fairly uniform.

[FIG. 314. SECTION THROUGH THE SPINAL COLUMN OF A YOUNG SALMON. (From Gegenbaur.)

cs. sheath of notochord; k. neural arch; k´. hæmal arch; m. spinal cord; a. dorsal aorta; v. cardinal veins.]

In the early stages of development the spaces in the notochordal sponge-work, each containing a nucleus and protoplasm, probably represent cells. In the types in which the notochord persists in the adult the mesh-work becomes highly complicated, and then forms a peculiar reticulum filled with gelatinous material, the spaces in which do not indicate the outlines of definite cells (figs. 315 and 318).

Around the sheath of the notochord there is formed in the Cyclostomata, Ganoidei, Elasmobranchii and Teleostei an elastic membrane usually known as the membrana elastica externa.

In most Vertebrates the notochord and its sheath either atrophy completely or become a relatively unimportant part of the axial skeleton; but in the Cyclostomata (fig. 315) and in the Selachioidean Ganoids (Acipenser, etc.) they persist as the sole representative of the true vertebral axis. The sheath becomes very much thickened; and on the membrana elastica covering it the vertebral arches directly rest. In Elasmobranchii the sheath of the notochord undergoes a more complicated series of changes, which result first of all in the formation of a definite unsegmented cartilaginous tube[199] round the notochord, and subsequently (in most forms) in the formation of true vertebral bodies.

[199] This tube consists of a peculiar form of fibrous tissue rather than true cartilage, though part of it subsequently becomes hyaline cartilage.

[FIG. 315. SECTION THROUGH THE VERTEBRAL COLUMN OF AMMOCOETES. (From Gegenbaur.)

Ch. notochord; cs. notochordal sheath; m. spinal cord; a. aorta; v. cardinal veins.]

Between the membrana elastica externa and the sheath of the notochord a layer of cells becomes interposed (fig. 316, n), which lie in a matrix not sharply separated from the sheath of the notochord. The cells which form this layer appear to be derived from a special investment of the notochord, and to have penetrated through the membrana elastica externa to reach their final situation. The layer with these cells soon increases in thickness, and forms a continuous unsegmented tube of fibrous tissue with flattened concentrically arranged nuclei (fig. 317, Vb). Externally is placed the membrana elastica externa (mel), while within is the cuticular sheath of the notochord. This tube is the cartilaginous tube spoken of above and is known as the cartilaginous sheath of the notochord.

[FIG. 316. LONGITUDINAL SECTION THROUGH A SMALL PART OF THE NOTOCHORD AND ADJOINING PARTS OF A SCYLLIUM EMBRYO, AT THE TIME OF THE FIRST FORMATION OF THE CARTILAGINOUS SHEATH.

ch. notochord; sc. sheath of notochord; n. nuclei of cartilaginous sheath; me.e. membrana elastica externa.]

The exact origin of the cartilaginous tube just described is a question of fundamental importance with reference to the origin of the vertebral column and the homologies of its constituent parts; but is by no means easy to settle. In the account of the subject in my memoir on Elasmobranch Fishes I held with Gegenbaur that it arose from a layer of cells outside the sheath of the notochord, on the exterior of which the membrana elastica externa was subsequently formed. To this view Götte (No. 419) also gave his adhesion. Schneider has since (No. 429) stated that this is not the case, but that, as described above, the membrana elastica externa is formed before the layer of cartilage. I have since worked over this subject again, and am on the whole inclined to adopt Schneider's correction.

It follows from the above description that the cartilaginous tube in question is an essential part of the sheath of the notochord, and that it is to some extent homologous with the notochordal sheath of the Sturgeon and the Lamprey, and not an entirely new formation.

[FIG. 317. TRANSVERSE SECTION THROUGH THE VENTRAL PART OF THE NOTOCHORD AND ADJOINING STRUCTURES OF AN ADVANCED SCYLLIUM EMBRYO AT THE ROOT OF THE TAIL.

Vb. cartilaginous sheath of the notochord; ha. hæmal arch; vp. process to which the rib is articulated; mel. membrana elastica externa; ch. notochord; ao. aorta; V.cau. caudal vein.]

This sheath forms the basis of the centra of the future vertebræ. In a few adult forms, i.e. Chimæra and the Dipnoi, it retains its primitive condition, except that in Chimæra there are present delicate ossified rings more numerous than the arches; while in the Notidani, Læmargi and Echinorhini the indications of vertebræ are imperfectly marked out. The further history of this sheath in the forms in which true vertebræ are formed can only be dealt with in connection with the formation of the vertebral arches.

