Text-Book of Embryology 2-2 (1919)

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A personal message from Dr Mark Hill (May 2020)  
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I have decided to take early retirement in September 2020. During the many years online I have received wonderful feedback from many readers, researchers and students interested in human embryology. I especially thank my research collaborators and contributors to the site. The good news is Embryology will remain online and I will continue my association with UNSW Australia. I look forward to updating and including the many exciting new discoveries in Embryology!

Kerr JG. Text-Book of Embryology II (1919) MacMillan and Co., London.

Textbook Chapters: 1 Formation of the Germ Layers | 2 Skin and Derivatives | 3 Alimentary Canal | 4 Coelomic Organs | 5 Skeleton | 6 Vascular | 7 Internal Body Features | 8 Adaptation to Environmental Conditions | 9 General Considerations | 10 Common Fowl | 11 Lower Vertebrates | Appendix

- Currently only early Draft Version of Text -

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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

Chapter II The Skin And Its Derivatives

The skin of the vertebrate consists of the epidermis—the persistent and less or more modified ectoderm—resting upon the superficial layer of mesenchy1ne—the dermis—which in the higher forms becomes strengthened by the formation of numerous tough interlacing fibres.

In studying the development of the skin in the various types of vertebrate we find that the ectoderm undergoes characteristic modifications to fit it for the carrying out of special functions. In the fishes it becomes converted into a highly glandular mechanism concerned with the production of slippery mucus for the diminution of what the naval architect calls “skin-friction,” in other words the friction between the surface of the body and the water in contact with it. Local or general specializations of this glandular apparatus lead to the development of cement organs by the secretion of which the young animal is able to attach itself to solid supports, to the production of digestive ferments by which the eggshell is softened or, in the case of the portion of ectoderm which lines the buccal cavity, the digestion of the food initiated, or to the production of poisonous defensive or offensive secretions. In the case of the terrestrial amphibians the glandular apparatus serves to keep the skin moist, while in the Birds it develops arrangements for oiling the feathers.

Again the ectoderm develops important protective functions. It becomes hardened and toughened to give mechanical protection: it becomes more or less loaded with opaque pigment to prevent the penetration of light rays, while in those highest vertebrates, in which, correlated with intensely active metabolism, the body is kept at a higher temperature than its surroundings, the superficial horny layer becomes as it were frayed out into a fluffy coating of feathers or hair which with its entangled air retards loss of heat from the surface of the body.

Finally the ectoderm forms the great mechanism for the reception of impressions from the external world. It develops sensory cells which may become crowded together to form organs of special sense while from its deeper layers arise tl1e main portions of the central nervous system.

The Epidermis

The ectoderm covering the surface of the embryo becomes converted, normally, into the epidermis of the fully developed individual. Very usually the embryonic ectoderm consists of two layers of cells, the lower layer composed of actively living cells, the superficial of flattened plate-like protective cells. This outer layer has been termed by Krause the periderm: its superficial protoplasm is commonly hardened to form a cuticle in the strict sense of the term. Normally it plays no active part in development a11d is shed at an early period.

The deep layer of the ectoderm on the other hand is active. Its cells multiply so that it becomes several layers thick: the outer layers become cornified to form the horny stratum of the epidermis while the deeper cells, composed of active living protoplasm, form the stratum of Malpighi.

The outer layer of ectoderm cells may be for a time ciliated. -This is well seen in young Amphibian embryos (Assheton, 1896). In Rana. tempommltv, the 6-mm. embryo possesses ciliated cells scattered thickly over its surface, the movement of the cilia being such as to drive a current of water tailwards over the surface of the embryo‘. When the external gills develop, a specially strong ciliary current sweeps backwards over them and it is noteworthy that this current passes over the olfactory organ on route to the external gills so that the olfactory organ possibly plays an important part in testing the quality of the water going to the respiratory organs. The ciliary -apparatus is sufliciently powerful at the stage in question to cause an embryo of this stage when laid on the bottom of a. flat glass vessel to slide along at the rate of a millimetre in from four to seven seconds. As development proceeds the ciliation becomes less and less prominent and in a 20-mm. tadpole it has almost disappeared except on the surface of the tail which remains richly ciliated until the time of metamorphosis. This persistence of the tail cilia is doubtless correlated with the fact that the skin of the tail plays an important part in the process of respiration.

Horny Developments of the Epidermis

8ca1es. — In many terrestrial Vertebrates the horny layer of the epidermis becomes so thickened and hardened as to become practically rigid. In such cases the flexibility of the skin as a whole is retained by the thickened areas of epidermis being separated from one another by lines along which thickening does not take place. The thickened portions now form epidermal scales of the type seen in Reptiles. They may take the form of simple rounded projecting bosses or tubercles as in Chameleons, or they may be flattened horny plates arranged edge to edge — as in Uhelonians or as ml the ventral side of the body in Crocodiles or the dorsal surface of the head in Snakes and Lizards—or, finally, they may overlap like slates on a roof as is the case on the bodies of Lizards and Snakes. Occasionally, as in certain Lizards, individual scales may become greatly thickened and assume a conical spike-like form.

The individual scale arises in development (F ig.,4l) as a slight elevation of the surface beneath which the dermal connective tissue is somewhat concentrated. The epidermis covering the projection develops a well-marked cuticle. As development goes on the epidermis increases much in thickness and the cells of the outer layers become entirely cornified so ‘as to form a horny plate or scale ——~supported by the underlying tough condensed portion of the dermis.

It will be borne in mind that such typical reptilian scales have to be sharply distingu'ished from the morphologically quite different scales developed in the dermis in fishes, The ordinary reptilian scales serve mainly to protect the body from mechanical violence and from desiccation.

FIG. 41.-—Early stage in the development of the scale of a :s'|ml{v .-is seen In a longitudinal section perpendicular‘ to the sm‘face of the skin.


In the homoiothermic Birds, where the body is kept at a constant temperature usually higher than that of the surrounding atmosphere, the scales havebecome for the most ‘part replaced by fluffy feathers which with the air entangled in their interstices form an admirable non-conducting envelope to retard the loss of heat by radiation, or convection, from the surface of the body.

The rudiment of the feather begins (Fig. 42, A) as a slight thickening of the epidermis resting upon somewhat condensed dermis. The rudiment in fact differs little from that of a normal scale. The rudiment comes to project backwards (B) and then increases in length (0), projecting freely tailwards while its now relatively narrow base of attachment becomes sunk below the general surface into a pit or follicle.

The rudiment now consists of a core of dermis surrounded by thick epidermis. The epidermis becomes incised along its axial surface by deep longitudinal grooves which divide its deeper portions into longitudinally arranged masses (Fig. 42, D, b), the rudimentary barbs, While leaving the superficial portion as a continuous sheath (sh.). The grooves in question do not reach to the base of the rudiment — the uuineised basal portion forrni.ng the quill of the feather. The horny sheath becomes strongly cornified and then lgreaks open and the 1ongitudinal thickenings of the epidermis, now also strongly coruilied, break away from the sparse cornified dermal tissue of the axis and form the fluffy barbs of the clown feather. _ _ In the basal quill portion of the feather the epidermis immediately covering the outer end of the axial dermal tissue or pulp forms a thin strongly cornified superficial layer which separates off as a septum cutting across the cavity of the quill. This process being repeated periodically gives rise to a series of horny caps fitting one over the other, in the interior of the quill (Fig. 42, H, 0).

the ah-.ve1opme.nt of feathers. (After Davies, 1889.)

A, B, ('3, lm1_«.fil.udiIml so-.(;l.i0ll.*~'-2 I), E. F, tr:ms\'t-rsr- .\-«-(-tions (I), E, «lown 1'e=.:1t.lu-1': 1!‘, flight feather) I U, lu1'1giI_4uli1n::l Sl'.(?l.l()lI llIl‘uIl_<_,"ll lmrh rudiment sl1o\\'in:.,-' «le\'u'-lopi1'1;,j' b:u‘lmles: H, lo11_r_-;itudin:1lsection 1..ln'ou;;'h l_ms«- of fa-ullu-r. b, hurh; bb, h:n'l)Hlo.': 4'. lmrny svln‘-:'I: c.r. l:n,\‘m' of I-ylin:_lI‘i¢.-:11 4-pitlwlium; _/‘, I‘:-utln-r rmlinu-nt : 3/_. ;.u-nniiml re-gion ; p, pulp: 4,, quill; I'_, r.-u.-hi~<: sh, slu-nil).

The flat feathers, found as contour featliers arranged in patches over the general surface and as Remiges and Rectrices in the wings and tail, originate from the basal portions of down feathers which undergo a great increase in length. The basal part of the rudiment in this case increases much in diameter. The epidermis here again becomes incised on its inner surface to form barb rudiments. These however are much more numerous (Fig. 42, F) than in the typical down feather and, further, instead of being arranged Strictly longitudinally they are arranged somewhat spirally, starting from a continuous epidermal thickening which runs along the outer side of the feather rudiment. This thickening is the rudimentary rachis or shaft and the barb rudiments run from it spirally round the feather rudiment until their tips meet along its inner side.

The feather is thus in early stages curled into a cylindrical form round the central dermis or pulp-—the whole being enclosed in a continuous sheath which disintegrates sooner or later setting free the elastic barbs and allowing ‘them to flatten out to form the vexillum or vane.

As is well known the barbs are united together in the fullydeveloped feather into a functionally continuous web, through the agency of the barbules which project from the two sides of the barbs much as the barbs do from the rachis. The mode of origin of the barbules is seen in a longitudinal radial section through a barb such as that shown in Fig. 42, G, where the outer portion of the barb rudiment is seen to be splitting up into barbules (121)) while its inner portion remains continuous to form the definitive barb (I2).

Traced downwards, towards the base of the feather, the raehis increases in width so as to extend round the whole periphery of the feather rudiment. Its outer layer assumes a translucent character and forms the cylindrical gculll (calamus), the basal end of which becomes somewhat narrowed, bounding the umbilicus, the opening through which the dermal pulp extends up into the interior of the quill. The pulp of the feather undergoes a gradual shrinkage leaving behind it the series of cornified caps (H, 0) formed on its apical surface as already mentioned and which eventually lie loose within the quill.

The lips of the umbilicus are continued (Fig. 42, H) into a deep rim of uncornified epidermis (g). This with the dermal papilla projecting into the feather base remains inactive until the period of moulting when it springs into activity, grows rapidly, and becomes converted into a new feather which pushes the old one out and takes its place.

The scales which frequently occur upon the legs and feet of birds are probably not, as might at first sight be supposed, to be looked upon as having persisted from the Reptilian condition. They frequently bear feathers in the young condition and are probably secondary developments replacing an earlier feathery covering. I

In view of the convincing evidence offered by comparative anatomy and palaeontology we are compelled to believe that Birds have been evolved out of Reptile-like ancestors. Accepting this 74 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

view and having regard further to the fact that Reptiles are typically covered with a coating of scales, we may safely also accept the view that feathers are to be looked upon as highly specialized and modified scales. While the mode of development of the feather fully substantiates this hypothesis, perhaps the most interesting point that emerges

FIG. 43.———lllustrating the neonychium or claw-pad in the developing Bird. (From Agar, 1909.)

A, median longitudinal section through the claw of a chick of 19 days‘ incubation. B, claw of a chick taken in the act of hatching. Thu nconychium is seen beginning to break away from the rest of the claw. C, sa-ction similar to A, but from a chick 12 hours :1fLcr hatching. 4.-.32, claw-plate; as, sole of claw ; n, claw-pad (nuonychiuni).

from its study is that the successive sets of feathers———the down feathers of the nestling, and the annual or other sets of feathers in the adult——are not to be looked on, as has been customary, as successive series of independent individual feathers. On the contrary the down. feather and the definitive feathers, which succeed it in the series of inoults, are all simply portions of a single greatly elongated and basally growing structure--——the first down feather being its tip, and the succeeding feathers being successive portions of it. The moult consists not in the shedding of the whole feather but merely in the breaking off of its projecting portion.

Claws, which make their first appearance in Anura (Xenopus), arise as special developments of the horny layer ensheathing the tip of the digit. To produce and retain a sharp edge or point by differential wear the claw is normally of denser consistency and harder on the dorsal side and laterally, forming the “ claw-plate ” (Boas) (Fig. 43, C, (3.19), while on the ventral side it forms the softer “sole” of the claw (Boas) (Fig. 4.3., C, c.s). A Neonychia or Claw-pads.—-To the embryo of an Amniotic Vertebrate, enclosed within its delicate membranes, the possession of sharp claws on the digits would obviously be a source of considerable danger during the later stages of development when the embryo moves its limbs, because of the liability of such structures to tear the foetal membranes. This danger is obviated by a beautiful adaptive arrangement which has been described by Agar (1909).

In the embryo, the concavity on the lower side of the claw is completely filled up by a soft rounded pad or cushion (Fig. 43, A, 71.) formed by a thickening of the horny layer of the epidermis superficial to the sole of the claw. Agar has given the name N eonychium to this structure. In addition to mammals, which do not concern us here, Agar has studied these claw-pads i_n the Fowl and in the Lizard Tejus

and there can be no doubt that the expanded

claw-tips observed by Rathke (1866), Voeltzkow ““.‘ T“"""'“i*‘='~'l" 1T°"“,”"” ' lunh of ill! eml)1'_y0 bro (1899) and Goeldi (1900) in Crocodilian (Fig.44) (,(,,m._. ,,1,,,m, W, ,,,.,,,t;,_., embryos are the same structures and it seems after twinm-itiuu, show

probable that they will be foundto occur in lt.'_.k w, claw-bearing Amniotic Vertebrates generally. ‘1§§,l5,_)( 9 W I 0

The neonychia are purely foetal structures which become detached soon after hatching (Fig. 43, B and C) leaving behind the functional claw.

Jaws and Oral Combs of Anuran larvae. -——Amongst the most interesting developments of the horny layer are the jaws and oral combs of frog tadpoles. The buccal opening is bounded by an upper and lower horny jaw, and external to and roughly parallel with these are rows of little horny denticles which form the oral combs and are used for fraying out the food. The number and arrangement of these rows of denticles-—“ upper labial” and “lower labial” ——-differs in different Anura and 1.11:,-.5’ afford useful characters for the identification of tadpoles (see Boulenger, 1897).

The horny jaw is composed simply of a row of denticles so closely apposed as to be in contact. The terminal fl11'1(_+li0nal_ portion of each dentiele is seen in longitudinal section (l<‘ig. 4:3, A and B) to be composed of a series of hollow cones of lmrd horny materi:1.l which closely ensheath ‘one another. The tenninal cone as it undergoes wear and tear eventually drops oil’, its function being taken over by the cone which it previously ensheathed. 76 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

These cones form simply the terminal members of a series vyhich extends inwards in the form of a curved column nearly to the mner surface of the epidermis. Only the terminal members. are strongly cornified, the other members showing less and less cormfication until at a little distance down the series the cone is seen to be composed of unmodified protoplasm containing at one side, near its base, 21.

