Chapter XV: Final Remarks (4)

{82}On the other hand, Dendy describes in the New Zealand lamprey, _Geotria australis_, a cavity where the nerve enters into the eye, which he calls the atrium. This cavity is distinct from the main cavity of the eye, and is separated from it by a mass of cells similar in appearance to those of the cortex of the _ganglion habenulæ_. In these two eyes then, groups of cells, resembling in appearance those belonging to an optic ganglion, exist in the eyes themselves. This atrium is evidently that part of the central cavity which I have called the handle of the cornucopia in the European lamprey, and the very fact that it is separated from the rest of the central cavity is evidence that we are dealing here with a later stage in the history of the pineal eyes than in the case of the Ammocoetes of _Petromyzon Planeri_. Taking also into consideration the continuity of the mass of small ganglion-cells which surround this atrium with the cells of the _ganglion habenulæ_ by means of the similar cells scattered along the course of the nerve, and also bearing in mind the fact already stated that in the more degenerate left eye of Ammocoetes the cells of the _ganglion habenulæ_ extend right up to the eye itself, it seems more likely than not that these cells do not represent the original optic ganglion of a compound retina, but rather the subsequent invasion, by way of the pineal nerve, of ganglion-cells belonging to a portion of the brain. In the last chapter it has been suggested that the presence of the trochlear or fourth cranial nerve has given rise to the formation of the cerebellum by a similar spreading.

There is certainly no appearance in the least resembling a compound retina such as is seen in the vertebrate or crustacean lateral eye. In the median eyes of scorpions and of Limulus, cells are found within the capsule of the eye among the nerve-fibres and the nerve end-cells. These are especially numerous in the median eyes of Limulus, as described by Lankester and Bourne, and are called by them intrusive connective tissue cells. The meaning of these cells is not, to my mind, yet settled. It is sufficient for my purpose to point out that the presence of cells interneural in position among the nerve end-cells of the retina of the median eyes of Ammocoetes is more probable than not, on the assumption that the retina of these eyes is built up on the same plan as that of the median eyes in Limulus and the scorpions.

It is further to be borne in mind that these specimens of _Geotria_ worked at by Dendy were in the 'Velasia' stage of the New Zealand {83}lamprey, and correspond, therefore, more nearly to the Petromyzon than to the Ammocoetes stage of the European lamprey.

THE DIOPTRIC APPARATUS.

Besides the retina, all eyes possess a dioptric apparatus. What is the evidence as to its nature in these vertebrate median eyes? Lankester and Bourne have divided the eyes of scorpions and Limulus into two kinds, monostichous and diplostichous. In the first the retinal cells are supposed to give rise to not only rhabdites but also the cuticular chitinous lens, so that the eye is one-layered; in the second the lens is formed by a well-marked hypodermal layer, in front of the retina, composed of elongated cells, so that these eyes are two-layered or diplostichous. The lateral eyes, according to them, are all monostichous, but the median eyes are diplostichous.

_l._, chitinous lens; _c._, corneagen; _pr._, pre-retinal layer; _rh._, rhabdites; _ret._, retinal end-cells.]

This distinction is not considered valid by other observers. Thus, {84}as already indicated, Patten looks on all these eyes as three-layered, and states that in all cases a corneagen or vitreogen layer exists, which gives origin to the lens. For my own part I agree with Patten, but we are not concerned here with the lateral eyes. It is sufficient to note that all observers are agreed that the median eyes are characterized by this well-marked cell-layer, the so-called vitreous or corneagen layer of cells.

_l._, chitinous lens; _c._, corneagen; _pr._, pre-retinal layer; _rh._, rhabdites; _ret._, retinal end-cells.]

This layer (_c._, Fig. 35) is composed of much-elongated cells of the hypodermal layer, in each of which the large nucleus is always situated towards the base of the cell. The space between it and the retina contains, according to Patten the cells of the pre-retinal layer _(pr.)_. These may be so few and insignificant as to give the impression that the vitreous layer is immediately adjacent to the retina (_ret._).

Let us turn now to the right pineal eye of Ammocoetes (Fig. 37) and see what its further structure is. The anterior part of the eye is free from pigment, and is composed, as is seen in hæmatoxylin or carmine specimens, of an inner layer of nuclei which are frequently arranged in a wavy line. From this nucleated layer, strands of tissue, free from nuclei, pass to the anterior edge of the eye.

In the horizontal longitudinal sections it is seen that these strands are confined to the middle of the eye. On each side of them the nuclear layer reaches the periphery, so that if we consider these strands to represent long cylindrical cells, as described by Beard, then the anterior wall may be described as consisting of long cylindrical cells, which are flanked on either side by shorter cells of a similar kind. The nuclei at the base of these cylindrical cells are not all alike. We see, in the first place, large nuclei resembling the large nuclei belonging to the nerve end-cells; these are the nuclei of {85}the long cylindrical cells. We see also smaller nuclei in among these larger ones, which look like nuclei of intrusive connective tissue, or may perhaps form a distinct layer of cells, situated between the cells of the anterior wall and the terminations of the nerve end-cells already referred to.

These elongated cells are in exactly the same position and present the same appearance as the cells of the corneagen layer of any median eye. Like the latter they are free from pigment and never show with osmic staining any sign of the presence of translucent rhabdite-like bodies, such as are seen in the termination of the retinal cells, and like the latter their nuclei are at the base. The resemblance between this layer and the corneagen cells of any median eye is absolute. Between it and the terminations of the retinal cells there exists some ill-defined material certainly containing cells which may well correspond to Patten's pre-retinal layer of cells.