In Teleostei there is present, as in Elasmobranchii, an elastica externa, and an inner notochordal sheath. The elastica externa contains, according to Götte, cells. These cells, if present, are however very difficult to make out, but in any case the so-called elastica externa appears to correspond with the cartilaginous sheath of Elasmobranchii together with its enveloping elastica, since ossification, when it sets in, occurs in this layer. The sheath within becomes unusually thick.

In the Amphibia and in the Amniota no membrane is present which can be identified with the membrana elastica externa of the Elasmobranchii, Teleostei, etc. In Amphibia (Götte) there is formed round the notochord a cellular sheath, which has very much the relations of the cartilaginous tube around the notochord of Elasmobranchii, and is developed in the same way from the perichordal connective tissue cells. It is only necessary to suppose that the membrana elastica externa has ceased to be developed (which in view of its extreme delicacy and unimportant function in Elasmobranchii is not difficult to do) and this cellular sheath would then obviously be homologous with the cartilaginous tube in question. In the Amniota an external sheath of the notochord cannot be traced as a distinct structure, but the connective tissue surrounding the notochord and spinal cord is simply differentiated into the vertebral bodies and vertebral arches.

Vertebral arches and Vertebral bodies.

Cyclostomata. The Cyclostomata are the most primitive forms in which true vertebral arches are present. Their ontogeny in this group has not been satisfactorily worked out. It is however noticeable in connection with them that they form for the most part isolated pieces of cartilage, the segmental arrangement of which is only imperfect.

Elasmobranchii. In the Elasmobranchii the cells forming the vertebral arches are derived from the splanchnic layer of the mesoblastic somites. They have at first the same segmentation as the somites (fig. 313, Vr), but this segmentation is soon lost, and there is formed round the notochord a continuous sheath of embryonic connective tissue cells, which gives rise to the arches of the vertebræ, the tissue forming the dura mater, the perichondrium, and the general investing connective tissue.

The changes which next follow result in what has been known since Remak as the secondary segmentation of the vertebral column. This segmentation, which occurs in all Vertebrata with true vertebræ, is essentially the segmentation of the continuous investment of the notochord and spinal cord into vertebral bodies and vertebral arches. It does not however follow the lines of the segmentation of the muscle-plates, but is so effected that the centres of the vertebral bodies are opposite the septa between the muscle-plates.

The explanation of this character in the segmentation is not difficult to find. The primary segmentation of the body is that of the muscle-plates, which were present in the primitive forms in which vertebræ had not appeared. As soon however as the notochordal sheath was required to be strong as well as flexible, it necessarily became divided into a series of segments.

The condition under which the lateral muscles can best cause the flexure of the vertebral column is clearly that each myotome shall be capable of acting on two vertebræ; and this condition can only be fulfilled when the myotomes are opposite the intervals between the vertebræ. For this reason, when the vertebræ became formed, their centres were opposite not the middle of the myotomes but the intermuscular septa.

These considerations fully explain the characters of the secondary segmentation of the vertebral column. On the other hand the primary segmentation (fig. 313) of the vertebral rudiments is clearly a remnant of a condition when no vertebral bodies were present; and has no greater morphological significance than the fact that the cells of the vertebræ were derived from the segmented muscle-plates, and then became fused into a continuous sheath around the notochord and nervous axis; till finally they became in still higher forms differentiated into vertebræ and their arches.

During the stage represented in fig. 28 g, and somewhat before the cartilaginous sheath of the notochord is formed, there appear four special concentrations of the mesoblastic tissue adjoining the notochord, two of them dorsal (neural) and two of them ventral (hæmal). They are not segmented, and form four ridges, seated on the sides of the notochord. They are united with each other by a delicate layer of tissue, and constitute the substance in which the neural and hæmal arches subsequently become differentiated.

At about the time when the first traces of the cartilaginous sheath of the notochord arise, differentiations take place in the neural and hæmal ridges. In the neural ridge two sets of arches are formed for each myotome, and resting on the cartilaginous sheath of the notochord in the region which will afterwards form the centrum of a vertebra, and constituting a true neural arch; and a second separate from the cartilaginous sheath, forming an intercalated piece[200]. Both of them soon become hyaline cartilage.

