Fig. 31.—One of a Series of Horizontal Sections through the Head of Ammocœtes.l.m., upper lip muscles;m.c., muco-cartilage;n., nose;na.c., nasal cartilage;pn., right pineal eye and nerve;g.h.r., rightganglion habenulæ;s.m., somatic muscles;cr., membranous wall of cranium;ch., choroid plexus;gl., glandular substance and pigment filling up brain-case.
Fig. 31.—One of a Series of Horizontal Sections through the Head of Ammocœtes.l.m., upper lip muscles;m.c., muco-cartilage;n., nose;na.c., nasal cartilage;pn., right pineal eye and nerve;g.h.r., rightganglion habenulæ;s.m., somatic muscles;cr., membranous wall of cranium;ch., choroid plexus;gl., glandular substance and pigment filling up brain-case.
Fig. 31.—One of a Series of Horizontal Sections through the Head of Ammocœtes.
l.m., upper lip muscles;m.c., muco-cartilage;n., nose;na.c., nasal cartilage;pn., right pineal eye and nerve;g.h.r., rightganglion habenulæ;s.m., somatic muscles;cr., membranous wall of cranium;ch., choroid plexus;gl., glandular substance and pigment filling up brain-case.
Fig. 32.—Eye of Acilius Larva, with its Optic Ganglion.On the right side the nerve end-cells have been drawn free from pigment.
Fig. 32.—Eye of Acilius Larva, with its Optic Ganglion.
On the right side the nerve end-cells have been drawn free from pigment.
Fig. 33.—Pineal Eye of Ammocœtes, with itsGanglion Habenulæ.On the left side the eye is drawn as it appeared in the section. On the right side I have removed the pigment from the nerve end-cells, and drawn the eye as, in my opinion, it would appear if it were functional.
Fig. 33.—Pineal Eye of Ammocœtes, with itsGanglion Habenulæ.
On the left side the eye is drawn as it appeared in the section. On the right side I have removed the pigment from the nerve end-cells, and drawn the eye as, in my opinion, it would appear if it were functional.
This difference between right and left indicates a greater degeneration on the left side, and points distinctly to a close relationship between the nerve-masses known asganglia habenulæand the median eyes. In my opinion this ganglion is, in part, at all events, the optic ganglion of the median eye on each side. It is built up on the same type as the optic ganglia of invertebrate simple eyes, with a cortex of small round cells and a medulla of fine nerve-fibres. Into this ganglion, on the right side, there passes a very well-defined nerve—the nerve of the dorsal eye. The eye itself with its nerve,pn., and its optic ganglion,g.h.r., is beautifully shown by means of a horizontal section through the head of Ammocœtes (Fig.31). Originally, as described by Scott, the eye stood verticallyabove its optic ganglion, and presented an appearance remarkably like Fig.32, which represents one of the simple eyes and optic ganglia of a larva of Acilius as described by Patten; then, with the forward growth of the upper lip, the right pineal eye was dragged forward and its nerve pulled horizontally over theganglion habenulæ. For this reason the eye, nerve, and ganglion are better shown in a nearly horizontal than in a transverse section.
The optic nerve belonging to this eye is most evident and clearly shown in Fig.31, and in the series of consecutive sections which follow upon this section; no doubt can arise as to the structure in question having been the nerve of the eye, even though, as is possible, it does not contain any functional nerve-fibres.
Fig. 34.—Horizontal Section through Brain of Ammocœtes, to show the Left, or Ventral Pineal Eye.pn.2, left or ventral pineal eye;pn.1, last remnant of right, or dorsal pineal eye;g.h.r., rightganglion habenulæ;g.h.l.1,g.h.l.3, parts of leftganglion habenulæ;pi., fold ofpia materwhich separates the leftganglion habenulæfrom the left pineal eye;f., strands of nerve-fibres connecting the left eye with its ganglion,g.h.l.3;V3, third ventricle;V.aq., ventricle of aquæduct.
Fig. 34.—Horizontal Section through Brain of Ammocœtes, to show the Left, or Ventral Pineal Eye.pn.2, left or ventral pineal eye;pn.1, last remnant of right, or dorsal pineal eye;g.h.r., rightganglion habenulæ;g.h.l.1,g.h.l.3, parts of leftganglion habenulæ;pi., fold ofpia materwhich separates the leftganglion habenulæfrom the left pineal eye;f., strands of nerve-fibres connecting the left eye with its ganglion,g.h.l.3;V3, third ventricle;V.aq., ventricle of aquæduct.
Fig. 34.—Horizontal Section through Brain of Ammocœtes, to show the Left, or Ventral Pineal Eye.
pn.2, left or ventral pineal eye;pn.1, last remnant of right, or dorsal pineal eye;g.h.r., rightganglion habenulæ;g.h.l.1,g.h.l.3, parts of leftganglion habenulæ;pi., fold ofpia materwhich separates the leftganglion habenulæfrom the left pineal eye;f., strands of nerve-fibres connecting the left eye with its ganglion,g.h.l.3;V3, third ventricle;V.aq., ventricle of aquæduct.