Retina, corneagen, nerve, optic ganglion, all are there, all in their right position, all of the right structure, what more is needed to complete the picture?

In order to complete the dioptric apparatus a lens is necessary. Where, then, is the lens in these pineal eyes? In all the arachnid eyes, whether median or lateral, the lens is a single corneal lens composed of the external cuticle, which is thickened over the corneagen cells. This thickened cuticle is composed of chitin, and is not cellular, but is dead material formed out of the living underlying corneagen cells. Such a lens is in marked contrast to the lens of the lateral vertebrate eye, which is formed by living cells themselves. This {86}thickening of the cuticular layer to form a lens could only exist as long as that layer is absolutely external, so that the light strikes immediately upon it; for, if from any cause the eye became situated internally, the place of such a lens must be filled by the structures situated between it and the surface, and the thickened cuticle would no longer be formed.

In all vertebrates these pineal eyes are separated from the external surface by a greater or less thickness of tissues; in the case of Ammocoetes, as is seen in Fig. 31, the eye lies within the membranous cranial wall, and is attached closely to it. The position, then, of the cuticular, or corneal lens, as it is often called, on the supposition that this is a median eye of the arachnid type, is taken by the membranous cranium, and, as I have described in my paper in the _Quarterly Journal_, on carefully lifting the eye in the fresh condition from the cranial wall, it can be seen under a dissecting microscope that the cranial wall often forms at this spot a lens-like bulging, which fits the shallow concavity of the surface of the eye, and requires some little force to separate it from the eye.

As will appear in a subsequent chapter, this cranial wall has been formed by the growth, laterally and dorsally, of a skeletal structure known by the name of the _plastron_. The last part of it to be completed would be that part in the mid-dorsal line, where apparently, in consequence of the insinking of the degenerating eyes, a dermal and subdermal layer already intervened between the source of light and the eyes themselves.

When the membranous cranium was completed in the mid-dorsal region, it was situated here as elsewhere just internally to the subdermal layer, and therefore enclosed the pineal eyes. This, to my mind, is the reason why the pineal eyes, which, in all other respects, conform to the type of the median eyes of an arachnid-like animal, do not possess a cuticular lens. Other observers have attempted to make a lens out of the elongated cells of the anterior wall of the eye (my corneagen layer), but without success.

Studniçka, who calls this layer the _pellucida_, does not look upon it as the lens, but considers, strangely enough, that the translucent appearances at the ends of each nerve end-cell represent a lens for that cell, so that every nerve end-cell has its own lens. Still more strange is it that, holding this view, he should yet consider these knobs {87}to be joined by filaments to the cells in the anterior wall of the eye, a conception fatal to the action of such knobs as lenses.

The discovery that the vertebrate possesses, in addition to the lateral eyes, a pair of median eyes, which are most conspicuous in the lowest living vertebrate, together with the fact that such eyes are built up on the same plan as the median eyes of living crustaceans or arachnids, not only with respect to the eye itself but also to its nerve and optic ganglion, constitutes a fact of the very greatest importance for any theory of the origin of vertebrates; especially in view of the further fact, that similar eyes in the same position are found not only in all the members of the Palæostraca, but also in all those ancient forms (classed as fishes) which lived at that time. At one and the same moment it proves the utter impossibility of reversing dorsal and ventral surfaces, points in the very strongest manner to the origin of the vertebrate from some member or other of the palæostracan group, and insists that the advocates of the origin of vertebrates from the Hemichordata, etc., should give an explanation of the presence of these two median eyes of a more convincing character than that given here.

THE LATERAL EYES.

Turning now to the consideration of the lateral eyes, we see that these eyes in the arachnids often possess an inverted retina, in the crustaceans always an upright retina. In the arachnids they possess a simple retina, while in the crustaceans their retina is compound; so that in the latter case the so-called optic nerve is in reality a tract of fibres connecting together the brain-region with a variable number of optic ganglia, which have been left at the periphery in close contact with the retinal cells, when the brain sunk away from the superficial epithelial covering.

There is, then, this difference between the lateral eyes of crustaceans and arachnids, that the retina of the former is compound, but never inverted, while that of the latter may be inverted, but is always simple.

The retina of the lateral eyes of the vertebrate resembles both of these, for it is compound, as in the crustacean, and inverted as in the arachnid.

It must always be borne in mind that in the palæostracan epoch {88}the dominant race was neither crustacean nor arachnid, but partook of the characters of both; also, as is characteristic of dominance, there was very great variety of form, so that it seems more probable than not that some of these forms may have combined the arachnid and crustacean characteristics to the extent of possessing lateral eyes with an inverted yet compound retina. A certain amount of evidence points in this direction. As already stated, the compound retina which characterizes the vertebrate lateral eyes is characteristic of all facetted eyes, and in the trilobites facetted lateral eyes are commonly found. From this it may be concluded that many of the trilobites possessed eyes with a compound retina. There have, however, been found in certain species, e.g. _Harpes vittatus_ and _Harpes ungula_, lateral eyes which were not facetted, and are believed by Korschelt and Heider to be of an arachnid nature. They say, "Palæontologists have appropriately described them as ocelli, although, from a zoological point of view, they do not deserve this name, having most probably arisen in a way similar to that conjectured in connection with the lateral eyes of scorpions." If this conjecture is right, then in these forms the retina may have been inverted, but because they belonged to the trilobite group, the retina was most probably compound, so that here we may have had the combination of the arachnid and crustacean characteristics. On the other hand, in some forms of Branchipus, and many of the Gammaridæ, a single corneal lens is found in conjunction with an eye of the crustacean type, so that a non-facetted lateral eye, found in a fossil form, would not necessarily imply the arachnid type of eye with the possibility of an inverted retina. Whatever may be the ultimate decision upon these particular forms, the striking fact remains, that both in the vertebrate and in the arachnid the median eyes possess a simple upright retina, while the lateral eyes possess an inverted retina, and that both in the vertebrate and the crustacean the median eyes possess a simple upright retina, while the lateral eyes possess a compound retina.