[200] The presence of intercalated pieces in the neural arch system of Elasmobranchii, Chimæra, etc. is probably not the indication of an highly differentiated type of neural arch, but of a transitional type between an imperfect investment of the spinal cord by isolated cartilaginous bars, and a complete system of neural arches like that in the higher Vertebrata.

There is a considerable portion of the original tissue of the neural ridge, especially in the immediate neighbourhood of the notochord, which is not employed in the formation of the neural arches. This tissue has a fibrous character and becomes converted into the perichondrium and other parts.

[FIG. 318. SECTION THROUGH THE VERTEBRAL COLUMN OF AN ADVANCED EMBRYO OF SCYLLIUM IN THE REGION OF THE TAIL.

na. neural arch; ha. hæmal arch; ch. notochord; sh. inner sheath of notochord; ne. membrana elastic externa.]

The hæmal arches are formed from the hæmal ridge in precisely the same way as the neural arches, but interhæmal intercalated pieces are often present. In the region of the tail the hæmal arches are continued into ventral processes which meet below, enclosing the aorta and caudal veins.

Since primitively the postanal gut was placed between the aorta and the caudal vein, the hæmal arches potentially invest a caudal section of the body cavity. In the trunk region they do not meet ventrally, but give support to the ribs. The structures just described are shewn in section in fig. 318, in which the neural (na) and hæmal (ha) arches are shewn resting upon the cartilaginous sheath of the notochord.

While these changes are being effected in the arches the cartilaginous sheath of the notochord undergoes important differentiations. In the vertebral regions opposite the origin of the neural and hæmal arches (fig. 318) its outer part becomes hyaline cartilage, while the inner parts adjoining the notochord undergo a somewhat different development, the notochord in this part becomes at the same time somewhat constricted. In the intervertebral regions the cartilaginous sheath of the notochord becomes more definitely fibrous, while the notochord is in no way constricted. A diagrammatic longitudinal section through the vertebral column, while these changes are being effected, is shewn in fig. 320 B.

These processes are soon carried further. The notochord within the vertebral body becomes gradually constricted, especially in the median plane, till it is here reduced to a fibrous band, which gradually enlarges in either direction till it reaches its maximum thickness in the median plane of the intervertebral region. The hyaline cartilage of the vertebral region forms a vertebral body in which calcification may to some extent take place. The cartilage of the base of the arches gradually spreads over it, and on the absorption of the membrana elastica externa, which usually takes place long before the adult state is reached, the arch tissue becomes indistinguishably fused with that of the vertebral bodies, so that the latter are compound structures, partly formed of the primitive cartilaginous sheath, and partly of the tissue of the bases of the neural and hæmal arches. Owing to the beaded structure of the notochord the vertebral bodies take of necessity a biconcave hourglass-shaped form.

The intervertebral regions of the primitive sheath of the notochord form fibrous intervertebral ligaments enclosing the unconstricted intervertebral sections of the notochord.

A peculiar fact may here be noticed with reference to the formation of the vertebral bodies in the tail of Scyllium, Raja, and possibly other forms, viz. that there are double as many vertebral bodies as there are myotomes and spinal nerves. This is not due to a secondary segmentation of the vertebræ but, as I have satisfied myself by a study of the development, takes place when the vertebral bodies first become differentiated. The possibility of such a relation of parts is probably to be explained by the fact that the segmentation of the vertebral column arose subsequently to that of the nerves and myotomes.

Ganoidei. In Acipenser and other cartilaginous Ganoids the hæmal and neural arches are formed as in Elasmobranchii, and rest upon the outer sheath of the notochord. Since however the sheath of the notochord is never differentiated into distinct vertebræ, this primitive condition is retained through life.

Teleostei. In Teleostei the formation of the vertebral arches and bodies takes place in a manner, which can be reduced, except in certain minor points, to the same type as that of Elasmobranchii.

There are early formed (fig. 314 k and k´) neural and hæmal arches resting upon the outer sheath of the notochord. The latter structure, which, as mentioned on p. 549, corresponds to the cartilaginous sheath of the notochord of Elasmobranchii, soon becomes divided into vertebral and intervertebral regions. In the former ossification directly sets in without the sheath acquiring the character of hyaline cartilage (Götte, 419). The latter forms the fibrous intervertebral ligaments. The notochord exhibits vertebral constrictions.