The second, ventral or left, eye, belonging to the left ganglion habenulæ is very different in appearance, being much less evidently an eye. Fig.34is one of the same series of horizontal sections as Fig.31,pn.1being the last remnant of the right, or dorsal, eye, whilepn.2shows the left, or ventral, eye with its connection with the leftganglion habenulæ.
In a series of sections I have followed the nerve of the right pineal eye to its destination, as described in my paper in theQuarterly Journal of Microscopical Science, and have found that it enters into theganglion habenulæjust as the nerve to any simple eye enters into its optic ganglion. This nerve, as I have shown, is a very distinct, well-defined nerve, with no admixture of ganglion-cells or of connective tissue, very different indeed to the connection between the left pineal eye and its optic ganglion. Here there is no defined nerve at all; but the cells of theganglion habenulæstretch right up to the remains of the eye itself. Seeing, then, that both the eye and ganglion on this side have reached a much further grade of degeneration than on the right side, it may be fairly concluded that the original condition of these two median eyes is more nearly represented by the right eye, with its well-defined nerve and optic ganglion, than by the left eye, or by the eyes in lizards and other animals which do not show so well-defined a nerve as is possessed by Ammocœtes. Quite recently Dendy has examined the two median eyes in the New Zealand lampreyGeotria australis. In this species the second eye is much better defined than in the European lamprey, and its connection with theganglion habenulæis more nerve-like. In neither eye, however, is the nerve so clean cut and isolated as is the nerve of the dorsal, or right, eye in the Ammocœtes stage ofPetromyzon Planeri; in both, cells resembling those of the cortex of theganglion habenulæand connective tissues are mixed up with the nerve-fibres which pass from each eye to its respective optic ganglion.
The Right Pineal Eye of Ammocœtes.
The optic fibres of the right median eye of Ammocœtes are connected with a well-defined retina, the limits of which are defined by the white pigment so characteristic of this eye. This pigment is apparently calcium phosphate, which still remains as the 'brain-sand' of the human pineal gland. The cells, which are hidden by this pigment, were described by me in 1890 as the retinal end-cells with large nuclei. In 1893, Studniçka examined them more closely, and concluded that the retinal cells are of two kinds: the one, nerve end-cells, the sensory cells proper; the other, pigmented epithelial cells, which surround the sense-cells. The sense-cells may contain some of the white pigment, but not so much as the other cells. Similarly, in themedian eyes of Limulus, Lankester and Bourne find it difficult to determine how far the retinal end-cells contain pigment and how far that pigment really is in the cells surrounding these nerve end-cells.
The interior of the eye presents the appearance of a cavity in shape like a cornucopia, the stalk of which terminates at the place where the nerve enters. This cavity is not empty, but the posterior part of it is filled with the termination of the nerve end-cells of the retina, as pointed out by me and confirmed by Studniçka. These terminations are free from pigment, and contain strikingly translucent bodies, which I have described in my paper in theQuarterly Journal, and called rhabdites, for they present the same appearance and are situated in the same position as are many of the rhabdites on the terminations of the retinal end-cells of arthropod eyes. Studniçka has also seen these appearances, and figures them in his second paper on the nerve end-cells of the pineal eye of Ammocœtes.
Up to this point the following conclusions may be drawn:—
1. Ammocœtes possesses a pair of median eyes, just as was the case with the most ancient fishes, and with the members of the contemporary palæostracan group.2. The retina of one of these eyes is well-defined and upright, not inverted, and therefore in this respect agrees with that of all median eyes.3. The presence of nerve end-cells, with pigment either in them or in cells around them, to the unpigmented ends of which translucent bodies resembling rhabdites are attached, is another proof that this retina agrees with that of the median eyes of arthropods.4. The simple nature of the nerve with its termination in an optic ganglion closely resembling in structure an arthropod optic ganglion, together with Studniçka's statement that the nerve end-cells pass directly into the nerve, points directly to the conclusion that this retina is a simple, not a compound, retina, and that it therefore in this respect also agrees with the retina of all median eyes.
1. Ammocœtes possesses a pair of median eyes, just as was the case with the most ancient fishes, and with the members of the contemporary palæostracan group.
2. The retina of one of these eyes is well-defined and upright, not inverted, and therefore in this respect agrees with that of all median eyes.
3. The presence of nerve end-cells, with pigment either in them or in cells around them, to the unpigmented ends of which translucent bodies resembling rhabdites are attached, is another proof that this retina agrees with that of the median eyes of arthropods.