The resemblance of the retina of the lateral eyes of vertebrates to that of the lateral eyes of many arthropods, especially crustaceans, has been pointed out by nearly every one who has worked at these invertebrate lateral eyes. The foundation of our knowledge of the compound retina is Berger's well-known paper, the results of which are summed up by him in the following two main conclusions.

{89}1. The optic ganglion of the Arthropoda consists of two parts, of which the one stands in direct inseparable connection with the facetted eye, and together with the layer of retinal rods forms the retina of the facetted eye, while the other part is connected rather with the brain, and is to be considered as an integral part of the brain in the narrower sense of the word.

_Br._, brain; _O.n._, optic nerve; _n.l.o.g._, nuclear layer of ganglion of optic nerve; _m.l._, molecular layer (Punktsubstanz); _n.l.r.g.i._ and _n.l.r.g.o._, inner and outer nuclear layers of the ganglion of the retina; _f.br.r._, terminal fibre-layer of retina; _r._, layer of retinal end-cells (indicated only).]

2. In all arthropods examined by him, the retina consists of five layers, as follows:--

(1) The layer of rods and their nuclei.
(2) The layer of nerve-bundles.
(3) The nuclear layer.
(4) The molecular layer.
(5) The ganglion cell layer.

Berger passes under review the structure and arrangement of the optic ganglion in a large number of different groups of arthropods, and concludes that in all cases one part of the optic ganglion is always closely attached to the visual end-cells, and this combination he calls the retina. On the other hand, the nerve-fibres which connect the peripheral part of the optic ganglion with the brain, the so-called optic nerve, are by no means homologous in the different groups; for in some cases, as in many of the stalk-eyed crustaceans, the whole optic ganglion is at the periphery, while in others, as in the Diptera, only the retinal ganglion is at the periphery, and the nerve-stalk connects this with the rest of the optic ganglion, the latter being fused with the main brain-mass. In the Diptera, in fact, according to Berger, the optic nerve {90}and retina are most nearly comparable to those of the vertebrate. For this reason I give Berger's picture of the retina of Musca (Fig. 38), in order to show the arrangement there of the retinal layers.

_Ant. I._ and _Ant. II._, nerves to 1st and 2nd antennæ. _f.br.r._, terminal fibre-layer of retina; _Op. g. I._, first optic ganglion; _Op. g. II._, second optic ganglion; _O.n._, optic nerve-fibres forming an optic chiasma.]

In Branchipus and other primitive Crustacea, Berger also finds the same retinal layers, but is unable to distinguish in the brain the rest of the optic ganglion. Judging from Berger's description of Branchipus, and Bellonci's of Sphæroma, it would almost appear as though the cerebral part of the retina in the higher forms originated from two ganglionic enlargements, an external and internal enlargement, as Bellonci calls them. The external ganglion (_Op. g. I._, Fig. 39) may be called the ganglion of the retina, the cells of which form the nuclear layer of the higher forms, and the internal ganglion (_Op. g. II._, Fig. 39), from which the optic nerve-fibres to the brain arise, may therefore be called the ganglion of the optic nerve. Bellonci describes how in this latter ganglion cells are found very different to the small ones of the external ganglion or ganglion of the retina. So also in Branchipus, judging from the pictures of Berger, Claus, and from my own observations (_cf._ Fig. 46, in which the double nature of the retinal ganglion is indicated), the peripheral part of the optic ganglion--_i.e._ the retinal ganglion--may be spoken {91}of as composed of two ganglia. The external of these is clearly the ganglion of the retina; its cells form the nuclear layer, the striking character of which, and close resemblance to the corresponding layer in vertebrates, is shown by Claus' picture, which I reproduce (Fig. 40). The internal ganglion with which the optic nerve is in connection contains large ganglion cells, which, together with smaller ones, form the ganglionic layer of Berger.

The most recent observations of the structure of the compound retina of the crustacean eye are those of Parker, who, by the use of the methylene blue method, and Golgi's method of staining, has been able to follow out the structure of the compound retina in the arthropod on the same lines as had already been done for the vertebrate. These two methods have led to the conclusion that the arthropod central nervous system and the vertebrate central nervous system are built up in the same manner--viz. by means of a series of ganglia connected together, each ganglion being composed of nerve-cells, nerve-fibres, and a fine reticulated substance called by Leydig in arthropods 'Punktsubstanz,' and known in vertebrates and in invertebrates at the present time as 'neuropil.' A further analysis resolves the whole system into a combination of groups of neurones, the cells and fibres of which form the cells and fibres of the ganglia, while their dendritic connections with the terminations of other neurones, together with the neuroglia-cells form the 'neuropil.' As is natural to expect, that part of the central nervous system which helps to form the compound retina is built up in the same manner as the rest of the central nervous system.