Flu. 45.— Illustrating; the development of the larval teeth of Tadpoles

A, H, C. l*‘ulmI'icolu j'usvum.aculum ; I), Ihmu tcm.;mr¢Lriu_.. (I) at'tv1-(‘mtzeit, 1889.)

nucleus. The cone is in fact simply a cornified cell. Traced towards the base of the column the cells are seen to be composed of more granular protoplasm and to have not yet developed a hollow, while the extreme base of the column is formed by an initial cell of comparatively small size and flattened shape.

The whole column is seen, then, to be composed of a sequence of conical teeth forming a replacement series, each tooth being a single cornified cell.

The jaw, composed of a closely set row of such columns, is supported by the neighbouring parts of the epidermis which also undergo a certain amount of cornification. Thus just internal to the jaw is a cushion—like mass of large slightly cornitied cells which forms an efficient backing to it (cf. Fig. 45, A and B) while external to the jaw the surface of the epidermis is composed A ,3: of flattened much I cornified cells (Fig. T. _ _ " 45, A). ' . '

The oral combs consist of a pallisade— like arrangement of similar denticles which however in this case are not in contact. Fig. 45, C, shows a longitudinal section through the posterior labial comb of Palacdvlcolot. Here again we see a successioncolumn of epidermal cells commencing with a small initial cell near the inner surface of the epidermis. From the initial cell outwards the cells increase in size,become gradually cornified and each one fits closely into the base of the next one which becomes more and more deeply excavated as the tip is approached.

Two conspicuous differences distinguish the denticle of the A‘__u_“‘_1_.BWN_M_ I ]_ g oral O0]-nb from of , }l)€-l})lll£,l; is-, llL111utio1liil-siiiiuz2I.3i11:’);:31;);.’ll:;li::::m:'"MI the jaw: (1) instead I A I of being regularly conical in shape it is claw-shaped with serrated edges (Fig. 45, D) the tip being recurved, and (2) the hollow base of the cornified cell is not entirely occupied by its successor in the series: it also accommodates an indifferent cell of the epidermis (supporting cell of Gutzeit) which bulges into it.

I have described the development of these interesting structures

Fm. 46.——Vertica1 section through lingual spine of Pet1'o7nJ/sort. (After \-‘Varrcn, 1902.) 78

as they occur in a. South American tadpole (.Pal'u.d'icola.)‘ but the description [its quite well the mode of development as it occurs in

_|<‘I<:. ccuu-mt — organ sagittul M.-«_'.t.ir'n1|~.

47.--——|ll11sll':'ltlng the «lu.vulopIm_-..nl.. of the

of Ln/"M/_o.s'ira'n as S0011 in

A, 8t&lg'I' 132-}; ll. .‘-l.'l_'_;¢‘ ‘_'."i; (,'. .~l.'1_:.'~‘ til : I). Sim.-;v-. 35. In Atlle rualim:-nl. ml‘ the 4-1-lllvnl -4-I-;_;:iI1 is .\‘I'o'H tn) lw :i tliickcning or llw «lo-up I.-nya-r of tho 0‘(5l(_)Il|‘l'lll: in I; anal (3 th«- !~‘.|l|H'l'lll‘l.'|l l.'l_\'t‘l‘ has IllS:l1)]M':lI‘I‘(l m‘--r thot.lii«-lu-nu-«I _-.-,1.-uulului-:u.-:u ; in I) t-lu- m-;.-,:m is <:ommvn ring 1o.-In-iv:-l and i-1'o\\-«ls of pli:igo(-._\'l«.-s :m- 1-ollI'ct.-ml in its nu.-igliliuiurlmod.

Tadpoles generally (Keiffer, G utzeit), the differences be tween different species and genera, though of systematic importance, being differences in detail. such as sl1ape and arrangement of the individual teeth of the comb. ' “Teeth” of Cyclostomes.-The horny teeth of cyclostoniatous fishes, though they would naturally fall to be treated in the next chapter, situated as they are within the buccal cavity, may conveniently be considered n0W owing to their resemblance—on a much larger scale and with multiccllular structure—-—to the horny denticles of the tadpole. The tooth-like spines of the eyclostome are cones of highly cornified epidermal cells. Each tooth develops in the substance of the epidermis (Fig. 46, A) being strikingly like a hairrudiment during early stages. Successional spines develop beneath the bases of the functional ones as shown in Fio‘. 46. GLANDULAR DEVELOPMENTS 01? THE ErInEuM1s.—In the Anamnia it is usually the case that scattered cells of the epidermis take on a glandular function and serve to form a slimy secretion which amongst other functions serves to diminish the “ skin-friction ” which is the main resistance to movement through Water. Such unicellular glands may become collected

together to form multicellular glands. Of these the most conspicuous examples are found, outside the Mammalia, in the Lung-fishes and Amphibians--where they form the flask-glands and the cement—organs.

1 Probably P. fusconmculata according to Boulenger.

‘The flask-glands of Lung-fishes and Amphibians develop in the ilirst instance as solid local proliferations of the deep layers of the epidermis which grow down into the subjaeent connective tissue of the dermis and form a lumen by secondary excavation. The fully developed flask-gland is ensheathed in a coat of smooth muscle-fibres and it is an interesting fact that these are believed to be developed from the cctodermal cells of the gland—rudiment.

Cement-organs of apparently ectodermal origin occur in two out of the three surviving lung-fishes-——P7'0toptea‘-as and Lep'£¢7los1Ir(m—and form conspicuous features during late embryonic and larval life (see Fig. 200, F, Chap. VII.). ' In an embryo of Lepz'dos7S~re'n three days before hatching the cement-organ forms a crescentic structure stretching across the mid FIG. 48.——Embryos and larvae of Bufo ':m,_7_qu..n'.s tn sllmv the cement-organ upon the ventral surface. (After 'l‘hiele, 1887.)

ventral line with its concavity forwards, just behind the position in which the mouth will appear later. About stages 32-34 the organ is at its maximum development and forms a large prominently projecting structure ventrally below the opercular region. Towards the end of larval life the cement-organ commences to atrophy, the process being furthered by its invasion by crowds of phagocytes, and in a short time the organ has completely disappeared.

The cement-organ is a derivative of the deep layer of the epidermis. It commences as a slight thickening of this layer (Fig? 47, A) the cells assuming a tall columnar form. These columnar cells become the secretory cells while the superficial layer of the ectoderm breaks down over them so as to expose their outer ends (Fig. 47, B and C). It is to be noted that there is no trace whatever of any connexion of this cement-organ with the endoderm: it is ontogenetically a purely ectodermal structure (see, however, p. 181).

Cement-organs of very similar appearance are found in the larvae of many Anura. In this case they appear very precociously in development, being indeed in some cases the first definite organs to become visible on the surface of the embryo. Fig. 48 illustrates the development of the cement-organ in the common toad (Bufo vulgaris) from the time of its first appearance up to the time of its atrophy. The organ is seen to be at first crescentic as in Lepidosdren then to become V-shaped and finally to become paired by the atrophy of its median portion.

When at the height of its development, the cement-organ shows characteristic differences in form and position in diiferent species of Anura and is consequently of use in identifying the species. of Tadpoles.

The general appearance of the Anuran cement—organ as observed in sections is illustrated by Fig. 49. The glandular layer is commonly said to belong to the superficial layer of the ectoderm but this does not seem by any means certain.

Pigment of the

Skin.-——One of the con |<‘:«:;‘..1u. '.‘lul'l.l()ll l.ln'ougln .tl1egccn1e1l’t-organ of a l*‘rog spicuous features ofthe hulpnla (Rum! /4-.-m-,mu-u.m1.) 8 mm. 111 length. (From Skin in the majority of

ASSMOII’ 1896') _ I , _ _ _ Vertebrates is the fact (.'.‘0, cc-nit-int-t):::::t:Lt}:n‘Lfgt’ .h:.1.}.:r-r’l‘l(‘-‘1(:‘n£nl::‘yI:-lg:al vctmlu-1-m, is coloured the deposition within it of excretory matter in the form of pigments. This is of physiological importance to the organism in two different ways, firstly in that it gives to the particular species its characteristic coloration, and secondly it serves to protect the underlying living tissues from the harmful influence of light rays.

A certain amount of pigment may be formed within the protoplasm of the ectoderm cells. For example in frog tadpoles of about an inch in length, numerous fine granules of melanin are crowded together near the surface of the outer layer of ectoderm cells, just beneath the cuticular superficial layer.

But by far the most important part of the pigmentary system of Vertebrates consists of mesenchyme cells with pigment-laden cytoplasm which are positively heliotropic during life and creeping by the extrusion of slender pseudopodia, like those of Foraminifera, crowd together immediately beneath the ectoderm and form there a l.ight-proof layer, some of them even wandering into the substance of the ectoderm between i.ts constituent cells}

The chromatophores, during the process of development, commonly become specialized in different directions so that in the fully developed

1 The interpretation of the branched clirmnatophores as mesenchymatous in origin appears to the author to accord best with observation but it should be mentioned that some regard them as modified ectoderm cells, as_,for instance Winklcr (1910). II THE SK_IN AND ITS DERIVATIVES 81

condition several distinct types may be recognized. Thus in Lepidosiren the most abundant type of chromatophore is characterized by the stout projections of the cell-body which carry the finer pseudopodia and by the somewhat brownish pigment granules. A less abundant type has long slender, less richly branched and often varicose pseudopodia with dense black and opaque pigment granules. Still another type of chromatophorc has its protoplasm charged with bright yellow pigment.

The melanin pigments are probably to be looked upon as waste products of cell metabolism. They are iron-containing pigments and during at least the later periods of development their produr tion is commonly associated with the breaking down of that other great iron-containing pigment——haeinoglobin.

Their production is also related to the degree of activity of the cell metabolism. Thus, in the male Lepidosiren, at the close of the breeding season, when the moribund remains of the richly vascular respiratory projections of the hind limb are being devoured by crowds of voracious phagocytes, there takes place an active formation of melanin.

Again melanin apparently tends particularly to be produced when the cell metabolism of comparatively unspecialized cells is interfered with by the prolonged action of light-rays. Thus as already indicated the layer of protoplasin in the egg which is turned towards the light frequently develops melanin granules. Again in developing eyes it commonly holds that comparatively unspecialized mesenchyme cells wandering into the zone of exposure to the light deposit melanin granules in their cytoplasm.

Cells then which become chromatophorcs may be regarded as cells which are specially sensitive to light-stimulus and whose metabolism is liable to be so modified thereby as to produce pigment.

Although it is reasonable to suppose that melanin-formation is primarily related to the influence of light it must not be forgotten that, as indicated in the preceding chapter, the actual laying down of pigment in the case of species where it has become a specific character may take place under circumstances in which the lightstimulus is incomparably more feeble than that which probably originally brought about pigmentation in the course of phylogenetic evolution, as e.g. in the case of the ovarian egg of the frog. That pigment -formation during individual development still remains linked up with exposure to light is shown by the frequency of the unpigmented condition in Anuran larvae which develop in water rendered opaque by fine clay held in suspension (Wenig, 1913).

To illustrate the dependence of pigment-formation upon light during individual development the case of young flatfish (Pleuronectidae) is sometimes quoted, where the shading of the upper and the illumination of the lower surface during development brings about a reversal of the ordinary colouring (Cunningham, 1893). It is possible however that this reversal of colouring is due merely to the strongly heliotropic tendencies of the chromatophores which lead them to migrate actively towards the illuminated side and there to remain. The chromatophores of Vertebrates often display their sensitiveness to light very markedly by movement reactions. Such are well seen in the young stages of many fishes and Amphibians. In the young Lepidosiren for example the chromatophores duri.ng the day have their pseudopodia extended in all directions and their bodies flattened out into a plate-like form so that they constitute a lightprnof coat giving a rich

purplish-black effect. At dusk the pseudopodia become slowly withdrawn so that a few hours after darkness has set in the chromatophores have shrunk into minute spheres so wide apart as to have no influence on the general colouring. The young fish is then practically colourless except for the large yellow chrornatophores here and there which remain expanded. FIG. 50.---Section through ('.pl(l(‘.l‘llllS of Lepvldoszlreln Dunng the course of 1;”-V.-u.._ development in many fishes, A. lixml nmlvr comlilions of «lull tlayliglnt; B, under ainurous Amphlblans’ and a’ crmtliliunsul'<l;n'l<m-sstlIn'in;.:l.l1enig'lIt. ('l‘lIv chroma- few RBIJUICS Such as the

tophores in the dermis, nrhich crowd together under the chalneleon’ the compara inner surface of the epidermis are not shown in A.) - - . ,- , 7», cll1'()1ll:ll'.I)])h0I'(‘-', av, l_)loo(l-vessel. tlvely Sllnple reactions to

light such as have just been indicated develop into reactions of a much more complex type in which the central nervous system is involved. Research into the development of these more complex reactions is highly desirable for at present little is known regarding them. »

Nervous System

The nervous system, which has to do with the receiving of, and the reacting towards, impressions from the outer world, appears to have arisen in evolution, as might have been expected, from the outer layer or ectoderm. The first steps in the evolution of the Vertebrate nervous system are not within the scope of direct observation but the view is probably correct that it arose from a diffuse subepidermal network or plexus of the type still persisting in some of the more primitive invertebrates. 111 the development of the Vertebrate embryo the main parts of the nervous system may stillphe seen to take their origin from the ectoderm.

Origin of the Central Nervous System

The first obvious trace of the central nervous system consists of a thickening of the ectoderm of the dorsal surface of the embryo. This thickening extends forwards from the anus, or from a point slightly behind the anus, to the head region, and is termed the medullary plate. The thickening of the medullary plate is due primarily to the ectoderm cells, or where two layers are present, to the deep-layer cells of the ectoderm taking on a tall columnar form.

There is also growth in area of the mcdullary plate and this, in conjunction with the binding down of the medullary plate along the line of the notochord and primitive streak, causes it to become curved from side to side so as to form a gutter or groove~—the medullary groove. The, usually conspicuous, lips of this groove are known as the medullary folds.

As the medullary plate keeps on increasing in width it bulges downwards and laterally into the surrounding mesenchyme and assumes the form of a longitudinally placed tube with a slit along its dorsal wall representing the original opening of the groove.

Finally the lips of this slit grow towards one another and undergo fusion, so as completely to close in the neural tube, which now separates off from the ectoderm of the outer surface. The closing in of the neural tube commonly commences in the binder head region and spreads from this point forwards and backwards.

An interesting modification of this normal mode of origin of the neural tube is found in the case of Lampreys, Lepidosiren and many of the tclcostomatous fishes. In this modification of the typical process the increase in bulk of the medullary plate leads to its growing downwards into the underlying tissue as a solid keel. In the middle of this at first solid rudiment a cavity appears secondarily either by the development of a fine intercellular split or by the cells along the axis breaking down. The cavity so formed gradually dilates and eventually there is a neural tube agreeing with that of normal forms.

The neural tube which has originated in the way described is the rudiment of the central nervous system, its anterior portion becoming relatively enlarged to form the brain while the remainder forms the spinal cord. .