The ossified outer sheath of the notochord forms but a small part of the permanent vertebræ. The remainder is derived partly from an ossification of the connective tissue surrounding the sheath, and partly from the bases of the arches, which do not spread round the primitive vertebral bodies as in Elasmobranchii. The ossifications in the tissue surrounding the sheath usually (fig. 319) take the form of a cross, while the bases of the arches (k and k´) remain as four cartilaginous radii between the limbs of the osseous cross. In some instances the bases of the arches also become ossified, and are then with difficulty distinguishable from the other parts of the secondary vertebral body. The parts of the arches outside the vertebral bodies are for the most part ossified (fig. 319). In correlation with the vertebral constrictions of the notochord the vertebral bodies are biconcave.

Amphibia. Of the forms of Amphibia so far studied embryologically the Salamandridæ present the most primitive type of formation of the vertebral column.

It has already been stated that in Amphibia there is present around the notochord a cellular sheath, equivalent to the cartilaginous sheath of Elasmobranchii. In the tissue on the dorsal side of this sheath a series of cartilaginous processes becomes formed. These processes are the commencing neural arches; and they rest on the cellular sheath of the notochord opposite the middle of the vertebral regions.

A superficial osseous layer becomes very early formed in each vertebral region of the cellular sheath; while in each of the intervertebral regions, which are considerably shorter than the vertebral, there is developed a ring-like cartilaginous thickening of the sheath, which projects inwards so as to constrict the notochord. At a period before this thickening has attained considerable dimensions the notochord becomes sufficiently constricted in the centre of each vertebral region to give a biconcave form to the vertebræ for a very short period of foetal life.

[FIG. 319. VERTICAL SECTION THROUGH THE MIDDLE OF A VERTEBRA OF ESOX LUCIUS (PIKE). (From Gegenbaur.)

ch. notochord; cs. notochordal sheath; k. and k´. cartilaginous tissue of the neural and hæmal arches; h. osseous hæmal process; n. spinal canal.]

The stage with biconcave vertebræ is retained through life in the Perennibranchiata and Gymnophiona.

The chief peculiarity which distinguishes the later history of their vertebral column from that of fishes consists in the immense development of the intervertebral thickenings just mentioned, which increase to such an extent as to reduce the notochord, where it passes through them, to a mere band; while the cartilage of which they are composed becomes differentiated into two regions, one belonging to the vertebra in front, the other to that behind, the hinder one being convex, and the anterior concave. The two parts are not however absolutely separated from each other.

By these changes each vertebra comes to be composed of (1) a thin osseous somewhat hourglass-shaped cylinder with a dilated portion of the notochord in its centre, and (2 and 3) of two halves of two intervertebral cartilages, viz. an anterior convex half and a posterior concave half. The vertebræ thus come to be opisthocoelous. A longitudinal section through the vertebral column at this stage is diagrammatically shewn in fig. 320 C.

[FIG. 320. DIAGRAM REPRESENTING THE MODE OF DEVELOPMENT OF THE VERTEBRÆ IN THE DIFFERENT TYPES. (From Gegenbaur.)

A. Ideal type in which distinct vertebræ are not established.

B. Type of Pisces with vertebral constrictions of the notochord.

C. Amphibian type, with intervertebral constrictions of the notochord by the intervertebral parts of the cellular sheath.

D. Intervertebral constriction of the notochord as effected in Reptilia and Aves.

E. Vertebral constriction of the notochord as effected in Mammalia, the intervertebral parts of the cartilaginous sheath being converted into intervertebral ligaments.

c. notochord; cs. cuticular sheath of notochord; s. cartilaginous sheath; v. vertebral regions; iv. intervertebral regions; g. intervertebral joints.]

To the centre of each of these vertebræ the neural arches, the origin of which was described above, become in the meantime firmly attached; and grow obliquely upwards and backwards, so as to meet and unite above the spinal cord. The transverse processes of the vertebræ would seem (Fick) to be developed independently of the arches, though they very soon fuse with them. According to Götte the transverse processes are double in the trunk, there being two pairs, one vertically above the other for each vertebra. The pair on each side eventually fuse together.

In the tail hæmal arches are formed, which are similar in their mode of development to the neural arches.

The unconstricted portion of the notochord, which persists in each vertebra, becomes in part converted into cartilage.