_f.br.r._, terminal fibre-layer of retina; _n.l.r.g._, bipolar cells of the ganglion of the retina = inner nuclear layer; _m.l._, Punktsubstanz = inner molecular layer; _b.m._, basement membrane formed by neurilemma round central nervous system.]

Thus, according to Parker, the mass of nervous tissue which occupies the central part of the optic stalk in Astacus is composed {92}of four distinct ganglia; the retina is connected with the first of these by means of the retinal fibres, and the optic nerve extends proximally from the fourth ganglion to the brain. Each ganglion consists of ganglion-cells, nerve-fibres, and 'neuropil,' and, in addition, supporting cells of a neuroglial type. By means of the methylene blue method and the Golgi method, it is seen that the retinal end-cells, with their visual rods, are connected with the fibres of the optic nerve by means of a system of neurones, the synapses of which take place in and help to form the 'neuropil' of the various ganglia. Thus, an impulse in passing from the retina to the brain would ordinarily travel over five neurones, beginning with one of the first order and ending with one of the fifth. He makes five neurones although there are only four ganglia, because he reckons the retinal cell with its elongated fibre as a neurone of the first order, such fibre terminating in dendritic processes which form synapses in the 'neuropil' of the first ganglion with the neurones of the second order.

Similarly the neurones of the second order terminate in the 'neuropil' of the second ganglion, and so on, until we reach the neurones of the fifth order, which terminate on the one hand in the 'neuropil' of the fourth ganglion, and on the other pass to the optic lobes of the brain by their long neuraxons--the fibres of the optic nerve.

He compares this arrangement with that of Branchipus, Apus, Estheria, Daphnia, etc., and shows that in the more primitive crustaceans the peripheral optic apparatus was composed, not of four but of two optic ganglia, not, therefore, of five but of three neurones, viz.--

1. The neurone of the first order--_i.e._ the retinal cell with its fibre terminating in the 'neuropil' of the first optic ganglion (ganglion of the retina).

2. The neurone of the second order, which terminates in the 'neuropil' of the second ganglion (ganglion of the optic nerve).

3. The neurone of the third order, which terminates in the optic lobes of the brain by means of its neuraxons (the optic nerve).

We see, then, that the most recent researches agree with the older ones of Berger, Claus, and Bellonci, in picturing the retina of the primitive crustacean forms as formed of two ganglia only, and not of four, as in the specialized crustacean group the Malacostraca.

{93}The comparison of the arthropod compound retina with that of the vertebrate shows, as one would expect upon the theory of the origin of vertebrates put forward in this book, that the latter retina is built up of two ganglia, as in the more primitive less specialized crustacean forms. The modern description of the vertebrate retina, based upon the Golgi method of staining, is exactly Parker's description of the simpler form of crustacean retina in which the 'neuropil' of the first ganglion is represented by the external molecular layer, and that of the second ganglion by the internal molecular layer; the three sets of neurones being, according to Parker's terminology:--

1. The neurones of the first order--viz. the visual cells--the nuclei of which form the external nuclear layer, and their long attenuated processes form synapses in the external molecular layer with

2. The neurones of the second order, the cells of which form the internal nuclear layer, and their processes form synapses in the internal molecular layer with

3. The neurones of the third order, the cells of which form the ganglionic layer and their neuraxons constitute the fibres of the optic nerve which end in the optic lobes of the brain.

Strictly speaking, of course, the visual cells with their elongated processes have no right to be called neurones: I only use Parker's phraseology in order to show how closely the two retinas agree even to the formation of synapses between the fine drawn-out processes of the visual cells and the neurones of the ganglion of the retina.

THE RETINA OF THE LATERAL EYE OF AMMOCOETES.

As in the case of all other organs, it follows that if we are dealing here with a true genetic relationship, then the lower we go in the vertebrate kingdom the more nearly ought the structure of the retina to approach the arthropod type. It is therefore a matter of intense interest to determine the nature of the retina in Ammocoetes in order to see whether it differs from that of the higher vertebrates, and if so, whether such differences are explicable by reference to the structure of the arthropod eye.

Before describing the structure of this retina it is necessary to clear away a remarkable misconception, shared among others by {94}Balfour, that this eye is an aborted eye, and that it cannot be considered as a primitive type. Thus Balfour says: "Considering the degraded character of the Ammocoete eye, evidence derived from its structure must be received with caution," and later on, "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, in which it resembles in most important features that of other Vertebrata."

Again and again the aborted character of the eye is stated to be evidence of degeneration in the case of the lamprey. What such a statement means, why the eye is in any way to be considered as aborted, is to me a matter of absolute wonderment: it is true that in the larval form it lies under the skin, but it is equally true that at transformation it comes to the surface, and is most evidently as perfect an eye as could be desired. There is not the slightest sign of any degeneration or abortion, but simply of normal development, which takes a longer time than usual, lasting as it does throughout the life-time of the larval form.

Kohl, who has especially studied degenerated vertebrate eyes, discusses with considerable fulness the question of the Ammocoetes eye, and concludes that in aborted eyes a retarded development occurs, and this applies on the whole to Ammocoetes, "but with the important difference that in this case the period of retarded development is not followed by a stoppage, but on the contrary by a period of very highly intensified progressive development during the metamorphosis," with the result that "the adult eye of _Petromyzon Planeri_ does not diverge from the ordinary type."

Referring in his summing up to this retarded development, he says: "Such reminiscences of embryonic conditions are after all present here and there in normally developed organs, and by no means entitle us to speak of abnormal development."