The central nervous system during the period of its development gradually attains to a condition of the greatest complexity and all that will be attempted here is to give an outline sketch of the more conspicuous changes which take place in its general form and in the arrangement of its parts without going into minute detail.

Spinal Cord

The spinal cord remains throughout life in the form of a tube the lumen of the tube becoming relatively insignificant while the walls become greatly thickened especially laterally. The relatively small size of the lumen (central canal) is not, as a rule, due merely to its retaining its embryonic dimensions while the Walls of the tube are growing in thickness. On the contrary actual occlusion of part of the lumen takes place in the great majority of the lower Vertebrates. The side Walls of the tube approach one another so as to convert the rounded lumen into a vertical slit and finally they come into contact and fuse so as completely to obliterate the cavity except in its ventral portion which remains open as the definitive central canal.

In the ease of the Bird-—in which the process has been worked out in detail (see ltamcin y Uajal, 1909) the. increase in thickness of the wall of the neural tube is due primarily to the cells composing it taking on a tall columnar form-—-the individual cell extending right from the central canal to the outer surface. The cell-body becomes very attenuated, with a marked dilatation containing the nucleus. The nuclei become necessarily situated at difl'erent levels and this in an ordinary transverse section obscures the fact that the wall is still composed only of a single layer of cells.

With subsequent development the cells become dill'erentiated into those which are actually nervous and those which remain relatively indifferent and fulfil a mainly supporting function. The latter continue for a considerable period to traverse the whole thickness of the wall. They increase greatly in length: their form becomes more and more attenuated the greater part of their length becoming practically filamentous with small irregular projections and varicosities, while_the portion nearer the central canal, in the course of which the nucleus is embedded, remains somewhat stouter.

The presence of such supporting cells traversing the Whole thickness of the wall is only temporary: in later stages they are replaced by the greatly branched neuroglia cells. While many authors have taken the view that these latter are to be regarded as immigrant mesenchyme cells——-a View that has weighty general considerations in its favour——-Ramon y Cajal and others have adduced strong evidence to show that they are simply the original supporting cells which have withdrawn, or lost, their internal and external portions and assumed a complicated branched form.

In addition to the comparatively indifferent supporting cells which have just been mentioned there are present in the wall of the neural tube the numerous elements which are destined to become actual neurones or nerve-cells. Such embryonic nerve-cells have been termed by His neuroblasts in contradistinction to the nonnervous elements or spongioblasts.

At first isodiametrie these cells like their neighbours take on a tall columnar shape stretching throughout the thickness of the wall: their terminal portions become more and more attenuated and they present a spindle-like (bipolar) appearance. Later their shape becomes pearlike the stalk being prolonged into a nerve fibre (neurite, axon) while finally the development of branched projections (dendrites) brings about the definitive multipolar condition.

These developing neurones lie ‘in the spaces between the indifferent cells and from an early stage (third day in the case of the fowl embryo) the use of appropriate methods reveals the presence of neurofibrils in their protoplasm. The tail-like prolongation of the neurone which forms the neurite or axon is still believed by the great majority of workers to arise as an actual outgrowth of the cell body as was taught by His. Others regard the appearances upon which this belief is based as being probably deceptive, as will be explained later.

The longitudinal axons of the spinal cord are concentrated in its outer layers forming the “ white substance ” of the early anatomists. This makes its appearance as a rule in the more primitive Vertebrates as a continuous layer and in the higher forms as a sharply separated dorsal and ventral portion upon each side.

The enclosure of the axons in the insulating medullary sheaths commences only within a few days of the end of incubation, in the case of the bird, and at similarly advanced stages of development in other Vertebrates. The sheath is generally believed to be secreted by the protoplasm of the axon. Its formation tends to take place approximately synchronously in all the axons belonging to a particular group. This fact, in conjunction with the use of specific stains for the insulating substance, facilitates the mapping out of the various groups of axons.

The spinal cord, like the rest of the central nervous system, becomes invaded during ontogeny by immigrant mesenchymatous tissue. This provides the capillary network which traverses the nervous tissue, in addition doubtless to many other elements of a less conspicuous kind.

A curious detail which is noticed in studying sections of developing spinal cord (or brain) is that the active cell-multiplication is confined to the layer next the central cavity, in other words to what was originally the superficial region of the ectoderm. This is in striking contrast with the general cetoderm of the surface of the body where cell-multiplication is confined to the deep (Malpighian) layer.


The anterior portion of the neural tube becomes enlarged and dilated to form the brain and this gradually becomes so modelled as to present the various regions seen in the brain of the adult. The general course of this process will first be sketched as it occurs in Lepidosrren one of the lower gnathostomatous Vertebrates in which the egg is holoblastic.


The brain rudiment becomes apparent as a slight enlargement of the neural tube. The first sign of differentiation is

- the appearance of a constriction marking off the primitive fore-brain

or cerebrum (archencephalon of Kupffer) from the primitive hindbrain or rhombencephalon. As development goes on this boundary becomes specially marked ventrally where the floor of the brain bulges upwards into the cavity as a transverse fold ‘ (see Figs. 52 and 53, f).

‘ This fold may in other vertebrates make its appearance before the medullary groove is covered in. This is shown clearly in Polypterus-—Fig. 80, B, p. 146. The side wall of the hind-brain now comes to project outwards as a prominent knob while the side wall of the fore-brain also bulges out—

Fm. 51.——Brain of young IA‘-}ll(l()h'll'(‘ll as seen from the (lm"S{1l side.

A, .s't:i;.:t'* 3l+: B. :-:t.:|_«.,»'u- :55--— ; ('.'-, .~'i:|;,-‘u 38; I"), zulult. c.II, cerebral lu=.mi.~;plw1-c; n.u, lll'Hl':Il :n-(-h; _p£n, pin:-:|l lnNl,\-': ,-h., rlmmIn-In-4-pllillnn; Hml, Llmlaniencephalon; t.o, tectum optic-um. I, II, «-I«-., mmuiul nu-rws. [l<‘i«,gs. A and 13 um nun-u hi;_-'hl_\' umusnified than C, and Fig. C than D. "I

wards—the bulging in this case. he_ing- the rudiment. of the cerebral hemisphere (Fig. 51, A, c.I1).

The portion of the primitive fore~brain lying just in front of the transverse fold of the brain-floor is— the infundibulum. Farther forwards the inner surface of the brain-floor forms a transverse into tmlamencevhalic and mesencevhalic Orbions groove hounded behind and in front by a slightly projecting ridge-~ the rudiments of the optic chiasina. and of the anterior commissure respectively (Fig. 53, ch, a.c).

About stage 31 a little pocket-like diverticulum of the roof of the primitive fore-brain makes its appearance (Fin. 53, D, pin). This is the pineal body and -its appearance is of topographical importance as serving to demarcate the primitive fore-brain roof

FIG. 5'3.-—~Brai11 of young Lepidosiren as seen from the left side.

A, stage 20.; B, .s'l..:|_-.40. 31 ; (3, sl.:tge 35- ; D, stage 39. c.H, cerebral lu!lui.s'plm1'n; f, primitive fold of lu'uin-llnnr; -in_/; in1'muIil_mlmn; o.h_, ulf.-u-tury bulb; o.t, olfactory tubercle; pin, pineal body; (,I¢_.u(._ |.huhum-I|c«-pl1:1l(m; I.u, tact.-"um upI:'v'21.:n.

The lateral bulgings of the fore-brain have become more prominent and now project forwards beyond the limit of the rest of the fore-brain. In the mesial plane between the two hemispheres there projects upwards and forwards a little pocket of the anterior wall of the fore-brain. This is the rudiment of an organ of unknown significance———the paraphysis (Fig. 53, D, par). .

Soon after the appearance of the pineal body the roof of the primitive fore-brain becomes divided into a posterior portion belonging to the mesencephalon and an anterior portion belonging to the thalamencephalon (Fig. 51, B, 5.0, and thal). As development goes

‘FIG. 53.——Camera tracings of sagittal sections through the brain of Lepidosircn, at successive periods of development.

Figs. A to F urn drawn nndvr tho szuno magnification, Fig. 0 under :1 lower magnification. A, stage 25; B, stage 28; 0, stage 29+; D, stage 31; E, stage 35; F, stage 88; G, adult in second year. a.c, anterior cominiszeuro; oer, cerebellum ; c.H, cerebral hemisphere; ch, optic chiasma; f, primitive fold of brain-floor; h.g, ganglion liabenulao; h.c, lmbe-nular (superior) commissuro; Lg, infnndibular gland ; inf, infundibulum ; par, purapliysis ; pin, pineal body; p.c, postorior commissuro ; 1.1», choroid plexus of lateral ventricle: (.0, teolum opticum ; * originally anterior mug of brain-floor. Structures occurring not in the sagittal plmw but in sections parallel to but some distanco from it, arv shaded with oblique lines.

on the constriction between thalamencephalon and mesencephalon becomes more marked. The roof of the former remains thin and membranous, forming the cushion-like dorsal sac upon which the pineal body rests. 'l‘he .roof of the mesencephalon becomes slightly thickened on each side of the mesial plane forming the tectum opticum but correlated with the small size of the eyes in Lepidosiren the thickening never becomes so great as to produce projecting optic lobes such as are formed in most Vertebrates.

In the hind-brain region the greater part of the roof, covering in the fourth ventricle, becomes thin and membranous. Across the anterior boundary of the hind-brain the roof does not undergo this secondary process of thinning but persists as a transverse thickened band—-the rudiment of the cerebellum.


RHOMBENCEPHALON or Hind-Brain.——The hind-brain, correlated perhaps with the fact that it contains nerve—centres of supreme importance to life, develops precociously and reaches a relatively enormous size during early stages (Fig. 51, A, rh). The bulging inwards which marks its anterior limit is doubtless to be regarded as an expression of the active growth in length of its floor during these early stages.

During later stages of development it forms a conspicuous projecting restiform body on each side reaching forwards nearly to the anterior limit of the inesencephalon but this becomes again less and less prominent as the adult condition is approached. The cerebellum retains through life its primitive condition as a simple transverse thickening of the hind-brain roof.

MESENCEPHALON.-——Tl1e roof, as already indicated, becomes thickened somewhat on each side (tectum opticum) but not to such an extent as to bulge outwards and form optic lobes. Close to its anterior limit a conspicuous bridge of transversely-running nervefibres makes its appearance at a late stage of development. This is the posterior commissure—-an important brain landmark (Fig. 53, Gr, 19.0).

THALAMENCEPHALON.———The side wall of the thalamencephalon becomes greatly thickened to form the optic thalamus which bounds on each side the slit-like third ventricle. The roof becomes for the most part thin and membranous forming the dorsal sac. On either side of the pineal body however it becomes greatly thickened to form the habenular ganglion. As these ganglia develop a bridge of transverse nerve-fibres makes its appearance uniting them-—the superior or, better, habenular commissure.

The pineal body as development goes on enlarges somewhat and assumes a carrot shape. Its lumen becomes obliterated posteriorly so that it no longer opens into the third ventricle. The anterior isolated part of the cavity becomes eventually almost filled with granular material produced by the breaking down of the epithelial linin .

Tghe paraphysis forms for a time a conspicuous tube passing upwards and forwards in the space between the two hemispheres and ending blindly. In later stages of development it undergoes a relative reduction in size, and becomes irregularly twisted and mixed up with the choroid plexus of the ventricles.

On either side of the paraphysis and just dorsal and posterior to its base, the wall of the brain becomes involuted into the third ventricle, the iuvoluted portion being thin and membranous and enclosing an ingrowth of blood-vessels. This vascular ingrowth represents a structure which in most Vertebrates is continuous across the mesial plane with its fellow so as to form an unpaired structure the velum transversum. This is regarded by most writers on the brain as an important landmark i11 brain topography.

On the floor of the thalamencephalon the optic chiasma and the anterior connnissure form prominent bulgings into the ventricle. Each develops nerve-fibres in its substance, connected in the one case with the organs of vision and in the other with the cerebral hemispheres, especially those portions devoted to the sense of smell.

In front of the optic chiasma lies a deep optic recess which is prolonged outwards by an outgrowth of the side wall of the brain, the optic outgrowth, which gives rise to a great part of the eye and will be gbscribed later. Behind the chiasma is the infundibulum, the tip of which at a late stage in development (about stage 38) sprouts out into narrow tubular diverticula. These increase in length, wind hither and thither, and partially penetrate into the substance of the pituitary body which lies immediately beneath. The epithelium of these tubular diverticula assumes a glandular appearance and together they constitute the “ infundibular gland ”-— often called the “nervous portion of the pituitary body.”

The series of sagittal sections in Fig. 53 is of interest from its bearing upon a question which has excited some discussion, namely as to what point in the fully developed brain of the vertebrate corresponds to the morphologically anterior end of the brain rudiment in earlier stages of development. It has been held by many morphologists, such as V011 Baer, His, Sedgwick, that the tip of the infundibulum represents the anterior end of the primitive brain, the present condition having been brought about by the anterior portion of the brain becoming bent upon itself into a retort shape. As will be seen by an inspection of the figures the brain of Lepidosiren lends no support to this idea. On the contrary the tip of the infundibulum clearly corresponds to a point close to the letter A of Fig. 53, A. On the other hand, equally clearly the anterior tip (*) of the brainfloor of an early stage such as that shown in Fig. 53, B is represented in the adult by a point well up on the anterior wall of the thalamencephalon (lamina terminalis) and just ventral to the root of the paraphysis.

CEREBRAL HEMIsPHEREs.— The hemispheres arise as bulgings of the side wall of the fore-brain. As development goes on they increase in size and grow first dorsalwards and later on forwards until in the adult they are relatively very large. This increase in size is associated with a corresponding growth in the thickness of the wall of the hemisphere——except at its hinder end next the thalamencephalon. Here the inner wall of the hemisphere facing the thalamencephalon remains relatively thin.

About stage 35 a small rounded portion of this thin part of the hemisphere wall bulges into its cavity—the lateral ventricle. This ingrowth contains a vascular loop and is the rudiment of the choroid plexus of the hemisphere or lateral plexus. The plexus grows rapidly into the ventricular cavity, forming an irregular crumpled lamina which in the adult attains to great size and complexity traversing thelwhole lateral ventricle (Fig. 53, F and G, 1.)»). No doubt this, by diffusion between the blood in its vessels and the fluid in the lateral ventricle, helps to provide for the nutritive and respiratory needs of the hemisphere wall.

During the later development of the hemisphere its walls become differentiated into regions in the manner described by Elliot Smith (1908). Most important from the point of view of general vertebrate morphology is the fact that a distinct cortex is developed in the form of a layer of ganglion-cells traversing the roof of the hemisphere parallel to its surface, and at about one-third of the distance from the surface to the ventricular cavity. This cortex extends on the one hand just on to the mesial face of the hemisphere and on the other to a point rather more than one-third of the distance from dorsal to ventral edge on the outer face of the hemisphere.