Anura. In the Anura the process of formation of the vertebral column is essentially the same as that in the Salamandridæ. Two types may however be observed. One of these occurs in the majority of the Anura, and mainly differs from that in Salamandra in (1) the earlier fusion of the arches with the cellular sheath of the notochord; (2) the more rapid growth of the intervertebral thickenings of the cellular sheath, which results in the early and complete obliteration of the intervertebral parts of the notochord; (3) the complete division of these intervertebral thickenings into anterior and posterior portions, which unite with and form the articular surfaces of two contiguous vertebræ. The vertebræ are moreover procoelous instead of being opisthocoelous.

The unconstricted vertebral sections of the notochord always persist till the ossification of the vertebræ has taken place. In some forms they remain through life (Rana), while in other cases they eventually either wholly or partially disappear.

The second type of vertebral development is found in Bombinator, Pseudis, Pipa, and Pelobates. In these genera the formation of the vertebra takes place almost entirely on the dorsal side of the notochord; so that the latter forms a band on the ventral side of the vertebral column. In other respects the history of the vertebral column is the same in the two cases; the vertebral unconstricted parts of the notochord appear however to become in part converted into cartilage. The type of formation of the vertebral column in these genera has been distinguished as epichordal in contradistinction to the more normal or perichordal type.

Amniota. In the Amniota all trace of a distinction between a cellular notochord sheath and an arch tissue is lost, and the two are developed together as a continuous whole forming an unsegmented tube round the notochord, with a neural ridge which does not at first nearly invest the neural cord. This tube becomes differentiated, in the manner already described for other types, into (1) vertebral regions with true arches, and (2) intervertebral regions.

Reptilia. In Reptilia (Gegenbaur, No. 416) a cartilaginous tube is formed round the notochord, which is continuous with the cartilaginous neural arches. The latter are placed in the vertebral regions, and in these regions ossification very early sets in, while the notochord remains relatively unconstricted. In the intervertebral regions the cartilage becomes thickened, as in Amphibia, and gradually constricts the notochord. The cartilage in each of the intervertebral regions soon becomes divided into two parts which form the articular faces of two contiguous vertebræ.

The general character of the vertebral column on the completion of these changes is shewn in fig. 320 D. The later changes are relatively unimportant. The constricted intervertebral sections of the notochord rapidly disappear, while the vertebral sections become partially converted into cartilage, and only cease to be distinguishable at a considerably later period.

The ossification extends from the bodies of the vertebræ into the arches and into the articular surfaces, so that the whole vertebræ eventually become ossified.

The Ascalabotæ (Geckos) present an exceptional type of vertebral column which has many of the characters of a developmental stage in other Lizards. The body of the vertebra is formed of a slightly hourglass-shaped osseous tube, united with adjoining vertebræ by a short intervertebral cartilage. There is a persistent and continuous notochord which, owing to the small development of the intervertebral cartilages, is narrower in the vertebral than in the intervertebral regions.

Aves. In Birds the cellular tube formed round the notochord is far thicker than in the Reptilia. It is continuous in the regions of the future vertebræ with neural arches, which do not at first nearly enclose the spinal cord.

On about the fifth day, in the case of the chick, it becomes differentiated into vertebral regions opposite the attachments of the neural arches, and intervertebral regions between them; the two sets of regions being only distinguished by their histological characters. Very shortly afterwards each intervertebral region becomes segmented into two parts, which respectively attach themselves to the contiguous vertebral regions. A part of each intervertebral region, immediately adjoining the notochord, does not however undergo this division, and afterwards gives rise to the ligamentum suspensorium.

The notochord during these changes at first remains indifferent, but subsequently, on about the seventh day in the chick, a slight constriction of each vertebral region takes place; so that the vertebræ have temporarily, as they have also in Amphibia, a biconcave form which repeats the permanent condition of most fishes. By the ninth and tenth days, however, this condition has completely disappeared, and in all the intervertebral portions the notochord has become distinctly constricted, and at the same time in each vertebral portion there have also appeared two constrictions of the notochord giving rise to a central and to two terminal enlargements.

On the twelfth day the ossification of the cartilaginous centra commences.

The first vertebra to ossify is the second or third cervical, and the ossification gradually extends to those behind. It does not commence in the arches till somewhat later than in the bodies. For each arch there are two centres of ossification, one on each side.

The notochord persists for the greater part of foetal life and even into post-foetal life. The larger vertebral portions are often the first completely to vanish. They would seem in many cases at any rate (Gegenbaur) to be converted into cartilage, and so form an integral part of the permanent vertebræ. Rudiments of the intervertebral portions of the notochord may long be detected in the ligamenta suspensoria.