The evidence, then, is quite clear that the eye of Petromyzon, or, indeed, of the full-grown Ammocoetes, is in no sense an abnormal eye, but simply that its development is slow during the ammocoete stage. The retina of Petromyzon was figured and described by Langerhans in 1873. He describes it as composed of the following layers:--

(1) _Membrana limitans interna._
(2) Thick inner molecular layer.
(3) Optic fibre layer.
(4) Thick inner nuclear layer.
(5) Peculiar double-layered ganglionic layer.
(6) External molecular layer.
(7) External nuclear layer.
(8) _Membrana limitans externa._
(9) Layer of rods.
(10) Pigment-epithelium.

{95}

On the left side the Müllerian fibres and pigment-epithelium are represented alone. The retina is divided into an epithelial part, _C_ (the layer of visual rod-cells), and a neurodermal or cerebral part which is formed of, _A_, the ganglion of the optic nerve and, _B_, the ganglion of the retina. 1, int. limiting membrane; 2, int. molecular layer with its two layers of cells; 3, layer of optic nerve fibres; 4, int. nuclear layer; 5, double row of tangential fulcrum cells; 6, layer of terminal retinal fibres; 7, ext. nuclear layer; 8, ext. limiting membrane; 9, layer of rods; 10, layer of pigment-epithelium. _D_, axial cell layer (Axenstrang) in optic nerve. The layer 6 is drawn rather too thick.]

He points out especially the peculiarity of layer (2) (2, Fig. 41), the inner molecular, in which two rows of nuclei are arranged with great regularity, the one row closely touching the _membrana limitans interna_, the other at the inner boundary of the middle third of the {96}molecular layer. Of these two rows of nuclei, he describes the innermost as composed almost entirely of large nuclei belonging to ganglion cells, while the outermost is composed mainly of distinctly smaller nuclei, which in staining and appearance appear to belong not to nerve-cells but to the true reticular tissue of the molecular layer.

He also draws special attention to the remarkable layer (5) (5, Fig. 41), which is not found in the retina of the higher vertebrates, the cells of which, in his opinion, are of the nature of ganglion-cells.

W. Müller, in 1874, gave a most careful description of the eye of Ammocoetes and Petromyzon, and traced the development of the retina; the subsequent paper of Kohl does not add anything new, and his drawings are manifestly diagrams, and do not represent the appearances so accurately as Müller's illustrations. In the accompanying figure (Fig. 41) I reproduce on the right-hand side Müller's picture of the retina of Petromyzon, but have drawn it, as in Langerhans' picture, at the place of entry of the optic nerve.

From his comparison of this retina with a large number of other vertebrate retinas, he comes to the conclusion that the retina of all vertebrates is divisible into

_A._ An ectodermal (epithelial) part consisting of the layer of the
visual cells, and

_B._ A neurodermal (cerebral) part which forms the rest of the retina.

Further, Müller points out that the neuroderm gives origin throughout the central nervous system to two totally different structures, on the one hand to the true nervous elements, on the other to a system of supporting cells and fibres which cannot be classed as connective tissue, for they do not arise from mesoblast, and are therefore called by him 'fulcrum-cells.' In the retina he recognizes two distinct groups of such supporting structures--(1) a system of radial fibres with well-marked elongated nuclei, which extend between the two limiting layers, and form at their outer ends a membrane-like expansion which was originally the outer limit of the retina, but becomes afterwards co-terminous with the _membrana limitans externa_, owing to the piercing through it of the external limbs of the rods. This system, which is known by the name of the radial Müllerian fibres (shown on the left-hand side of Fig. 41), has no connection with (2) the spongioblasts and neurospongium, which form a framework of neuroglia, in which the terminations of the {97}optic ganglion and of the retinal ganglion ramify to form the molecular layers.

It is evident from Fig. 41 that the retina of Ammocoetes and Petromyzon differs in a striking manner from the typical vertebrate retina. The epithelial part (C) remains the same--viz. the visual rods, the external limiting membrane, and the external nuclear layer; but the cerebral part, the retinal ganglion (A and B), is remarkably different. It is true, it consists in the main of the small-celled mass known as the inner nuclear layer, and of the reticulated tissue or 'neuropil' known as the inner molecular layer, just as in all other compound retinal eyes; but neither the ganglion cell-layer nor the optic fibre-layer is clearly defined as separate from this molecular layer; on the contrary, it is matter of dispute as to what cells represent the ganglionic layer of higher vertebrates, and the optic fibres do not form a distinct innermost layer, but pass into the inner molecular layer at its junction with the inner nuclear layer. A comparison of this innermost part of the retina (A, Fig. 41), with the corresponding part in Berger's picture of Musca (_n.l.o.g._, Fig. 38), shows a most striking similarity between the two. In both cases the fibres of the optic nerve (_O.n._, Fig. 38) which cross at their entrance pass into the 'neuropil' of this part of the retinal ganglion, and are connected probably (though that is not proved in either case) with the cells of the ganglionic layer. In both cases we find two well-marked parallel rows of cells in this part of the retina, of which one, the innermost, is composed in Ammocoetes of large ganglion-cells, and the other mainly of smaller, deeper staining cells apparently supporting in function. Similarly, also, in Branchipus, as I conclude from my own observations as well as from those of Berger and Claus, the ganglionic layer is composed partly of true ganglion-cells and partly of supporting cells arranged in a distinct layer. This part, then, of the retina of Ammocoetes is remarkably like that of a typical arthropod retina, and forms that part of the retinal ganglion which may be called the ganglion of the optic nerve.