Of this cortical formation, which constitutes the archipallium, the mesial portion corresponds to the hippocampus of higher vertebrates, and the outer portion to the pyriform lobe. The neopallium which in the higher forms becomes interposed between these does not appear yet to have become distinctly recognizable in Lepidosiren.

Less important from the point of view of general morphology but more conspicuous in their structural expression are certain changes which take place in relation to the olfactory apparatus.

The portion of hemisphere wall to which the first cranial nerve is attached——the olfactory bulb—is at first simply part of the lateral wall of the hemisphere but as development proceeds it is found to take the form of a sort of cap lying on the dorsal side or roof of the hemisphere at about the middle of its length as viewed from above. This change in position is brought about by an enormous hypertrophy of the portion of the ventral wall of the hemisphere which lies in front of the optic ehiasma—the olfactory tubercle.

Later on, from stage 38, the portion of hemisphere roof lying posterior to the olfactory bulb undergoes active growth in length with the result that the bulb is gradually carried forwards and 92 EMBRYOLOGY OF THE LOWER V ERTEBRATES CH.

eventually comes to lie right at the anterior end of the hemisphere (Fig. 52, I), 0.7)). At the same time the bulb comes to form a definite hollow projection of the brain surface immediately dorsal to the still greatly enlarged olfactory tubercle (0.6).

l)1l+‘l+‘EREN'1‘IA'1‘ION or THE BRAIN REGIONS IN ACANTHIAS. The development of the brain of Elasmobranchs has been worked out by Kupii'er (1906) for Acu/at/1/ias and his account has been made use of ill writing the following short smnmary.

Figures of the early stages of the medullary plate as seen in surface view are given in Chap. XI. The medullary plate projects forwards from the posterior boundary of the blastoderm and is raised well above the general surface. As it increases in length its lateral edges become raised up so that the portion on each side slopes inwards and dowmvards into a kind of valley. Each hall‘ of the mcdnllary plate extends back into one of the “caudal lobes" which with growth in length come to project freely beyond the edge of the blastoderm.

Another result of the increase in length is that the anterior end of the medullary plate comes to project freely forwards over the blastoderm forming a head-fold. Each side of the mednllary plate arches inwards towards the mesial plane and the whole becomes converted into a neural tube in a perfectly normal fashion.

As in the case of Le1)'i(l0si'I'cn, the first sign of dif'f'erentiation of the brain into its parts is a division into primitive fore-brain (Archencephalfii) and hind-brain. The demarcation is again most distinct ventrally where the brain-floor bulges into the ventricle (Fig. 54, B) as a prominent fold. Later on this fold spreads upwards on each side to the dorsal surface forming the rhombo-mesencephalic fissure which marks oil’ the mid-brain from the hind-brain. It is only at a later stage in development that the mesencephalon becomes marked off by a constriction from the anterior portion of the archencephalon which forms the thalamencephalon.

It is of interest to compare sagittal sections through the brain of the Elasmobranch with the corresponding sections already described for the holoblastic lung-fish. N egleeting small differences in detail there is seen to be a striking difference between the two brains-most marked in the middle stages figured—in relation to the longitudinal axis. In Fig. 54, C the Elasmobranch brain is seen to be as a whole strongly curved in a ventral direction: it shows a high degree of “cerebral fle.1u11'e.” The corresponding stage of the Dipnoan brain is on the other hand almost straight, the superficial appearance of curvature being due mainly to the prominent fold of its floor which projects up into the. cavity at the level of the mid-brain.

This cerel_»ral fiexure, which is especially conspicuous not only in the brain of the Elasmobranch but also in the other types of Brain (Mammalian and Avian) that were. first investigated developmentally, has played a large part in discussions on brain morphology. Thus the idea, already alluded to, that the tip of the infundibulum is the morphologically anterior end of the brain rests upon it. II BRAIN 93

That this idea is unsound. seems clearly to be indicated by such series of sections as that shown in Fig. 53. As a matter of fact it

FIG. 54.———Sagittal sections through the brain of A mnthms. (After Kupffer.)

A, 3-8 mm. embryo; B, 7-8 mm. ; C, 10 mm.; 1'), ‘.27 mm. ; E, 70 mm. cm-, cerelwllmn; ch, optic ehiasma; eat, external (‘.Ct()d(‘.I'1Yl; h.c, habenular commissnre; inf, infnndihulmn; M, cavity of mesencephalon; N, notochord; 'n..p, anterior neuropore; p.c, posterior COIIlII1iSSlll‘(‘.; pin, pineal organi; Rh, cavity of rhombencephulon ; t.o, tecmm opticmn; v, velum tmnsvversum. ; v.IV, fourth \'t‘llt.I‘i(:l¢’*.

seems probable that Very pronounced flexure of‘ the brain, such as is seen in the developing Elasmobranch, is to be regarded as a secondary result of the heavily yolked condition of the egg. As a result of the concentration of yolk towards the ventral side in such heavily yolked Vertebrates the processes of growth are retarded upon that side. But it is clear that retardation of growth in length on the ventral side as compared with the dorsal would bring about a flexure towards the ventral side. That the cerebral flexure is due rather to such a general cause than to any inherent peculiarity in the brain itself is supported by the fact that the notochord is also strongly flexed (see Fig. 54, 0).

As a consequence of these considerations, we are inclined to take the view that the phenomenon of cerebral flexure is of much less fundamental morphological significance than is commonly supposed.

Comparing the later stages figured for Acantluias with those of Lepidoszrcn, it will be seen that the brain shows the same elements although these differ in their relative size and other features in the two cases. Thus the cerebellum of the sharks——correlated with the active and complex movements of these fishes——becon1es much more developed. It grows greatly in anteroposterior extent and that causes it to bulge outwards as shown in Fig. 54, E (oer).

The pineal body is slender and elongated in form: the velum forms a conspicuous infolding of the thalamencephalic roof continuous across the mesial plane.

The wall of the anterior portion of the primitive fore-brain undergoes a fairly uniform increase in thickness throughout with the exception of a transverse band just in front of the velum which becomes thin and membranous. This portion of the brain increases somewhat in transverse diameter so that it is broad in shape as seen from above, but there is no definite bulging in its side wall to form a distinct hemisphere. The material that would ordinarily go to form the hemispheres remains here in the thickness of the wall.

The olfactory bulb arises as a slight projection from the side wall of the fore-brain, but as development proceeds and the olfactory organ becomes removed from the brain by the interposition of ni_esenchyme the olfactory bulb remains in contact with the olfactory "organ, its attachment to the brain becoming drawn out into a more or less elongated stalk the olfactory peduncle or olfactory tract.

The salient features in the establishment of the topography of the Vertebrate brain have been illustrated in outline in the sketch which has just been given. It would be beyond the scope of this work to make any attempt to fill in the picture in detail but it is necessary to recall a few points which are of interest to morphologists apart from specialists in neurology.

It should in the first place be borne clearly in mind that the brain——like indeed the whole of the nervous system (see below, p. 118) is to be looked upon as a fundamentally continuous structure. The parts which compose the adult brain—-—medulla, cerebellum, mesencephalon and so on—are not to be regarded as constituent units which go to build up the complete brain, but rather as specialized portions of a once homogeneous whole. The process of specialization has probably been linked up more particularly with the processes of localization or centralization of particular functions in particular brain regions. When this has come about, increase in the number of ganglion-cells devoted to the particular function will cause an increase in bulk of that portion of the brain in which they are situated and it will assume definite characteristics of its own.

The first step in the development of such a brain region consists in the mere thickening of the brain wall but with still greater increase in the number of cellular elements involved mere increase in thickness becomes insufficient for their accommodation and an increase in area comes about in addition. This necessarily causes a bulging of the particular part of the brain wall and some of -the most characteristic differences between the brains of different types of Vertebrate depend upon whether the bulging takes place outwards or inwards.

Thus in the majority of Vertebrates the cerebellum bulges outwards as has been indicated in the case of Acantl:/ias. In Teleostean fishes on the other hand this is the case with only the hinder part of the cerebellum: its anterior portion in these fishes bulges downwards and forwards underneath the roof of the mesencephalon forming the well-known valvula cerebelli. In the more primitive ganoid fishes on the other hand such as Pol;/pterus (Graham Kerr, 1907) the hind portion of the cerebellum also grows inwards, so as to form a structure projecting back into the fourth ventricle in just the same fashion as the valvula cerebelli projects forwards.

A somewhat similar difference appears to be present in the case of the hemispheres. These originate in most subdivisions of the Vertebrata as paired bulgings of the wall of the primitive fore-brain, and the present writer agrees with Studniéka (1896) in feeling compelled to accept on this ground the view taught by many of the older morphologists such as Von Baer, Reichert and Goethe that the hemispheres are to be looked on as fundamentally paired structures, rather than the view, more fashionable of recent years, which regards the portion of the primitive brain lying in front of the velum and optic recess as forming together with the hemisphere region an unpaired complex (Telencephalon-—His). The more complete knowledge that we now possess regarding the development of the brain in the more primitive Vertebrates with holoblastic eggs, seems to the writer to make it clear that the reasons which have led to a departure from the older view can no longer be regarded as adequate. We take it then that the hemispheres are fundamentally paired projections of the side wall of the primitive fore-brain. Physiologically they are probably to be regarded as portions of the brain wall which have become specially enlarged in relation with the sense of smell, just as are the optic outgrowths in relation with the sense of sight.

N ow whereas in the majority of Vertebrates the hemispheres bulge outwards, in the more primitive Teleostomes (e.g. Polypterus, 96 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

Graham Kerr, 1907) they bulge inwards. In the typical Teleosts what apparently corresponds to the hemisphere forms simply a solid mass projecting into the cavity of the fore-brain, the structure which is usually and probably erroneously spoken of as the corpzts st'riat'u'm in these fishes.

A part of the brain which is of very special morphological interest is the thalamencephalon——which persists with singularly little change throughout the series of Vertebrates. Even in .A')IljJ]b’ll0.’l7’Ll»S sagittal sections through the front end of the neural tube present appearances which vividly suggest the thalamencephalon of the more typical Vertebrates (Kuplier) and raise the question whether—as is probable enough on other gro1mds——-the head region in Amplmlowws is degenerate and once possessed a brain.

Amongst the structures connected with the thalamencephalon special interest a.ttaches to the pineal body.‘ So far this has been alluded to merely as a comparatively simple diverticulum of the thalamencephalic roof. in the majority of Vertebrates it remains comparatively uncomplicated and its main function appears to be that of forming a peculiar internal secretion.

In two sets of Vertebrates-——-the Lampreys on the one hand, and Sphenoclon and many Lizards on the other—-there becomes developed in relation to it an organ possessing a close resemblance to an eye, of the “camera” type, possessing a retina and in some cases a lens. The organ appears to be functional as the tissues overlying it a1'e commonly free from pigment and its retinal cells on exposure to light show a change of position in their pigment granules similar. to what is commonly found in visual organs. Though functional it does not follow that the organ serves for the detection of what We call light: it may be that its sensitiveness is rather towards radiant energy of other Wave-lengths than that included within the range of the visible spectrum.

There is a general tendency amongst those who have carried out researches upon the pineal eye to regard the eyelike condition as a relatively archaic condition ot‘ the pineal organ~—-a tendency which is encouraged by the evidence of palaeontology that certain ancient Tetrapods of the palaeozoic and mesozoic periods possessed a highly developed pineal organ——-the skulls of these animals possessing a relatively huge parietal foramen, corresponding with the foramen in the root‘ of the skull of modern lizards in which the pineal eye lies

embedded. The evidenceof embryology indicates that the most archaic con dition of the pineal organ was a simple diverticulum of the brain roof projecting towards the skin on the dorsal surface of the head. There is no clue whatever as to the original meaning of this diverticulum. But we do know from the study of invertebrates that where tissue rich in nerve-elements comes to be exposed to light there is frequently shown a well-marked tendency to the evolution of eye-like structure. In Molluscs for example we find eyes developing on the edge of the mantle (Pccten), round the tips of the siphons (Uardium sp.), on the dorsal surface of the body (independently in 0'/titan and Oncvlrlvluum)-—and similar instances might be quoted from other groups.

  • 1 An admirable account of the structure and development of this region of the brain by Studnieka. will be found in Oppel (1905).

Bearing such facts in mind one is compelled to acknowledge the possibility, if not probability, of such a projecting piece of nervous tissue as the pineal diverticulum, lying close under the surface of the head on its dorsal side, in the position where light stimulus would be most pronounced, developing secondamly in some cases into an organ of the nature of an eye.

Discovered by Leydig (187 2), its structure investigated by Spencer (1886) and other workers, the development of the pineal eye has formed the subject of a number of excellent researches. It will be convenient to take as an example that of the common lizards of the genus Lacerta ( N ovikofi”, 1910).

The first indication of the organ appears in embryos of about 3 mm. in length in the form of a thickening of the thalameneephalic roof, in the region of the mesial plane, and divided by a transverse furrow ‘on its outer surface into a smaller anterior and a larger posterior portion. This thickened part of the brain roof comes to bulge outwards and forms a prominent projection (Fig. 55, A) the groove dividing it externally into anterior and posterior portions being still visible though less distinct.

The projecting pocket now grows forwards parallel to, and in close contact with, the brain roof (Fig. 55, B), its forwardly projecting portion becoming constricted off from the rest. The constriction in question deepens and the anterior portion (parapvlneal body) becomes nipped off to form a completely closed vesicle (Fig. 55, C)—-the rudiment of the eye. As the external ectoderm recedes from the brain roof, with the increase in the amount of mcsenchyme between the two, the parapineal vesicle remains close to the ectoderm and consequently retreats from the brain surface (Fig. 55, D).

The eye is now seen to be connected with the brain wall by a distinct optic nerve which, in full accordance with the view taken in this book with regard to nerve-trunks in general, is merely a primary bridge which already existed (N ovikoff) at a time when the eye vesicle and the brain roof were still in immediate contact and which simply became extended in length as the gap between eye and brain became greater and greater (Fig. 56, pm). N erve-fibres develop in this optic nerve which pass at their cerebral end into the habenular commissure. Transverse sections through a 9-mm. embryo show that the fibres on entering the commissure bend away to the right, passing eventually to the right habenular ganglion. In this connexion with the right habenular ganglion Lacerta. resembles the other lizard Iguana, tuberculata (Klinckowstrom, 1894) but curiously differs from Sphenodon where according to Dendy (1899) the connexion is with the left habenular ganglion.

Meanwhile the wall of the vesicle lying next the outer skin

FIG. 55.———-Sa.gittal sections through the pineal organ of embryos of Lacerm. . (After Novikotf, 1910.)

A, L. m'm‘pam, 3 mm.; B, ditto, 4 mm.; C, L. -muralis, 6 mm.; D, L. mdpura, 9 mm. ect, external ectodorm; 1, lens; p.e, pineal eye; pan, pineal nerve; p.s, pineal stalk; pin, pineal mwgrowth; that, roof of thalamencephalon.

assumes a lenticular form, its cells becoming much elongated though remaining in a single layer. This lenticular thickening occasionally becomes lost during deve1op1nent—-a fact which may be taken as forming a piece of evidence in favour of the view that the eye, at the present time, is in a retrogressive phase of evolution.