Schwarck (No. 420) states that in both the intervertebral and the vertebral regions, though less conspicuously in the former, the cartilage is divided into two layers, an inner and an outer. He holds that the inner layer corresponds to the cartilaginous notochordal sheath of the lower types, and the outer to the arch tissue. Ossification (Gegenbaur) of the centra appears in a special inner layer of cartilage, which is probably the same as the inner layer of the earlier stage, though this point has not been definitely established.

[FIG. 321. LONGITUDINAL SECTION THROUGH THE VERTEBRAL COLUMN OF AN EIGHT WEEKS' HUMAN EMBRYO IN THE THORACIC REGION. (From Kölliker.)

v. cartilaginous vertebral body; li. intervertebral ligament; ch. notochord.]

Mammalia. The early development of the perichordal cartilaginous tube and rudimentary neural arches is almost the same in Mammals as in Birds. The differentiation into vertebral and intervertebral regions is the same in both groups; but instead of becoming divided as in Reptilia and Birds into two segments attached to two adjoining vertebræ, the intervertebral regions become in Mammals wholly converted into the intervertebral ligaments (fig. 322 li). There are three centres of ossifications for each vertebra, two in the arch and one in the centrum.

[FIG. 322. LONGITUDINAL SECTION THROUGH THE INTERVERTEBRAL LIGAMENT AND ADJACENT PARTS OF TWO VERTEBRÆ FROM THE THORACIC REGION OF AN ADVANCED EMBRYO OF A SHEEP. (From Kölliker.)

la. ligamentum longitudinale anterius; lp. ligamentum long. posterius; li. ligamentum intervertebrale; k, k´. epiphysis of vertebra; w. and w´. anterior and posterior vertebræ; c. intervertebral dilatation of notochord; c´. and c´´. vertebral dilatation of notochord.]

The fate of the notochord is in important respects different from that in Birds. It is first constricted in the centre of the vertebræ (figs. 320 E and 321) and disappears there shortly after the ossification; while in the intervertebral regions it remains relatively unconstricted (figs. 320 E, 321 and 322 c) and after undergoing certain histological changes remains through life as part of the nucleus pulposus in the axis of the invertebral ligaments[201]. There is also a slight swelling of the notochord near the two extremities of each vertebra (fig. 322 c´ and c´´). In the persistent vertebral constriction of the notochord Mammals retain a more primitive and piscine mode of formation of the vertebral column than the majority either of the Reptilia or Amphibia.

[201] This view was first put forward by Lushka, and his surmises have been confirmed by Kölliker and other embryologists. Leboucq (No. 424) however holds that the cells of the notochord in the intervertebral regions fuse with those of the adjoining tissue; and Dursy and others deny that the nucleus pulposus is derived from the notochord.

BIBLIOGRAPHY of Notochord and Vertebral column.

(415) Cartier. "Beiträge zur Entwicklungsgeschichte der Wirbelsäule." Zeitschrift für wiss. Zool., Bd. XXV. Suppl. 1875.

(416) C. Gegenbaur. Untersuchungen zur vergleichenden Anatomie der Wirbelsäule der Amphibien und Reptilien. Leipzig, 1862.

(417) C. Gegenbaur. "Ueber die Entwickelung der Wirbelsäule des Lepidosteus mit vergleichend anatomischen Bemerkungen." Jenaische Zeitschrift, Bd. III. 1863.

(418) C. Gegenbaur. "Ueb. d. Skeletgewebe d. Cyclostomen." Jenaische Zeitschrift, Vol. V. 1870.

(419) Al. Götte. "Beiträge zur vergleich. Morphol. des Skeletsystems d. Wirbelthiere." II. "Die Wirbelsäule u. ihre Anhänge." Archiv f. mikr. Anat., Vol. xv. 1878 (Cyclostomen, Ganoiden, Plagiostomen, Chimaera), and Vol. XVI. 1879 (Teleostier).

(420) Hasse und Schwarck. "Studien zur vergleichenden Anatomie der Wirbelsäule u. s. w." Hasse, Anatomische Studien, 1872.

(421) C. Hasse. Das natürliche System d. Elasmobranchier auf Grundlage d. Bau. u. d. Entwick. ihrer Wirbelsäule. Jena, 1879.