Next comes the ganglion of the retina (B, Fig. 41) (Parker's first optic ganglion), the cells of which form the small bipolar granule-cells of the inner nuclear layer; granule-cells arranged in rows just as they are shown in Claus' picture of the same layer in the retina of Branchipus (Fig. 40), just as they are found in the cortical layers of the optic ganglion of the pineal eye (_ganglion habenulæ_), in the {98}optic lobes and other parts of the Ammocoetes brain, or in the cortical layers of the optic ganglia of all arthropods.

Between this small-celled nuclear layer (4, Fig. 41) and the layer of nuclei of the visual rod cells (7, Fig. 41) (the external nuclear layer), we find in the eye of Ammocoetes and Petromyzon two well-marked rows of cells of a most striking character--viz. the two remarkably regular rows of large epithelial-like cells with large conspicuous nuclei, which give the appearance of two opposing rows of limiting epithelium (5, Fig. 41), already mentioned in connection with the researches of Langerhans and W. Müller. Here, then, is a striking peculiarity of the retina of the lamprey, and according to Müller the obliteration of these two layers can be traced as we pass upwards in the vertebrate kingdom. Among fishes, they are especially well seen in the perch; in the higher vertebrates the whole layer is only a rudiment represented, he thinks, by the simple layer of round cells which lies close against the inner surface of the layer of terminal fibres (Nervenansätze), and is especially evident in birds and reptiles. In man and the higher mammals they are probably represented by the horizontal cells of the outer part of the inner nuclear layer.

Seeing, then, that they are most evident in Ammocoetes, and become less and less marked in the higher vertebrates, it is clear that their origin cannot be sought among the animals higher in the scale than Ammocoetes, but must, therefore, be searched for in the opposite direction.

Müller describes them as forming a very conspicuous landmark in the embryology of the retina, dividing it distinctly into two parts, an outer thinner, and an inner somewhat thicker part, the zone formed by them standing out conspicuously on account of the size and regularity of the cells and their lighter appearance when stained. Thus in his description of the retina of an Ammocoetes 95 mm. in length, he says, "The layer of pale tangentially elongated cells formed a double layer and produced the appearance of a pale, very characteristic zone between the outer and inner parts of the retina."

Let us now turn to the retina of the crustacean and see whether there is any evidence there that the retina is divisible into an outer and inner part, separated by a zone of characteristically pale staining cells with conspicuous nuclei. The most elaborate description of the development of the retina of Astacus is given by Reichenbach, {99}according to whom the earliest sign of the formation of the retina is an ectodermic involution (Augen-einstülpung), which soon closes, so that the retinal area appears as a thickening. In close contiguity to this thickening, the thickening of the optic ganglion arises, so that that part of the optic ganglion which will form the retinal ganglion fuses with the thickened optic plate and forms a single mass of tissue. Later on a fold (Augen-falte) appears in this mass of tissue, in consequence of which it becomes divided into two parts. The lining walls of this fold form a double row of cells, the nuclei of which are most conspicuous because they are larger and lighter in colour than the surrounding nuclei, so that by this fold the retina is divided into an outer and an inner wall, the line of demarcation being conspicuous by reason of these two rows of large, lightly-staining nuclei.

Reichenbach is unable to say that this secondary fold is coincident with the primary involution, and that therefore the junction between the two rows of large pale nuclei is the line of junction between the retinal ganglion and the retina proper, because all sign of the primary involution is lost before the secondary fold appears.

Parker compares the appearances in the lobster with Reichenbach's description in the crayfish, and says that he finds only a thickening, no primary involution; at the same time he expressly states that in the very early stages his material was deficient, and that he had not grounds sufficient to warrant the statement that no involution occurs. He also finds that in the lobster the ganglionic tissue which arises by proliferation is divided into an outer and inner part; the separation is effected by a band of large, lightly-staining nuclei, which, in position and structure, resemble the band figured by Reichenbach. According to Parker, then, the line of separation indicated in the development by Reichenbach's outer and inner walls is not the line of junction between the retina and the retinal ganglion, as Reichenbach was inclined to think, but rather a separation of two rows of large ganglion-cells belonging to the retinal ganglion.

The similarity between these conspicuous layers of lightly-staining cells in Ammocoetes and in crustaceans is remarkably close, and in both cases observers have found the same difficulty in interpreting their meaning. In each case one group of observers looks upon them as ganglion-cells, the other as supporting structures. Thus in the lamprey, Müller considers them to belong to the supporting elements, while Langerhans and Kohl describe them as a double {100}layer of ganglion-cells. In the crustacean, Berger in Squilla, Grenacher in Mysis, and Parker in Astacus, look upon them as supporting elements, while Viallanes in Palinurus considers them to be true ganglionic cells.

Whatever the final interpretation of these cells may prove to be, we may, it seems to me, represent an ideal compound retina of the crustacean type by combining the investigations of Berger, Claus, Reichenbach, and Parker in the following figure.

The retina is divided into an epithelial part, _C_ (the layer of retinular cells and rhabdomes), and a neurodermal or cerebral part, which is formed of, _A_, the ganglion of the optic nerve, and, _B_, the ganglion of the retina. 1, optic nerve fibres which cross at their entrance into the retina; 2, int. molecular layer with its two rows of cells; 3, int. nuclear layer; 4, Reichenbach's double row of large lightly-staining cells; 5, layer of terminal retinal fibres; 6, ext. nuclear layer; 7, ext. limiting membrane; 8, layer of crystalline cones; 9, cornea.]