Those parts of the vesicle wall which do not take part in the formation of the lens undergo histogenetic changes into retinal tissue. The cells undergo differentiation in two directions. The one set become pigment eells—-tall columnar cells which traverse the whole thickness of the retina and have their nuclei towards the basal or outer end and which develop dark melanin granules in their proto- " Ian. plasrn. /7,52.

Interspersed with these are the " percipient cells, shorter in form, their basal ends not reaching the outer ‘surface, and carryi.ng at their inner ends Cllllllll-l7llx’(_‘, structures which project into the cavity of the vesicle. The idea that these projections correspond physiologically to rods appears to be negatived by the fact that they occur also on the inner ends of the cells forniingithe lens.

At their basal ends these cells are continued into nerve-fibres, which form a distinct layer internal to the nuclei of the pigment cells and are Fwut ?5:-piarieala 7W1:‘(Llv?78»f25ffIri}Ih1-,1Sagiteventually continuous phys1o.log1— c‘;p1::’1"m‘1‘f“ (‘Egg N‘(;‘:,‘i’k0‘t’,') “ ‘“”"“ cally with the fibres of the pineal _ _

seemed a»m0nsSt»&n€1 in the ..::;:;.i.:;?.:%::':‘:'.f:i l10lgl'll)()1lI'll()0d Of, blllfl lllj)I'0l1S liliyel‘ 70.3, pineal stalk ; pm‘, paraphysis. ganglion-cells are present: they are about the first definite elements to become recognizable during the histogenesis of the retina and appear first close to the point of attachment of the optic nerve.

The cavity of the pineal eye is kept distended by a clear substance,

the vitreous body, and this is colonized by a certain number of cells (see Fig. 55, C) which are most probably to be regarded as i1n1nigrant mesenchyine cells. M In Sphenodon, the sole survivor of the only other existing group of Reptiles in which a pineal eye is present, the development of the organ according to Dendy (1899), who has worked it out in detail, agrees with that of Lacerta in its main features.

‘In the Lampreys, also, somewhat eye-like developments occur in the pineal region. In theadult two vesicles--—a dorsal (“pineal”) and a ventral (“parapineal”)-—~are found overlying the roof of the thalamencephalon. In each of these the lower wall shows histological characteristics of retinal tissue and each is in continuity with the brain-—in the case of the parapineal organ directly and in the case of the pineal by an elongated stalk containing nerve—fibres. '

The parapineal organ lies in some cases (G’eotm3a-——-Dendy, 1907) slightly to the lef't of the pineal and its nerve-fibres have been traced into the left habenular ganglion while those of the pineal organ have been traced to the right habenular ganglion. In neither case does the outer wall of the vesicle show any signs of thickening to form a lens——so that neither organ can form an iinage-—but the overlying tissue is comparatively transparent so that diffuse light stimulus ca11 reach it. '

According to Studnicka the two organs develop as evaginations of the brain roof one (parapineal) in front of the other. The parapineal evagination soon loses its lumen and becomes solid and it is noteworthy that at first it is continuous on each side with the habenular ganglion of that side. Later on it becomes by differential growth shifted far forwards, away from the region of the habennlar ganglia, and it loses its connexion with the right ganglion while it remains connected by nerve-fibres with the left.

The two questions of special interest which present themselves in regard to the pineal and parapineal organs are (1) were they originally ocular in structure and function and (2) were they paired or unpaired?

(1) It is obvious that the presence of an eye-like pineal or parapineal organ in certain Reptiles and in Lampreys, and of a large parietal foramen in the skull of various extinct Vertebrates suggests the possibility of these organs having had the form of visual sense organs in the ancestral Vertebrate. Against this however must be set the fact that in all other Vertebrates than those mentioned, including such relatively archaic forms as Elasmobranchs, Crossopterygians, Dipnoans and Urodeles, there is no trace whatever of eye structure.

It seems highly improbable that a well-developed visual organ once present on the dorsal side of the head in the ancestors of Vertebrates should have disappeared without leaving a trace in all the varied groups, with their very different modes of life, outside the limits of the Lampreys and Reptiles. To the present writer it does not appear that the evidence, so far_ as it exists at present, is anything like convincing that the pineal eye is an ancestral feature _of Vertebrates in general rather than a mere secondary development.

(2) Various recent investigators of the pineal organs are inclined to look upon them as being originally paired structures, the pineal organ in the strict sense being the right-hand member of the pair and the parapineal organ the left. This is perhaps most clearly suggested by the Lampreys in which the .parapineal organ is connected by nerve-fibres with the left habenular ganglion and the II N EUROMERY 101

pineal organ with the right (though also with the posterior commissure). Again in various Vertebrates (Teleostomatous fishes-— Hill, 1894: Amphibians, Birds-—Ca1neron, 1903, 1904) the parapineal organ is in early stages slightly to the left of the pineal organ.

On the whole it does not appear to the present writer that the evidence is suflicient to make the view probable. In the Lampreys the connexion of the parapineal body with only the left habenular ganglion appears, as indicated above, to be secondary : it is originally connected with both right and left. Again, to turn to the lieptilia, the eye is in Spheaodon connected with the left habenular ganglion and in the Lacertilia with the right, although it seems perfectly clear from the figures given by Dendy and N ovikolf respectively that the eye is morphologically the same organ in the two types mentioned. Were it not so we should be driven to the position that of a pair of pineal eyes originally present one has disappeared entirely in Sphenodon and the other has disappeared equally completely in the lizards. The improbability from a physiological point of view of this having happened need not be accentuated.

Here again, then, there seems to be up to the present no sufficient reason for departing ‘from the view that pineal and parapineal organs were primitively median in position, one in front of the other. As to their original significance we have no obvious clue: the absence of convincing evidence that they were originally eyes does not of course preclude the possibility of their having been originally some kind of sense organ.

N EUROMERY.-——It has been noticed in various Vertebrates, particularly Elasmobranchs, Amphibians and Birds, that the neural rudiment while still in the form of an open plate is sometimes divided up by numerous and regular transverse markings. Whether this appearance of segmentation is caused simply by the active growth in length of the medullary plate or, whether on the other hand it has some deeper significance has not been conclusively determined. The name neuromere has been given to the apparent segments. That these are really primitive morphological segments as is believed by many and as is implied in the termination “ -mere ” seems improbable.

The existence of a clearly marked segmentation of the nervous system where it oecurs—in the phyla Annelida and Arthropoda——is brought about by the concentration of ganglion-cells in serially repeated masses, in correlation with the presence of serially repeated appendages (parapodia in Polychaeta), and there is no suflicient evidence to show that such were ever present in the ancestral Vertebrate. The fact that the longitudinal muscles are divided into myotomes would not be sufficient by itself to account for the external form of the central nervous system being segmented, for in that case the segmentation would be still clearly marked in the many fishes where the myotomes remain practically unm odified.

During later stages, after the neural tube has become closed in, “ neuromeres ” are particularly conspicuous in the brain region.

They are sometimes very distinct in the hind-brain of fowl embryos of about the fourth day (see Fig. 236 in Chap. X.). It is however an outstanding characteristic of the head region as compared with the trunk that the segmentation of its mesoderm has become blurred and in great part obliterated. It is under those circumstances improbable that a primitive segmentation of the central nervous system, which is in its nature linked up to a segmentation of mesodermal structures, should have remained particularly distinct in a region where the mesodermal segmentation itself has become particularly obscure.

The appearances mentioned seem to be adequately explained by the active growth of the developing brain within its confined space, combined with the presence round it of mesodermal tissue with vestigial segmentation. It will be noticed in the figure referred to above that the dividing lines between the “ neuromcres ” are spaced out at exactly the levels where We should expect to see boundaries of mesoderm segments were the existing series prolonged forwards. Segments are no longer visible in this region but there is, as will appear later, convincing evidence that the series of segments did formerly extend through this region now occupied by continuous mesenchyme. _

It may well be that the individuality of the segments, no longer visible as such, isstill expressed by a difference in consistency of the mesenchyme, suflicient to mould by its varying resistance the actively growing hind-brain as it presses against it.

Development of the Peripheral Nerves

The development of the peripheral nerves of Vertebrates has been the subject of a large amount of , investigation, partly on account of its intrinsic interest and partly on account of its bearing upon physiology and pathology. In spite of the labours of numerous investigators the problen1—-for We may take it that the mode of development is fzmda.mentally the same throughout——has not yet by any means been satisfactorily decided.

While bearing in mind the undesirability of making use of modern facts merely to support, or to undermine, old hypotheses, it will be convenient to approach the question by stating shortly the three prevalent views as to the main features of the development of peripheral nerve-trunks neglecting differences in detail. For shortness these three views may be termed after their most prominent supporters (1) the His view, (2) the Balfour view and (3) the Hensen view.

THE HIS VIEW (Outgrowth theory).-—This hypothesis may be said to have been founded by Kupffer in the embryological portion of Bidder and Kupffer’s work (1857) on the spinal cord. As however Kupffer later on gave up the view, in favour of that of Balfour, the hypothesis now under consideration is commonly associated with the name of His, who played the main part in’ building up the theory and who fully deserves to be regarded as its principal founder.

It is to be noted in passing that Kupfl’er’s original observations were made upon Mammals and those of His (1868) upon the Fowl. In other words, in both cases the embryos were such, in regard both to the minute size of their cell elements and to their high position in the Vertebrate scale, as to be unsuited to provide a reliable basis for the generalization that has been built upon them.

'l‘he His View as expounded by one of its most distinguished supporters S. Ramon y Cajal (1909) may be summarized as follows, the case of the motor nerves being taken for the sake of simplicity. Each motor nerve-fibre arises as an outgrowth from a neuroblast, or young ganglion-cell, lying within the spinal cord. The fibre sprouts out from the neuroblast, makes its way to the surface of the spinal cord, perforates that surface, and proceeds to grow freely through the mesenchyme. The free end of the fibre forms a “cone of growth,” commonly shaped somewhat like a grain of barley and with a pointed end. This “cone of growth” shows an active amoeboid movement, by which it insinuates itself through the interstices of the mesenchyme. Sometimes it may be seen to flatten or mould itself against obstacles in its path.

In the Fowl these processes take place during the third and fourth days. Eventually (about the fifth day, in the Fowl, in most cases) the growing nerve-fibres reach their destination and become joined up to the muscle cells which form their definitive end-organs.

The essential feature of the His view is that the nerve-fibre (which already shows the characteristic specific reactions of a nervefibre, e.g. on impregnation with silver salts, and is therefore not merely a strand of undfiferentiated protoplasm) sprouts out from the central nervous system and grows through the intervening mesenchyme with a free end until it becomes joined up secondarily with the end-organ.

The His view at the present day rests upon a large body of observed facts. In studying the embryology of almost any Vertebrate it is easy to find in sections what appear to be freely ending nerve-fibres sprouting out from the spinal cord. Some of the most beautiful preparations of this kind have been made by Ramon y Cajal and others by the use of silver impregnation methods.

Perhaps the most striking evidence, which has recently been adduced in favour of the His view, has been obtained by experimental methods, especially by Harrison (1908, 1910). In one set of experiments which have been regarded as particularly convincing Harrison removed small pieces of embryonic spinal cord from Frog embryos at a period just before that at which the motor nerves became visible, and was able, by using ordinary antiseptic precautions, to keep them in a living condition for relatively prolonged periods mounted in a drop of sterile lymph under a coverslip upon a slide. The lymph soon -clotted and held the piece of spinal cord in position. Harrison now observed in many cases little projections making their appearance from the pieces of spinal cord which he identified as rudimentary inotor nerves.

Any possible doubt as to the correctness of this identification was removed by Burrows (1911) repeating the work on the chick and obtaining the specific staining reaction of neuro-fibrils’ in the structures in question. These nerve-rudiments when l<(i-.pt alive under the conditions mentioned were observed to increase rapidly in length, the rate of growth being in one case as high as 56;; per hour. The end of the rudiment (Fig. 57) was somewhat enlarged and projected into fine protoplasmic tags which showed active amoehoid movement. It is this amoeboid protoplasm at the free end of the fibre which, in Harrison’s belief, is. the active agent in the extension of the nerve-fibre.

As to the method by which it is, in the actual body, guided along the proper path to its destination, Harrison does not commit himself, but he appears to have a leaning towards the view held by Ramon y

chemiotaxy. _

In the words of their author (1908) these “experiments place the outgrowth theory of His upon the firmest possible basis,—-that of direct observation. The attractive idea of Hensen must be abandoned as untenable.”

It should be added that the His theory fits in very well with current views in physiology and pathology—in particular with the fashionable neurone doctrine, according to which the cellular units which compose the nervous system are not in organic continuity with one another. Obviously this hypothesis and the Flu.‘ 57.--~ Viewpof outgrowing nerve- Outgrovvth hypotllesis, according to which the is for a me five minutes later than A. (After Separated by 3: gap fI'0n1 1tS end‘

Harrison. 1908-) organ, lend one another mutual support}

’ It must be borne in mind, however, that the histological basis of the neurone theory is not universally admitted to be beyond suspicion. Its main foundation consists.ol' observations by the Golgi and similar methods ol' metallic impregnation. In reparations made in this way single cellular units are frequently picked out witiout the reaction taking place in neighbouring units arranged in series with them. A ganglion-cell A with its axon aml ts-rminal branches stands out deep black in the preparation, while the ganglion—eull B, I'1u.\;t to it in the series, shows no reaction. Snell an observation obviously suggests discontinuity.

The P()S'.sll)l(_E fallacy in these observations lies in the"fact that the stain used is not a true stain in the ordinary sense of the word but merely a precipitation of metal upon

Cajal that it is mainly a matter of

The His view is concerned primarily with the actual functional nerve-fibres. As regards the primitive sheath (Gray Sheath of Schwann), in which these fibres are enclosed, the His view regards it as being formed by mesenchyme cells which apply themselves to, and spread out over, the surface of the originally naked nerve-fibre.

(2) THE BALFOUR VIEW (Cell -chai n theory). ———While Schwann(1839) long ago described the multicellular structure of nerve—trunks in the foetuses of mammals, it was F. M. Balfour (1876) who really founded the view that the nerve -trunk arises in development from a chain of cells. F10. 58. —Section through the dorsal part of the trunk Balfour fuund in E1aSInO_ of a Torpedo embryo. (From Balfour's Embryology.)

branch elnbl-yos the (1.:-, dorsal root; g, spinal ganglion; why, myotome; N, notonerve_trunk was repre_ n, nerve--trunk; m:, cavity of spinal cord; v.r, ventral sented by a chain of cells in early stages (Fig. 58, 22.7")’, and similar observations have been made by subsequent observers. According to this View the whole nervetrunk is niulticellular in origin, the cells not only forming the sheath of the nerve-trunk but also giving rise to the nerve-fibrils which come into existence traversing the cellular strand from end to end.