4. The simple nature of the nerve with its termination in an optic ganglion closely resembling in structure an arthropod optic ganglion, together with Studniçka's statement that the nerve end-cells pass directly into the nerve, points directly to the conclusion that this retina is a simple, not a compound, retina, and that it therefore in this respect also agrees with the retina of all median eyes.
With respect to this last conclusion, neither I myself nor Studniçka have been able to see any definite groups of cells between the nerve end-cells and the optic nerve such as a compound retina necessitates.
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 theganglion 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 Ammocœtes ofPetromyzon Planeri. Taking also into consideration the continuity of the mass of small ganglion-cells which surround this atrium with the cells of theganglion habenulæby 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 Ammocœtes the cells of theganglion habenulæextend 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 Ammocœtes 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 ofGeotriaworked at by Dendy were in the 'Velasia' stage of the New Zealandlamprey, and correspond, therefore, more nearly to the Petromyzon than to the Ammocœtes 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.
Fig. 35.—Eye of Acilius Larvæ.(AfterPatten.)l., chitinous lens;c., corneagen;pr., pre-retinal layer;rh., rhabdites;ret., retinal end-cells.
Fig. 35.—Eye of Acilius Larvæ.(AfterPatten.)l., chitinous lens;c., corneagen;pr., pre-retinal layer;rh., rhabdites;ret., retinal end-cells.
Fig. 35.—Eye of Acilius Larvæ.(AfterPatten.)
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,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.
Fig. 36.—Eye of Hydrophilus Larva, with the Pigment over the Retinal End-cells.l., chitinous lens;c., corneagen;pr., pre-retinal layer;rh., rhabdites;ret., retinal end-cells.
Fig. 36.—Eye of Hydrophilus Larva, with the Pigment over the Retinal End-cells.l., chitinous lens;c., corneagen;pr., pre-retinal layer;rh., rhabdites;ret., retinal end-cells.
Fig. 36.—Eye of Hydrophilus Larva, with the Pigment over the Retinal End-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 Ammocœtes (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 ofthe 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?
Fig. 37.—Pineal Eye of Ammocœtes, with itsGanglion Habenulæ.
Fig. 37.—Pineal Eye of Ammocœtes, with itsGanglion Habenulæ.
Fig. 37.—Pineal Eye of Ammocœtes, with itsGanglion Habenulæ.
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. Thisthickening 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 Ammocœtes, 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 theQuarterly 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 theplastron. 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 thepellucida, 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 knobsto 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 epochthe 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 vittatusandHarpes 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.
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.
Fig. 38.—The Retina of Musca.(AfterBerger.)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.andn.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).
Fig. 38.—The Retina of Musca.(AfterBerger.)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.andn.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).
Fig. 38.—The Retina of Musca.(AfterBerger.)
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.andn.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.
(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 nerveand 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.
Fig. 39.—The Brain ofSphæroma serratum. (AfterBellonci.)Ant. I.andAnt. 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.
Fig. 39.—The Brain ofSphæroma serratum. (AfterBellonci.)Ant. I.andAnt. 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.
Fig. 39.—The Brain ofSphæroma serratum. (AfterBellonci.)
Ant. I.andAnt. 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 spokenof 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.
Fig. 40.—Bipolar Cells of Nuclear Layer in Retina of Branchipus.(AfterClaus.)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.
Fig. 40.—Bipolar Cells of Nuclear Layer in Retina of Branchipus.(AfterClaus.)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.
Fig. 40.—Bipolar Cells of Nuclear Layer in Retina of Branchipus.(AfterClaus.)
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 composedof 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.
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 Ammocœtes.
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 Ammocœtes 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 byBalfour, 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 Ammocœte 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 Ammocœte. The development of such aborted eyes has as yet been studied only in the Ammocœte, 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 Ammocœtes eye, and concludes that in aborted eyes a retarded development occurs, and this applies on the whole to Ammocœtes, "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 ofPetromyzon Planeridoes 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 Ammocœtes, is in no sense an abnormal eye, but simply that its development is slow during the ammocœte 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.
(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.
Fig. 41.—Retina and Optic Nerve of Petromyzon. (After Müller and Langerhans.)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.
Fig. 41.—Retina and Optic Nerve of Petromyzon. (After Müller and Langerhans.)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.
Fig. 41.—Retina and Optic Nerve of Petromyzon. (After Müller and Langerhans.)
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 themembrana limitans interna, the other at the inner boundary of the middle third of themolecular 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 Ammocœtes 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, andB.A neurodermal (cerebral) part which forms the rest of the retina.
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 themembrana 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 theoptic ganglion and of the retinal ganglion ramify to form the molecular layers.
It is evident from Fig.41that the retina of Ammocœtes 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 Ammocœtes 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 Ammocœtes 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 theoptic lobes and other parts of the Ammocœtes 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 Ammocœtes 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 Ammocœtes, 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 Ammocœtes, 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 Ammocœtes 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,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 Ammocœtes 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 doublelayer 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.