The comparison of this figure (Fig. 42) with that of the Petromyzon retina (Fig. 41) shows how great is the similarity of the latter with the arthropod type, and how the very points in which it deviates from the recognized vertebrate type are explainable by comparison with that of the arthropod. The most striking difference between the retinas in the two figures is that the layer of terminal nerve fibres (5, Fig. 42), which, after all, are only the elongated terminations of the retinal cells belonging to Parker's neurones of the first order, is very much longer than in Petromyzon or in any vertebrate, for the external molecular layer (6, Fig. 41) (Müller's layer of Nervenansätze) is very short and inconspicuous (in Fig. 41 it is drawn too thick).

Turning from the retina to the fibres of the optic nerve we again find a remarkable resemblance, for in Ammocoetes, as pointed out by {101}Langerhans and carefully figured by Kohl, a crossing of the fibres of the optic nerve occurs as the nerve leaves the retina, just as is so universally the case in all compound retinas. To this crossing Kohl has given the name _chiasma nervi optici_, in distinction to the cerebral chiasma, which he calls _chiasma nervorum opticorum_. Further, we find that even this latter chiasma is well represented in the arthropod brain; thus Bellonci in Sphæroma, Berger, Dietl, and Krieger in Astacus, all describe a true optic chiasma, the only difference in opinion being, whether the crossing of the optic nerves is complete or not. Especially instructive are Bellonci's figures and description. He describes the brain of Sphæroma as composed of three segments--a superior segment, the cerebrum proper, a middle segment, and an inferior segment; the optic fibres, as is seen in Fig. 39, after crossing, pass direct into the middle segment, in the ganglia of which they terminate. From this segment also arises the nerve to the first antenna of that side--_i.e._ the olfactory nerve. The optic part, then, of this middle segment is clearly the brain portion of the optic ganglionic apparatus, and may be called the optic lobes, in contradistinction to the peripheral part, which is usually called the optic ganglion, and is composed of two ganglia, Op. g. I. and Op. g. II., as already mentioned. These optic lobes are therefore homologous with the optic lobes of the vertebrate brain.

The resemblance throughout is so striking as to force one to the conclusion that the retina of the vertebrate eye is a compound retina, composed of a retina and retinal ganglion of the type found in arthropods. From this it follows that the development of the vertebrate retina ought to show the formation of (1) an optic plate formed from the peripheral epidermis and not from the brain; (2) a part of the brain closely attached to this optic plate forming the retinal ganglion, which remains at the surface when the rest of the optic ganglion withdraws; (3) an optic nerve formed in consequence of this withdrawal, as the connection between the retinal and cerebral parts of the optic ganglion.

This appears to me exactly what the developmental process does show according to Götte's investigations. He asserts that the retina arises from an optic plate, being the optical portion of his 'Sinnes-platte.' At an early stage this is separated by a furrow (Furche) from the general mass of epidermal cells which ultimately form the brain. This separation then vanishes, and the retina and brain-mass {102}become inextricably united into a mass of cells, which are still situated at the surface. By the closure of the cephalic plate and the withdrawal of the brain away from the surface, a retinal mass of cells is left at the surface connected with the tubular central nervous system by the hollow optic diverticulum or primary optic vesicle. If we regard only the retinal and nervous elements, and for the moment pay no attention to the existence of the tube, Götte's observation that the true retina has been formed from the optic plate (Sinnes-platte) to which the retinal portion of the brain (retinal ganglion) has become firmly fixed, and that then the optic nerve has been formed by the withdrawal of the rest of the brain (optic lobes), is word for word applicable to the description of the development of the compound retina of the arthropod eye, as has been already stated.

THE SIGNIFICANCE OF THE OPTIC DIVERTICULA.

The origin of the retina from an optic epidermal plate in vertebrates, as in all other animals, brings the cephalic eyes of all animals into the same category, and leaves the vertebrate eye no longer in an isolated and unnatural position. In one point the retina of the vertebrate eye differs from that of a compound retina of an invertebrate; in the former, a striking supporting tissue exists, known as Müller's fibres, which is absent in the latter. This difference of structure is closely associated with another of the same character as in the central nervous system, viz. the apparent development of the nervous part from a tube. We see, in fact, that the retinal and nervous arrangements of the vertebrate eye are comparable with those of the arthropod eye, in precisely the same way and to the same extent as the nervous matter of the brain of the vertebrate is comparable with the brain of the arthropod. In both cases the nervous matter is, in structure, position, and function, absolutely homologous; in both cases there is found in the vertebrate something extra which is not found in the invertebrate--viz. a hollow tube, the walls of which, in the case of the brain, are utilized as supporting tissues for the nerve structures. The explanation of this difference in the case of the brain is the fundamental idea of my whole theory, namely, that the hollow tube is in reality the cephalic stomach of the invertebrate, around which the nervous brain-matter was originally grouped in precisely the same manner as in the invertebrate. What, then, are the optic diverticula?

{103}"The formation of the eye," as taught by Balfour, "commences with the appearance of a pair of hollow outgrowths from the anterior cerebral vesicle. 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 united to the base of the brain by comparatively narrow, hollow stalks, the rudiments of the optic nerves."