011 the question of the origin of the cells which constitute the nerve-rudiment opinions vary. Most supporters of this view have regarded them as having emigrated from the spinal cord (e.g. Balfour, van Wijhe, Dohrn): while others (Kolliker) have looked on them as mesenchymatous in nature. Sedgwick took this latter view and as he regarded the mesenchyme as a continuous syncytium, the bridges connecting the cells being primitive——-persisting from the the surface of the cell and its processes. We know from the recognized unreliability of the method that the occurrence, or not, of this precipitation is liable to be decided by extremely delicate chemical differences. We know further that the axis cylinder, however it arose in development, is morphologically and physiologically a prolongation of the cell-body (ganglion-cell), and therefore that its metabolism is under the control of the nucleus of that cell-body. The individuality of the cell and its prolongation, due to the metabolic control by its own special nucleus, is probably qulte enough, in itself, to account for a chemical character of its surface sufliciently different from that of its neighbours to influence the precipitation without there being, as the neurone theory assumes, any absolute discontinuity.

thalamencephalon. In each of these the lower wall shows histological characteristics of retinal tissue and each is in continuity with the brain-——-in the case of the parapineal organ directly and in the case of the pineal by an elongated stalk containing nerve-fibres.

The parapineal organ lies in some cases (GeomIa.——Dendy, 1907) slightly to the left of the pineal and its nerve-fibres have been traced _into the left habenular ganglion while those of the pineal organ have been traced to the right habenular ganglion. In neither case does the outer wall of the vesicle show any signs of thickening to form a lens———-so that neither organ can form an image»-but the overlying tissue is comparatively transparent so that diffuse light stimulus can reach it. '

According to Studniéka the two organs develop as evaginations of the brain roof one (parapineal) in front of the other. The parapineal evagination soon loses its lumen and becomes solid and it is noteworthy that at first it is continuous on each side with the habenular ganglion of that side. Later on it becomes by differential growth shifted far forwards, away from the region of the habenular ganglia, and it loses its connexion with the right ganglion while it remains connected by nerve-fibres with the left. ’

The two questions of special interest which present themselves in regard to the pineal and parapineal organs are (1) were they originally ocular in structure and function and (2) were they paired or unpaired?

(1) It is obvious that the presence of an eye-like pineal or parapineal organ in certain Reptiles and in Lampreys, and of a large parietal forainen in the skull of various extinct Vertebrates suggests the possibility of these organs having had the form of visual sense organs in the ancestral Vertebrate. Against this however must be set the fact that in all other Vertebrates than those mentioned, including such relatively archaic forms as Elasiuobranchs, Crossopterygians, Dipnoans and Urodeles, there is no trace whatever of eye structure.

It seems highly improbable that a well-developed visual organ once present on the dorsal side of the head in the ancestors of Vertebrates should have disappeared without leaving a trace in all the varied groups, with their very different modes of life, outside the limits of the Lampreys and Reptiles. To the present writer it does not appear that the evidence, so far as it exists at present, is anything like convincing that the pineal eye is an ancestral feature of Vertebrates in general rather than a mere secondary development.

(2) Various recent investigators of the pineal organs are inclined to look upon them as being originally paired structures, the pineal organ in the strict sense being the right-hand member of the pair and the parapiueal organ the left. This is perhaps most .clearly suggested by the Lainpreys in which the parapineal organ is connected by nerve-fibres with the left habenular ganglion and the 11' NERVE DEVEI.OPMEN'J.‘ 107

be, on the one hand, comparatively archaic-——it should belong to one of the relatively more primitive groups of Vertebrates—-and, on the other ha11d, its histological texture should be as coarse as possible, its cell elements being of large size.

Amongst Vertebrates investigated up to the present time in regard to nerve—development Lepzlclusiren (Graham Kerr, 1904) is unrivalled in its combination of these qualifications and a. summary will now be given of the main features which‘; have been made out from the study of the development of the motor nerves in this animal. It will be convenient to commence with the fully formed nerve-trunk and then work. backwards towards the earlier and more obscure stages.

Fig. 61 represents a portion of nerve-trunk from a fully developed larva of stage 34. The nerve-trunk consists of a cylindrical bundle of nerve-fibrils, dotted over the surface of which are the numerous large nuclei of the protoplasmic sheath. The sheath itself is so thin as to be practically invisible even under a high-power immersion objective except in the angle close to a nucleus where it is distinctly visible.

Fig. 60, D is taken from a larva. ten days after hatching. At this stage the nerve-trunk, when examined superficially, has the appearance of a thick strand of protoplasm containing numerous nuclei or a chain of cells. Careful examination of well-fixed and wellstained specimens shows however that this conspicuous mass of protoplasm is really only the sheath, the true nerve-trunk (n) being visible traversing it from end to end. Scattered about in the thick sheath of this stage there are still to be seen granules of yolk (black in the figure) which have not yet been used up.

Fig. 60, C is taken from a larva at the time of hatching. At this stage the nerve-trunk is a well-developed bundle of nerve-fibrils, just as in the later stages, but throughout the greater part of its length it is devoid of a sheath of protoplasm. In the section figured the sheath is visible as a mass of nucleated and heavily yolked protoplasm enclosing a portion of the nerve-trunk towards its outer end. This mass of protoplasm is obviously just a condensed part of the general mesenchyme which is scattered about in the form of irregular heavily yolked masses throughout the spaces between the main organ systems.

The mass in question is identical with the rest of this mesenchyme in its various features and every here and there it is continued into it without a break. The section figured shows the whole length of the motor nerve-trunk from the ventral root to the myoblasts or muscle cells which form the myotome. Towards its outer end the trunk_ is seen to break up into numerous diverging strands which are directly continuous with the protoplasm of the myoblasts (see below, p. 204). _

Fig. 60, B is taken from an embryo about three days before hatching. At this stage the myotome l1as barely commenced to 108 EMBRYOLOGY OF THE LOWER VERTEBRATES

FIG. 60.-—~Port.ions of t.x-ansvex-.~u:

A, stage 2-1 : J), .-at.:ng<- 2'.) 4.-. m, nn_mtu_m1t-: -u. m~r\'o'-trunk ', .<.«-, .<}»in:|l curd ; sh, slmzttlx.


FIG. 60/\.———Porti0ns of tr:m.wc-r the develolnment. of flu» spinal m.-rvv.~: (ventr:ml root.

recede from the spinal cord, but yet each motor nerve is already present as a distinctly fibrillated trunk bridging across the narrow gap between spinal cord and myotome. A few mesenchyme cells have wandered into the gap but they have not yet begun to concentrate round the nerve-trunk.

‘ Fig. 60, A is taken from an embryo of stage 24 at a time when myotome and spinal cord are still in close contact with one another. In specimens which were extended in one plane under normal salt solution while still alive and subjected to the action of the fixing agent in that position, it is found that the myotome is frequently pulled slightly away from the spinal cord (as in the specimen figured) and in such cases it is found that the nervetrunk already exists in the form of a bridge of soft granulai‘ protoplasm (n) without any trace of fibrillation, connecting spinal cord and 111y0t0me. That these bridges are really the nerve-trunks is indicated by their occurrence one to each myotome, apart from the fact that a continuous series of stages have been observed between them and the fully developed nerve-trunks. '

In summing up we may FIG. 6l.~——l’art of transverse section of Le.1)i<l0.s"i')'(’n, take the various stages in

(stage 34), showing a portion of nerve-trunk. their proper chronological in”, myotome; N, notoehord; n, nerve-trunk ; n.S, nucleus Sequcnde.

of nerve sheath; S1, pi-irnary sheath of notochord; XI, . e . lateral branch of vagus. The nerVC'trunk 18

already present as a protoplasmic bridge at a period so early in development that spinal cord and myotome are still in contact with one another.

(2) As the embryo grows and the myotome recedes from the spinal cord this protoplasmic bridge increases in length and becomes fibrillated.

(3) As the nerve-trunk lengthens amoeboid masses of mesenchymatous protoplasm collect round it and gradually spread out over its length to form the protoplasmic sheath.

In stages later than those figured the sheath protoplasm insinuates itself in amongst the nerve-fibrils of the trunk, dividing them up into bundles or nerve-fibres. As the myotome resolves itself into the various muscles of the adult each piece retains its primitive e nerve-strand, drawing it with it, as i.t becomes pushed about by the processes of differential growth, as its own special nerve.

It should be mentioned that the most important point in the II NERVE DEVELOPMENT 111

above deseription——the existence of the motor trunk in the form of a bridge of protoplasm between myotome and spinal cord at a time when they are still in close proximity—-has been confirmed for another very primitive group of Gnathostomes, the Elasmobranchs (Paton, 1907), as is shown in Fig. 62.

It will now be convenient to review the facts just described for Lepidosiren in relation to the general theory of nerve-development.

(1) It is clear in the first place that the His view is put out of court, seeing that before there is any development of nerve-fibrils the motor nerve-trunk already exists in the form of a bridge of protoplasm connecting spinal cord and myotome.

(2) It is equally cl.ear that the Balfour View is inapplicable: the nerve-rudiment cannot in early stages by any possibility be regarded as a chain of cells, seeing that its total length is greatly less than the diameter of a single cell-nucleus.

(3) While the nerve-rudiment forms a primary connexion between spinal cord and myotome, in the sense that it is in existence before these organs begin to recede from one another, there is no evidence by which the connexion can be traced back to intereellular bridges or plasmodesms (StraS_ FIG. 64'2'.r——~l‘:n'l .(')l'llI.‘.'l.l-l.’\'\."(£.l‘.1\‘:"lit-?(.ffll(ill tllrplugh burger, 1901) of early. e-.<7- SesInen- is "u'.‘$"';..Z;'t'.'»"’l‘;L£le.t£{l‘K12"'§II.’nTn§§iI tation, stages in the development (After Stewart Paton, 1907.)

Of egg, as would be case 'In'_1/,my0t'..nl'm'; n,mirvv-11-unk;s.r, .~:pin:ll ('n1'(l. according to Hensen’s theory.

(4) The primitive protoplasmic bridge gradually becomes fibrillated but there is no means of determining with any degree of certainty how these fibrils are developed.

It is s11ggeste(l 1 that the development of the actual nerve-fibril is simply the gradual coming into View of a pathway produced by the repeated passage of nerve i.mpulses over a given route.

It is clear from the study of the simpler organisms that one of

‘the most ancient properties of living protoplasm is that of the trans mission of impulses through its substance. Although nothing is really known as to the precise nature of living impulses it is reasonable to suppose that they involve changes in the distribution of energy analogous to those involved in the passage of an electric disturbance. If this be the case their passage between two points will be determined by the relative potential, and the route along which the impulse passes will be that of least resistance. If the conductivity of the living substance were uniform the path would be a straight line joining the two points: if the conductivity were not uniform on the other hand the path would be diverted along routes of high conductivity where the total resistance would be at its minimum. Looking at matters from such a point of view we should regard a motor ganglion-cell at the moment of functioning as a centre of high potential and its muscle ending as of low potential, while a sensory cell at the moment of its functioning would be a centre of high potential and the central termination of its nerve-fibre as at relatively low potential.

  • 1 Graham Kerr, 190-=1. ‘It has been pointed out th.-xi similar .-'1lg'gcsti0I1S in regard to the nervous system. in general were made long ago by .l'.l.a_-rburt; Spencer.

In early stages of evolution, whether phylogenetic or ontogenetic, we may take it that vital impulses fiitted hither. and thither in an indefinite manner within the living substance and that one of the features of progressive evolution has been the gradual more and more precise definition of the pathways of particular types of impulse, as well as of the transmitting and receiving centres between which they pass.

We may then regard the appearance of neuro-fibrils within the protoplasmic rudiment of the nerve-trunk as the coming into view of tracks, along which, owing to their high conductivity, nerve impulses are repeatedly passing} It may be that as each successive passer-by causes a jungle pathway to become more clearly defined so each passing impulse makes the way easier for its successors, and makes it less likely for them to stray into the surrounding substance.

The special physiological meaning of the differentiation of the fibril would simply be the increase of its conductivity —~—-possibly towards one specific type of impulse——but correlated with this are optical and staining peculiarities which, though unessential in themselves, make the fibril recognizable to the eye as a definite structure.”

The nerve-trunk in Lepidosiren is seen to be at first naked and later on to acquire a sheath formed by concentration of mesenchyme round it. This sheath is at first richly laden with nutriment in the form of yolk granules but these are gradually used up as the nervetrunk goes on with its development, the products of digestion of the yolk being doubtless passed on to the developing nerve-trunk. This as well as the marked increase in the number of nuclei in the sheath seem to indicate that the main r6le of the sheath is to look after the nutritional needs of the nerve-trunk.3

We have dealt, so far, only with the motor nerve-trunks. In regard to the general method of development of sensory nerves, there exists the same divergence of opinion as in the case of the motor nerves, and in endeavouring to decide which View has upon its side the balance of probability, it is well to bear in mind similar conditions to those alluded to on p. 106. Bearing these in mind, it is of interest to notice that in Lepidosriren (Elliot Smith, 1908) the process of development of the olfactory nerve takes place along exactly similar lines to that of the motor trunks. And it is significant that, in the opinion of those well qualified to judge (Retzius, Golgi, Rainon y Uajal, van Gehuchten, Kolliker, Elliot Smith), this nerve has advanced less from the primitive condition than has any other nerve, and in its general arrangements has undergone extraordinarily little complication during ontogeny.

1 Paton (1907) shows that impulses are actually transmitted across the protoplasmic bridge at a very early stage in the case of Elasmo ranchs.

2 The hypothesis here outlined in connexion with the embryonic development of nerve fits in well also with certain of the phenomena observed in the regeneration of nerves which have been severed and joined together a ain [see Trans. Roy. Soc. Edliné, ]xli, p. 126, also Mott, Halliburton and Edmunds in Proc. Roy. Soc., B, vo . 8 .

3 The medullary sheath of nerve-fibres is non-cellular and appears to be produced by the secretory activity of the protoplasm of the axon.

Already at a time when the olfactory organ has not yet commenced to recede from the wall of the hemisphere the olfactory nerve exists as a stout pri5toplasmic bridge (Fig. 63, I) which gradually increases in length as the olfactory organ recedes from the hemisphere. This observation seems to indicate clearly that the mode of development of the sensory nerve-trunk is fundamentally the same as that of the motor: that it develops out of a pre- existing protoplasmic bridge be tween Celltre and end-0rgan. FIG. 63.-—--All t3d.I'l_V Sl.fl,g(§ Of the Oll'fl.(3t.Ol‘y nerve of Lcpz.zlnsi7~en. (From Elliot Smith,


REMARKS UPON THE GENERAL ¢-.11, lateral wall of hemispliere; ulf, olfactory

PROBLEM OF NERVE DEVELOPMENT organ; 1, olfactory neI'\'e. The nuclei semi in the

region where the olfactory nerve enters the lu-.miIt; will be adlnitted by most sphere belong to the olfactory bulb.