(422) A. Kölliker. "Ueber die Beziehungen der Chorda dorsalis zur Bildung der Wirbel der Selachier und einiger anderen Fische." Verhandlungen der physical. medicin. Gesellschaft in Würzburg, Bd. X.

(423) A. Kölliker. "Weitere Beobachtungen über die Wirbel der Selachier insbesondere über die Wirbel der Lamnoidei." Abhandlungen der senkenbergischen naturforschenden Gesellschaft in Frankfurt, Bd. V.

(424) H. Leboucq. "Recherches s. l. mode de disparition de la corde dorsale chez les vertébrés supérieurs." Archives de Biologie, Vol. I. 1880.

(425) Fr. Leydig. Anatomisch-histologische Untersuchungen über Fische und Reptilien. Berlin, 1853.

(426) Aug. Müller. "Beobachtungen zur vergleichenden Anatomie der Wirbelsäule." Müller's Archiv. 1853.

(427) J. Müller. "Vergleichende Anatomie der Myxinoiden u. der Cyklostomen mit durchbohrtem Gaumen, I. Osteologie und Myologie." Abhandlungen der königlichen Akademie der Wissenschaften zu Berlin. 1834.

(428) W. Müller. "Beobachtungen des pathologischen Instituts zu Jena, I. Ueber den Bau der Chorda dorsalis." Jenaische Zeitschrift, Bd. VI. 1871.

(429) A. Schneider. Beiträge z. vergleich. Anat. u. Entwick. d. Wirbelthiere. Berlin, 1879.

Ribs and Sternum.

Ribs. Embryological evidence on the development of the ribs, though somewhat inadequate, indicates that they arise as cartilaginous bars in the connective tissue of the intermuscular septa, and that they are placed, in Elasmobranchii and Amphibia, on the level of division between the dorso-lateral and ventro-lateral divisions of the muscle-plates. This does not appear to hold true for either Ganoidei or Teleostei. In Teleostei they are entirely below the muscles along the lines of the intermuscular septa, and this is partially true for Ganoidei, though not wholly so in Lepidosteus. They may be attached either to the hæmal (Pisces) or neural (Amphibia and Amniota) arches. The connective tissue from which they are formed is continuous with the processes of the vertebræ to which they are attached; but the conversion of the tissue into cartilage takes place more or less independently of that of the arches, although in many cases the cartilage of the two becomes continuous, the separation of the ribs being then effected by a subsequent process of segmentation (Fick, No. 431). It is possible that the ribs of Pisces may not be homologous with those of Amphibia and the Amniota, but till the reverse can be proved it is more convenient to assume that the ribs are homologous structures throughout the vertebrate series.

In Elasmobranchii the ribs are relatively of less importance in the adult than in the embryo. By a careful examination of their early development, I have satisfied myself that the differentiation of the ribs is independent of that of the hæmal processes to which they are attached, although the differentiation proceeds in such a manner that, when both are converted into cartilage, they are quite continuous. Subsequently the ribs become segmented off from the hæmal processes. At the junction of the tail and trunk, where the hæmal processes commence to be ventrally prolonged, eventually to unite in the region of the tail below the caudal vein, the ribs are attached to short processes which spring from the sides of the hæmal arches (fig. 317). The ventral hæmal arches of these fishes are therefore clearly in no part formed by the ribs.

In Ganoidei and Teleostei there is very great difficulty in determining the homologies of the ribs.

In the cartilaginous Ganoidei there are well developed rib-like structures, which might be regarded as homologous with Elasmobranch ribs, and indeed probably are so; but at the same time their relations are in some respects very different from those of Elasmobranch ribs in the caudal region. In Ganoids the ribs, in approaching the tail, become shorter and then fuse with the ends of the hæmal processes, and finally in the caudal region form together with the hæmal arches a closed hæmal canal which superficially resembles that in Elasmobranchii.

In Lepidosteus and Amia, especially the former, the same phenomenon is still more marked; and in Lepidosteus it is easy, in passing backwards, to trace the ribs bending ventralwards, and uniting ventrally in the caudal region to form, with the hæmal processes, a complete hæmal canal.