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

He then goes on to explain how the formation of the lens forms the optic cup with its double walls from the primary optic vesicle, and says--

"Of its double walls, the inner, or anterior, is formed from the front portion, the outer, or posterior, from the hind portion of the wall of the primary optic vesicle. The inner, or anterior, which very speedily becomes thicker than the other, is converted into the retina; in the outer, or posterior, which remains thin, pigment is eventually deposited, and it ultimately becomes the tesselated pigment-layer of the choroid."

The difficulties in connection with this view of the origin of the eye are exceedingly great, so great as to have caused Balfour to discuss seriously Lankester's suggestion that the eye must have been at one time within the brain, and that the ancestor of the vertebrate was therefore a transparent animal, so that light might get to the eye through the outer covering and the brain-mass; a suggestion, the unsatisfactory nature of which Balfour himself confessed. Is there really evidence of any part of either retina or optic nerve being formed from the epithelial lining of the tube?

This tube is formed as a direct continuation of the tube of the central nervous system, and we can therefore apply to it the same arguments as have been used in the discussion of the meaning of the latter tube. Now, the striking point in the latter case is the fact that the lining membrane of the central canal is in so many parts absolutely free from nervous matter, and so shows, as in the so-called choroid plexuses, its simple, non-nervous epithelial structure. This also we find in the optic diverticulum. Where there is no evidence of any invasion of the tube by nervous elements, there it retains its simple non-nervous character of a tube composed of a single layer of {104}epithelial cells--viz. in that part of the tube which, as Balfour says, remains thin, in which pigment is eventually deposited, and which ultimately becomes the tesselated pigment-layer of the choroid. Nobody has ever suggested that this pigment-layer is nervous matter, or ever was, or ever will be, nervous matter; it is in precisely the same category as the membranous roof of the brain in Ammocoetes, which never was, and never will be, nervous matter. Yet, according to the old embryology both in the case of the eye and the brain, the pigment-layer and the so-called choroid plexuses are a part of the tubular nervous system.

Turning now to the optic nerve, Balfour describes it as derived from the hollow stalk of the optic vesicle. He says--

"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."

In this description Balfour, because he derived the optic nerve fibres from the epithelial wall of the optic stalk, of necessity supposed that such fibres originally supplied both the outer and inner walls of the optic cup and, therefore, seeing that when the fibres of the optic nerve appear they do not supply the outer wall, he supposes that their original connection with the outer wall is ruptured, because a discontinuity of the epithelial lining takes place coincidently with the appearance of the optic nerve-fibres, and, according to him, the optic nerve simply perforates the outer wall and becomes continuous with the inner one. This last statement is very difficult to understand. I presume he meant that some of the fibres of the optic nerve supplied from the beginning the inner wall of the optic cup, but that others which originally supplied the outer wall were first ruptured, then perforated the outer wall, and finally completed the supply to the inner wall or retina.

This statement of Balfour's is the necessary consequence of his belief, that the epithelial cells of the optic stalk gave rise to the fibres of the optic nerve. If, instead of this, we follow Kölliker and His, who state that the optic nerve-fibres are formed outside the {105}epithelial walls of the optic stalk, and that the cells of the latter form supporting structures for the nerve-fibres, then the position of the optic nerve becomes perfectly simple and satisfactory without any rupturing of its connection with the outer wall and subsequent perforation, for the optic nerve-fibres from their very first appearance pass directly to supply the retina--_i.e._ the inner wall of the optic cup and nothing else.

They pass, as is well known, without any perforation by way of the choroidal slit to the inner surface of the inner wall (retina) of the optic cup; then, when the choroidal slit becomes closed by the expansion of the optic cup, the optic nerve naturally becomes situated in the centre of the base of the cup and spreads over its inner surface as that surface expands.

A section across the optic cup at an early stage at the junction of the optic stalk and optic cup would be represented by the upper diagram in Fig. 43; at a later stage, when the choroidal slit is closed, by the lower diagram.

The upper diagram represents a stage before the formation of the choroidal slit, the lower one the stage of closure of the choroidal slit. _R._, retina; _O.n._, optic nerve; _p._, pigment epithelium.]

The evident truth of this manner of looking at the origin of the optic nerve is demonstrated by the appearance of the optic nerve in Ammocoetes and Petromyzon. In the latter, although the development is complete, and the eye, and consequently also the optic nerve-fibres, are fully functional, there is still present in the axial core of the nerve a row of epithelial cells (Axenstrang) which are altered so as to form supporting structures, in the same way as a row of epithelial cells in the retina is altered to form the system of supporting cells known by the name of the Müllerian fibres.

The origin of this axial core of cells is perfectly clear, as has been pointed out by W. Müller. He says--

"The development of the optic nerve shows peculiarities in {106}Petromyzon of such a character as to make this animal one of the most valuable objects for deciding the various controversial questions connected with the genesis of its elements. The lumen of the stalk of the primary optic vesicle is obliterated quite early by a proliferation of its lining epithelium. Also the original continuity of this epithelium with that of the pigment-layer is at an early period interrupted at the point of attachment of the optic stalk. This interruption occurs at the time when the fibres of the optic nerve first become visible."

Further on he says--

"The epithelium of the optic stalk develops entirely into supporting cells, which in Petromyzon fill up the original lumen and so form an axial core (Axenstrang) to the nerve-fibres which are formed entirely outside them; the projections of these supporting cells are directed towards the periphery, and so separate the bundles of the optic nerve-fibres. The mesodermal coat of the optic stalk takes no part in this separation; it simply forms the connective tissue sheath of the optic nerve. The development of the optic nerve in the higher vertebrates also obeys the same law, as I am bound to conclude from my own observations."