Zoologists that we are justified in believing that the process of nerve—deve1opment is probably fundamentally the same throughout the Animal Kingdom. It will also be clear, even from the short and imperfect statement which has been given here, that the detailed study of the phenomena of nerve—development has led, in the minds of different‘ observers, to widely divergent conclusions as to the exact nature of the process. The subject is one to the discussion of which we may devote with advantage some further space. It is in itself of great embryological and physiological interest. It presents many problems still unsolved. And it may be taken as a type of biological controversy with which it will be to the student’s advantage to become acquainted.

In approaching the question from the present-day standpoint it appears impossible to get round the fact that in two of the most archaic groups of Vertebrates (Elasmobranchii and Dipnoi) the motor nerve-trunk is already present as a protoplasmic bridge at a time when myotome and spinal cord -have 11ot yet commenced to recede from one another. It does not seem possible to explain the appearances recorded in these cases by any conceivable errors of observation. But if such bridges exist in these relatively archaic groups, the balance of probability is entirely on the side of their representing the primitive mode of development of nerve—trunks in general, and of a fundamentally similar mode of development occurring in other Vertebrates though possibly in a modified and less distinct form.

On the other hand appearances of the kind which led to the original formulation of the His view, and which are still adduced in its support, and which are easily observed in series of sections through almost any type of Vertebrate embryo—-nerve-trunks passing out from the spinal cord and ending freely amongst the mesenchyme—-are peculiarly apt to be misleading.

Such a misleading appearance is produiisd sometimes by comparatively simple causes-—-by breakage of the nerve-trunk or by the nerve-trunk passing away out of the plane of a section and‘ being unrecognizable when out transversely in a neighbouring section. In other cases the appearance of a freely ending nerve-trunk is due to the portion of nerve-trunk which has received its protoplasmic sheath being distinctly visible in a stained section, while the delicate peripheral portion which is still naked is practically unrecognizable. On account of such liability to misinterpretation a very large proportion of the observational evidence which supports the His view is open to suspicion.

A physiological difficulty which has been raised against accepting the His view is that involved in the idea that the free end of the growing fibre tracks down and finds its appropriate end-organ. It is pointed out that it never makes a mistake—-never becomes joined up to a wrong end cell. And yet; if it be the case that nerve-fibres do grow outwards with free ends in the way involved in the His theory, certain experimental results show that such fibres do possess a very decided power of making mistakes. This is brought out clearly by the beautiful experiments of Braus (1905).

In the experiments in question Braus made use of the method, invented by Born and developed by Harrison, Spemann and others, in which portions of one amphibian embryo are grafted upon the body of another, when the grafted portion (“parasite ”-—Braus) proceeds to develop as part of the individual (“ autosite ”--Braus) upon which it has been grafted. ,

In the experiments which are most important in their hearing on the point now under discussion the early rudiment of the pectoral limb was grafted upon a host in the region of the head. In this position the rudiment went on developing into a perfectly normal limb containing a normal arrangement of the limb nerves. Now the iniplanted limb in such. a case (Fi g. 64) is Situated in a region innervated by the facial nerve and the study of sections showed that the nerves in the i1upl:uited limb were continuous centrally with branches of the facial nerve.

"If we attempt to interpret this vxperilnent on the oiitgimvtli view we find ourselves compelled to admit that the facial fibres concerned made the serious mistake of growing into a limb rudiment; and then continued on their mistaken course until finally they established the muscular connexions normal for the nerves of such a limb. Braus repeated this type of experiment in a number of cases and there appears to be no question as to the accuracy of his observations. If accurate, however, they provide a formidable, if not unsurmountable, difficulty for the outgrowth view—a difliculty which is by n0‘means got rid of by the suggestion (Harrison, 1908) that after arriving in the limb the nerves are “ merely guided in their growth by the structures present in the transplanted part.”

A similar difficulty is seen in postembryonic nerve-development in the fact well known to surgeons that functional continuity can be established between the cut cent'ral stump of one nerve (ag. spinal accessory) and the severed peripheral portion Fm, 64,——Young Toad (Bomof another bimttor) on which an additional limb has been graltecl And so again in the development of in the head region (After

anastornoses between peripheral nerves such B,-ms, 1905,)

‘as the well-known “ dialyneury ” of Gaster0 pod molluscs, or the short circuiting of the left pulmonary nerve over the dorsal side of the oesophagus which has come about in the evolution of the Crossopterygians and Lung-fishes.

All such cases present great if not insuperable difliculties to the His view.

Again much of the evidence which is brought to the support of the His view is seen when looked at critically to be less convincing than it appears to be at first sight. Thus for example with the experiments of Harrison already described, which are rega.rded by their author as settling the whole question. Their true value will become more apparent if we bring Harrison's results into correlation With tlw results (h-.seribcd above for L6P’l:(l08"l:7‘81&.

As has already l)(*.("]l shown, in this animal the motor nerve-trunk is represented at an early stage by a bridge of soft fragile protoplasm. These bridges require a very favourable object and very careful technique for their detection, and it is clear that one could not expect to see them in comparatively coarse preparations Inade by excising a piece of living unfixed spinal cord. Tlioro is tlu-rol'o1'e no guarantee that sueli pi-otoplasmic nerve-rudiments were not already present in the pieces of spinal cord investigated by Harrison.

Let it be assumed that such an experiment is repeated upon Lepddosiren with a small piece of spinal cord rudiment with the protoplasmic bridge attached to it (Fig. 65, A). The piece of spinal cord is well supplied with food material in the form of yolk and, if kept under suitable conditions, it would go on developing. So also might the protoplasmic bridge, for every one agrees that the metabolic control of the motor nerve is exercised by the central ganglion-cell nuclei within the spinal cord. If this happened and the process Went on quite normally we should get in succession stages such as those shown in Band C of Fig. 65.

N ow these would be interpreted by Harrison presumably as demonstrating the outgrowth view, whereas all that they really show is that, given suitable conditions, the motor nerve increases in 1ength———a fact which of course is obvious. What is needed as a demonstration of the His view is not merely to show that a nerve-trunk increases in length but to show (1) that it ‘normally has a free end and (2) that it grows within the body at a greater rate than the tissues in which it is embedded, so that there is brought about a difl'er— cntial movement in which the FIG. 65. —-—-Drawings taken from the szune free (ind Pushes its a'y.thrOug.h

preparations as those illustrated in Fig. 60, the tlssues S“1T0undmg 113- ,Th]sS showing a piece of spinal cord with the has 1101'; been Sl10W1l by Harri~

developing motor nerve but ignoring the SOn’S experinwnts mm. could it niyotonie which is iii the actual embryo ‘

continuous with the outer end of the nerve. possibly be Shown by this type of experiment. In Lepi(‘]0s’i'/"6-72. the study of sections shows as has already been pointed out that, although the motor nerve-trunk grows actively in length with the increase in bulk of the body, at no period from the earliest stage figured has it a free end;‘it is throughout connected with its endorgan.‘ r In a word, it appears to the present writer that what are commonly regarded as the most convincing pieces of evidence in favour of the His View are by no means convincing. Views resembling that of His in that they also involve an out 1 The actively moving pseudopodium-like tags which Harrison observed at the end of his outgrowing nerve-trunk are believed y the present writer to he mesonchymatous in their nature--- ssibly shreds of sheath protoplasm. It is a general feature of embryonic mesenc iyme that its protoplasm shows active amoeboid move ment. ' II NERVE DEVELOPMENT 1 17

growth of the motor trunk from the spinal cord, but differing from it in the essential feature that the outgrowth is simply protoplasmic and not fibrillar, have been enunciated by some modern workers such as Dohrn and Held. Dohrn (1888) describes the motor nerve-rudiment as arising by a “plasmatic outflow from the neural tube” but Paton later on finds that at the stage referred to by Dohrn the nerve-rudiment is already continuous at its outer end with the protoplasm of the myotome.

Held (1909) also regards the motor trunk as arising by outgrowth from the spinal cord at a time when the myotome is still comparatively close to it. It has to be borne in mind in interpreting such sections as Held figures that there is more liability to error in demonstrating the absence of continuity than in demonstrating its presence, owing to the extremely fragile character of the nervetrunks during early stages in development and their consequent liability to rupture during the ordinary processes of preparation which precede. section—cutting.

It is sometimes said that the diiliculty attaching to the His view involved in the idea of the nerve-fibre tracking down its own particular end-organ disappears if the view is taken that the outgrowth takes place at a stage so early as that indicated by Dohrn and Held. But as a matter of fact this involves, as indicated, a distinct departure from the View enunciated by His according to which not merely undifferentiated protoplasm but definite fibrillated trunks grow out from the spinal cord. Further ii‘, as Held believes, the individual fibrils grow out in the substance of the protoplasmic outgrowth each one has still to seek out the particular portion of the myotome which will eventually be converted into its own proper muscle-cell—-a view which, looking to the comparatively undifferentiated condition of the myotome cells at these early stages, is even more difficult to comprehend physiologically than the» outgrowth towards a specialized muscle.

The embryological evidence upon which the His view rests is seen, when submitted to critical examination, to be unconvincing. The same is the case with the observational evidence upon which the Balfour View rests. The nuclei and cell-bodies which commonly give a multicellular appearance to the nerve—rudiment are quite reasonably interpretable as sheath-cells, 1J.e. mesenchyme elements which have collected round and it may be migrated into the, at first nonccllular, nerve-trunk.

In Lepidosireaz, with its coarse and heavily yolk-laden mesenchyme, it is comparatively easy to distinguish such elements from the actual nerve-trunk embedded in them, but in most Vertebrates this criterion is not available and there is no certain means of distinguishing in ordinary microscopic preparations the protoplasm of the nerve-trunk from that of the sheath-cells.

The primitive protoplasmic bridge described in 1902 for L6p'id08’i'r6’Ib as representing the motor trunk at a time when 118 EMBRYOLOG-Y OF THE LOWER VERTEBRATES CH.

myotome and spinal cord have not yet commenced to move apart, confirmed later in the case of the motor trunks of Elasmobranchs by Paton, and in the case of the olfactory nerve of various Vertebrates by Elliot Smith and others, seems to rest upon a secure basis of Observation. It is difficult, therefore, to avoid the expectation that the progress of future research will show such a primitive protoplasmic bridge between centre and end-organ to be the normal forerunner of nerves in general.

But, if this he so, we are faced by the question as to the actual mode of origin of such bridges and here we pass into a region where direct observation is either impossible or unreliable. Those who accept Hensen’:-s views in their entirety would look upon them as representing inter-cellular connexions persisting from the earliest segmentation stages. Reasons have already been given (p. 37) for disbelieving in the persistence of such bridges between the cells of the segmenting egg. The connexion appears certainly to arise at some later period-—hut exactly when seems to be a question incapable of answer by direct observation.

When considering these general problems regarding the nervous system it should be borne in mind that the nervous system has for its main purpose the keeping of the various parts of the body linked together into an organic whole, in spite of their increasing differentiation and specialization. It has for its function the providing of exquisitely specialized pathways by which the living impulses can traverse the whole length of a relatively immense body at least as readily as they originally did the minute blob of ancestral protoplasm.

Bearing in mind this primary consideration will cause one to reflect that the evidence must be overwhelming before one is justified in believing that this organ system, whose most striking functional feature is continuity, has come in the course of evolution to be characterized by the structural discontinuity involved in the neurone theory of adult structure, or in the outgrowth theory of ontogenetie development.

Again it is important to bear in mind the high degree of probability attached to the view, originated long ago by O. and R. Hertwig (1878), that the nervous system of the higher metazoa, including Vertebrates, has been evolved out of a subepithelial nervous network of the kind still seen in some of the more lowly organized groups such as Coelenterata and Echinodermata. We may suppose that such a plexus was present in the far back ancestors of Vertebrates over the basal surface of both ectoderm and endoderm cells (as in modern Actinians, Havet, 1901) and that nervetrunks became evolved as local condensations of such a network, just as we still see in the nerve-strands of a Medusa or a Starfish.

In this connexion, it is of interest to note that according to the protostoma theory of the fundamental structure of the vertebrate body, which will be found stated later, in Chapter IX., the points represented by the two ends of the motor trunk were originally in close proximity, and a condensed strand of the network joining the two points would naturally be left as a bridge when they became separated by the deepening of the cleft between mesoderm and endoderin (cf. Fig. -66).

To sum up, in regard to the mode of development of the nervetrunks, it seems reasonable 2l11_ the present state of our knowledge

(1) to reject definitely that portion of the Henseii view which looks on the protoplasmic bridges as having persisted from the com- mp menceineiit of segmentation,

(2) to regard the His view of free—en(ling fibrillated outgrowth as non-proven and for various reasons improbable,

(3) to believe that the nervetrunk already exists as a protoplasmic bridge between centre and end-organ at a period when these are still in immediate contact, even although this has up to the present been definitely shown by actual observation only in a few peculiarly favourable instances,

(4) to leave the exact period at which the protoplasmic bridges come into existence an absolutely open pad?

Fie. 66.-—-lllustrating the structure of a question as being beyond the limit of reliable observation,

(5) as regards the sheath of Schwaiin, to accept the view that it is derived from nieseiicliynie. It will be noticed that little has been said so far regarding the mode of development of the actual neurofibrillae. Their origin is indeed unverifiable by direct observation, with any certainty, owing to their

liypotlietieal primitive Vertebrate at a time when the protostoma was still open. In the lower figure an enterecoelie pocket, the rllllllllellt of a mesodérui segment, is beeoining demarcated froin the rest of the endoderni by the downward spreadiiig of a split between the points a and I). In the earlier stage shown in the upper figure this split has not yet begun to develop, and the points a and 6 are seen in close proximity to one another on the outer surface of the ciidoderin.

minute size. They appear to spread outwards frcin the centre, and Held interprets this appearance by a kind of His theory on a minute scale, holding that each fibril grows out with a free end through the protoplasmic bridge. On the other hand if it be the case as suggested on p. 112 that the fibrils simply represent the specialized paths of nerve impulses there would be nothing surprising in their becoming visible first in the neighbourhood of the ganglioncell from which the impulses start and from which also is exercised control over the nietabolisin of the nerve-trunk. Were this the case we should get appearances which would closely simulate growth of freely ending fibrils——eentrifugal in the case of motor nerves and centripetal in the case of sensory nerves.case we should get appearances which would closely simulate growth of freely ending fibrils——eentrifugal in the case of motor nerves and centripetal in the case of sensory nerves.

-m.p, niedullnry plate; p.8, pi-otostoma.

This view as to the meaning of the Iibrils bridges over a good many of the difficulties in the way of accepting the outgrowth view, either as regards the individual fibrils or the nerve-trunk as a whole. Thus the secondary establishment of anastomoses between peripheral nerves becomes less surprising if it be the case that undifferentiated protoplasm is liable to develop nerve-fibrils as a reaction to the passage of nerve impulses through it, for wherever there are nerves there’ must be a certain amount of leakage of the particular form of energy which constitutes the nerve impulse.