It might have been anticipated that the Teleostean Ganoids would resemble the Teleostei, but, from an examination of adult Teleostei, it would seem to be clear that the relations of the parts are the same as in Elasmobranchii, i.e. that the ribs have no share in forming the hæmal canal in the tail. Aug. Müller and Götte have however brought embryological evidence (though not of a conclusive character), to shew that in the embryo the ribs really fuse with the hæmal processes in the tail, and so assist, as in the Ganoids, in forming the hæmal canal. Götte moreover holds that the ribs in Elasmobranchii are not homologous with those of Teleostei and Ganoids; but that the hæmal arches in the tail are homologous in the three groups.

Without necessarily following Götte in these views it is worth pointing out that the undoubtedly close affinity between the bony Ganoids and the Teleostei is in favour of the view on the hæmal arches of Teleostei at which he has arrived on embryological grounds.

In Amphibia the formation of the ribs from the connective tissue of the intermuscular septa, their secondary attachment to the transverse processes of the neural arches, and their subsequent separation was first clearly established by Fick (No. 431), whose statements have since been confirmed by Hasse, Born, &c., and in part by Götte, who holds however that, though converted into cartilage independently of the transverse processes, they are formed in membrane as outgrowths of these processes.

In the Amniota the ribs are also independently established (Hasse and Born), though they subsequently become united to the transverse processes and to the bodies of the vertebræ, or to the transverse processes only. This junction is however stated by the majority of authorities, never to be effected by the fusion of the cartilage of the two parts, but always by fibrous tissue; though Hoffmann (No. 435) takes a different view on this subject, holding that the ribs are at first continuous with the intervertebral regions of the primitive cartilaginous tube surrounding the notochord.

Sternum. In dealing with the development of the sternum it will be convenient to leave out of consideration the interclavicle or episternum which is, properly speaking, only part of the shoulder-girdle and to confine my statements to the sternum proper.

This structure is found in all the Amniota except the Ophidia, Chelonia, and some of the Amphisbænæ.

From the older researches of Rathke, and from the newer ones of Götte, etc., it appears that the sternum is always formed from the fusion of the ventral extremities of a certain number of ribs. The extremities of the ribs unite with each other from before backwards, and thus give rise to two cartilaginous bands. These bands become segmented off from the ribs with which they are at first continuous, and subsequently fuse in the median ventral line to form an unpaired sternum. The Mammalian presternum (manubrium sterni) and xiphosternum have the same origin as the main body of the sternum (Ruge, No. 438).

In the Amphibia there is no structure which admits from its mode of development of a complete comparison with the sternum of the Amniota; and it must for this reason be considered doubtful whether the median structure placed behind the coracoids in the Anura, which is usually known as the sternum, is really homologous with the sternum of the Amniota[202].

The remaining Ichthyopsida are undoubtedly not provided with a sternum.

BIBLIOGRAPHY of Ribs and Sternum.

(430) C. Claus. "Beiträge z. vergleich. Osteol. d. Vertebraten. I. Rippen u. unteres Bogensystem." Sitz. d. kaiserl. Akad. Wiss. Wien, Vol. LXXIV. 1876.

(431) A. E. Fick. "Zur Entwicklungsgeschichte d. Rippen und Querfortsätze." Archiv f. Anat. und Physiol. 1879.

(432) C. Gegenbaur. "Zur Entwick. d. Wirbelsäule des Lepidosteus mit vergleich. anat. Bemerk." Jenaische Zeit., Vol. III. 1867.

(433) A. Götte. "Beiträge z. vergleich. Morphol. d. Skeletsystems d. Wirbelthiere Brustbein u. Schultergürtel." Archiv f. mikr. Anat., Vol. XIV. 1877.

(434) C. Hasse u. G. Born. "Bemerkungen üb. d. Morphologie d. Rippen." Zoologischer Anzeiger, 1879.

(435) C. K. Hoffmann. "Beiträge z. vergl. Anat. d. Wirbelthiere." Niederländ. Archiv Zool., Vol. IV. 1878.

(436) W. K. Parker. "A monograph on the structure and development of the shoulder-girdle and sternum." Ray Soc. 1867.

(437) H. Rathke. Ueb. d. Bau u. d. Entwicklung d. Brustbeins d. Saurier. 1853.

(438) G. Ruge. "Untersuch. üb. Entwick. am Brustbeine d. Menschen." Morphol. Jahrbuch., Vol. VI. 1880.

[202] The so-called sternum of the Amphibia develops in proximity with certain rudimentary abdominal ribs, and Ruge has with some force urged (against Götte) that it may be for this reason a rudimentary structure of the same nature as the sternum of the higher types.

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