So also with the joining up of the central and peripheral ends of a severed nerve or of the central stump of one nerve with the peripheral portion of another. In such cases we should assume that indifferent protoplasm accumulating between the cut ends gradually becomes iibrillated in response to the passage of more or less imperfect impulses through it, the newly developed portions of fibril being necessarily, from their mode of formation, continuous with both central and peripheral fibrils, leading respectively to the “high-potential” and the “ low-potential” end of the nervefibre.

_ Again it is known that a mass of embryonic ganglionic tissue implanted into some abnormal portion of another individual may establish nervous connexions with the surrounding tissue. On the outgrowth hypothesis this demonstrates “error” on the part of the outgrowing fibres: on the functional view it simply involves the gradual differentiation of paths along which impulses spread outwards from the high potential ganglion-cells into the low potential surrounding tissue.

On the whole, the present writer believes that this view, that the formation of nerve-fibrils is a response to functional activity, is at the present time the most plausible working hypothesis and also the one which is most likely to lead to fruitful research. Before leaving the subject it may be well to emphasize the fact that the solution of this general problem of nerve-development is to be sought in the study of Vertebrates of large-celled coarse histological texture, combined with a low degree of specialization of general structure. N 0 amount of observations upon small-celled highly specialized Vertebrates will ever lead to a really convincing solution with the methods new at our disposal.

Finally we would once more emphasize the fact that the kernel of the problem seems to centre round the origin of the fibrillae. Do they or do they not develop in a pre-existing bridge of protoplasm? Assuming that they do, the possibility of such bridges dating back to the period of segmentation seems to be definitely excluded. The question at what precise moment they do -become established seems to be of minor importance.

While the present writer is inclined to believe that the junction is already in existence while end-organ is still in close apposition to the central nervous system there is no difiiculty in principle in the way of admitting that the bridge may in certain cases be formed somewhat later, as Dohrn describes, provided always that the gap to be bridged over is small and the bridge itself protoplasmic and not flbrillar. It is probably along such lines that we may look for a reconciliation between the supporters of His (the outgrowth view) and those who believe in the protoplasmic bridge view but it will involve dropping what are essential features in the outgrowth View as enunciated by His himself——(1) that the outgrowth arises at a time when the end-organ has already retreated to a considerable distance from the nerve-centre and (2) that the outgrowth is already fibrillated during the outgrowing process and before it is united to its end—organs.

SPINAL GANGLIA AND DORSAL RooTs.——As has already been indicated, the central nervous system of the Vertebrate consists in its most primitive condition of a specialized area of the ectoderm of the dorsal surface. It is further very characteristic of the Vertebrate that those ganglion-cells which belong especially to the sensory fibres have become concentrated into segmentally arranged clumps towards the margin of the nervous plate and have eventually come to lie outside the limits of the actual plate, or tube into which the plate becomes converted. These little detached pieces of the central nervous system are the ganglia of the dorsal roots or the spinal ganglia.‘

During actual ontogeny the ganglion rudiments in some cases (ag. Birds, Fig. 67, A) become distinctly apparent While the spinal cord is still in the form of an open medullary plate. They appear in the form of a continuous proliferation from the inner surface of the ectoderm in the angle between the medullary plate and the external ectoderm. In such cases the two rudiments become carried in towards one another, as the edges of the medullary plate curve inwards to form the neural tube, and undergo fusion across the mesial plane. There is thus formed a median unpaired plate or tract of cells lying just over the roof of the neural tube. and between it and the external ectoderm. This is known as the neural crest (Marshall).

More usually the ganglionic rudiment makes its first appearance after the closure of the neural tube and in such cases the paired stage of the rudiment is slurred over, the neural crest being formed by proliferation of the roof of the neural tube. This is well seen in the case of Elasmobranchs (Fig. 67, B, 0).

However it originated, the plate-like neural crest splits into two

‘ There is reason to believe that this is an instance of a widespread tendency in evolution for groups‘of ganglion-cells to undergo gradual shifting towards the direction from which their most frequent afferent impulses come. In other words there is a. tendency to shorten the afferent path by shifting the cell-body. This principle of neurobiotaxis has been developed by Ariens-Kap ers in his various papers (e.g. 1913). It is particularly conspicuous in the changes whic 1 have come about in the position of the ganglionic centres of the various cranial nerves within the brain in the difl'erent groups of Vertebrates.

lateral halves and then grows outwards on each side opposite each myotome, each outgrowth representing a single spinal ganglion.

Eventually these l')I'(‘-itli apart "but in some of the more primitive Vertebrates the intervening portions of neural crest persist for a time in the form of a distinct longitudinal coiumissure (Fig. 68) linking up the series of‘ spinal gangliaito one another (Elasniohranchii --—Ball"our: Dipnoi).

The mode of development of the fibres forming the dorsal root, Whether by outgrowth from the ganglion-cells of the spinal ganglion

“or by difl'erentiatio.n of an already existing protoplasmic bridge, comes


Flu. 67.———Illn.~'traling the mode of origrin of the spinal ganglia.

Miiwle.r11ln'-_yo with four lll(':~2(_Nlt'l'lll segrr1¢mt..s' (:cl't¢-r .\'c-inn.-i_\'r. 19043); It and ('3, 'l'ur/mrlu .1 mm. embryo (aftc.-.r Dohrn, 1902); cut, ectoderm; g, rudiment o1'g.‘mi«,;-1i«_»n; s.v', spinal cord. under the general controversy as to nerve-development and need not

be specially discussed. URANIAL NERVEQ. Tilt: (leveluplilellt of tile (.'.1':1.Il1al nerves has

heen investigated by many workers and an i1nnn"-.nse alnonnt of detailed observation has been accumulated. There is however great discrepancy in detail between the results obtained by different W01‘ko1's, and much of the observation seems to be perilously near the limit of p1‘nin1.l)le error. Consequently the material seems hardly ripe for tn-.at1m-ant in a text-book of a general kind and nothing of the sort will he attempted here beyond noting one or two points of particular iniportaneel

1 A modern account of the development of cranial nerves will be found in Neumayr (1906).

In the first place We find in the head region as in the trunk a tendency for the nerve-fibres to come off from the central nervous system in segmentally arranged clumps, and for the motor fibres to be situated more ventrally and the sensory more dorsally. In the head region however the dorsal root becomes reinforced by a large mass of motor iihi-es which have become shifted dorsalwards and incorporated with it.

A neural crest develops resembling that of the trunk and in the Birds it can be seen similarly to have a paired origin, arising before the complete closure of the medullary tube. This neural crest of the brain region forms an anterior prolongation of that in the trunk: it is quite continuous with the latter, it develops outgrowths similarly, and the intervening portions here also persist for a time as a longi tudinal commissure. A number of the most important cranial nerves

FIG. 68.—l-lrr'z.u(/u'u..v, slag:-. ‘.33, 9 mm. long, .~<lmwing ganglia of cranial and spinal nerves. (Alter Scaiulnon, 1911.)

int, intestine; 1, lens; Z13, liver‘; pan, pancreas; sp.g, ganglia of spinal nerves; Th, thyroid; V, ventricle; v.c, visceral cleft; y.st, yolk-stalk; IV, V, etc., ganglia of cranial nerves.

are simply prolongations of the outgrowths in questi0n——V, VII, VIII, IX and X. I

A conspicuous feature in the development of the cranial nerves is that in portions of their length they receive components directly from localized thickenings (placodes) of the ectoderni (Kuplfer, Beard) a possible remi.niscence of the time when nerve-trunks became evolved out of a plexus in direct relation to the external ectoderm.

I. The Olfactory nerve is unrivalled amongst all the sensory nerves of the Vertebrates as a subject for investigation on account of its large size, its short uncomplicated course and its retention‘ of

comparatively primitive conditions even in the adult. Research

should therefore be specially concentrated upon its mode of development.

In the case of Lepidosdren, as already indicated, Elliot Smith has shown that the olfactofy nerve is simply .a. drawn — out primary connexion between brain and olfactory o1‘gan, already present at a period before these organs have begun to move a] part.

In other vertebrates (Elasmobranchs ———1lol1n, 'l‘eleosts, Amphibians l24 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

—-Cameron and Milligan) there is evidence that the same mode of development holds. One of the important points to be settled is whether the nuclei which are seen scattered about in the young nerve-trunk and which give it a syncytial appearance are not really immigrant sheath nuclei. The conditions in Jmyniclosiren where it is easy to distinguish the heavily yolked sheath protoplasm make it appear probable that this will be found to be the case.

II. The optic nerve is not a true peripheral nerve comparable with the other cranial nerves but simply a narrow isthmus or stalk connecting the main brain with its outlying portion which forms the retina. Its development is mentioned in the description of the eye.

III, IV and VI. The oculomotor, pathetic and abducent nerves appear to agree exactly in their n1ain developmentalfeatures with ordinary motor nerves of the trunk (Neal, 1914).

It is not proposed to say anything here regarding the topography of the cranial nerves but some points regarding it will be touched upon later on in connexion with the segmentation of the head.

SYMPATHETIC.-—The sympathetic ganglia, as was first shown by Balfour (1878) for Elasmobranchs, are derived directly from the spinal (or cranial) nerves. In its earliest recognizable stage the ganglion forms a swelling on the course of the nerve just ventral to and continuous with the spinal ganglion. With further development the ganglion bulges more and more pronouncedly towards the mesial plane at about the level of the dorsal aorta. The nerve-trunk in this region now splits longitudinally and the ganglion becomes shifted farther towards the mesial plane, lying immediately over the posterior cardinal vein and remaining connected by a slender bridge ——-the ramus communicans-—-with the spinal nerve from which it has become split oil’.

In Sauropsida the sympathetic ganglia arise in similar fashion. In Amphibia and Sauropsida, where the sympathetic ganglia are in the adult connected by a longitudinal trunk, this latter is said to arise secondarily, the ganglia being at first quite separate. In view, however, of the difficulty of detecting such nerve-trunks in early stages of development it will be well not to dismiss altogether the possibility that the ganglia are after all in continuity from the beginning.

From the basis of the sympathetic system so laid down extensions apparently sprout out into the various tissues which are eventually innervated by this system-—but again there has to be admitted great possibility of error. The problem of the mode of development of these obscure portions of the nervous system will probably only be satisfactorily settled after we know with certainty the processes at work in the development of the main nerve-trunks and ganglia.

THE ORGANS or SPECIAL SENSE.—-We may take it that in the early stages of the evolution of the nervous system, while this system was still a diffuse network, there, were already present

"scattered sensory ce1ls——-cells specialized for the reception of imI1 OLFACTORY ORGAN 125

pressions from without. Local concentrations of such sensory cells and their further specialization for the better perception of some particular type of stimulus has led to the evolution of the various organs of special sense.

The special sense organs of the vertebrate fall into two categories —(I.) the organ of vision, perhaps the Oldest organ of special sense, which is developed within the limits of the central nervous system and (II.) the other organs of special sense which have probably arisen more recently from the sense cells of the skin outside the limits of the central nervous system.

As the organs belonging to the second category have evolved less far from the primitive condition they will be considered first. They appear to have become specialized functionally in two different directions, those in the neighbourhood of the mouth for the appreciation of differences in chemical composition—the organs of taste and smell-—and those on other parts of the body surface for the appreciation of vibrations of the surrounding medium———the lateral line organs and the organ of hearing.

OLFACTORY 0RGAN.—-—Tl1e olfactory organ arises in the form of a localized thickening of the ectoderm on each side towards the anterior end of the head. Later this thickened ectoderm becomes depressed below the general surface so that it assumes a saucer- and later a cup-shape; its external opening eventually becomes comparatively narrow.

In many of the Elasmobranch fishes the olfactory organ retains throughout life the condition of a simple inpushing of the skin opening to the exterior on the ventral side of the snout. In many Vertebrates on the other hand characteristic changes come about in the relations of the external opening. These will best be understood by considering first what happens in the lung-fish Protopterus as shown by Fig. 69. In A and B the olfactory organ is visible as a little rounded dimple on each side. In C the dimple has become a deep groove running obliquely from before backwards and outwards. It is further seen that this groove is becoming involved in the sinking in of the skin to form the buccal cavity. In D and E the groove has become a deep slit narrow in its middle part and dilated at its two ends. Finally, in the stage represented in F, the margins of the narrow part of the slit have undergone complete fusion so that the continuous slit of the preceding stage is now represented merely by its terminal portions which form two widely separated rounded openings——the anterior and posterior nares (oéf 1 and 04/’ 2).

Turning to the other Vertebrates we find various divergences from this simplest mode of origin of the external and internal nares as seen in Protopterus and Oemtodus. In the Actinopterygian fishes the phenomena are quite similar to those described, only here differential growth leads to the gradual shifting of the olfactory organ and its openin s from the ventral side of the snout up to its dorsal side. The resu t is a. topographical reversal of the positions of 126 EMBRYOLOGY or THE LOWER VERTEBRAIITES an.

anterior and posterior naris: the morphologically posterior naris coming to lie in front of that which was originally anterior. '

In the Amphibian and Amniote the upper lip, which completes the huccal cavity in front, is situated between the anterior and posterior narial openings, so that the latter opens into the huccal cavity

Flo. 69.-——Vcntral views of llutltl region of larva of Protoptc-rus at stages 31 (A), 32 (B), 34 ((3), 34 (D), 35 (E), and 36 — (F), to illustrate the development of the olfactory organ.

c.o, celnent organ: e.g, external gill; olf, olfactory organ; olf 1, anterior (“external ") naris; olf2, posterior (“internal “) naris. In C the curved line running across the ventral side of the head is the posterior margin of the mouth: the darkly sluuled grooves passing inwards and forwards from its

outer ends are the olfactory rudiments.

(internal naris), while the former remains outside (external naris). In the developing Amniote embryo (cf. Fowl, Chap. X.) the general arrangements, while essentially the same as those of Protopterus, are somewhat obscured by the modelling of the face region. The ridge which forms the upper lip, or anterior boundary of the buccal cavity, is out across by the olfactory slit, here a wide and deep cleft, into a u L OLFAOTORY ORGAN 127

median portion (median “nasal process) and a lateral portion (maxillary process).

The ridge hounding the olfactory involution on its outer side remains for a time separated by a distinct groove from the maxillary process but as the latter grows forwards it oblitcrates this groove as Well;as the superficial portion of the -cleft which separates it from the median nasal process, the deep portion of the cleft remaining as a definitive canal leading from olfactory organ to huccal cavity.

In Amphibians, as in Lepialosiren among the lung-fishes, the posterior naris is frequently formed as a secondary perforation which

Flo. 70.—~I-lorizontal h'L‘(‘.l-l()llh' through the olfactory organs of I’nlg/p(¢:ru.s* of stages 25 (A), 26 (B), and 27 ((3).

c.o, cement organ; olf, olfactory rueliment: opt, optic stalk; '1‘Im.l_. cavity of tlialaniencephalon.

breaks through from the posterior portion of the olfactory organ into the part of the huecal cavity lined by “ endoderm.” This is a secondary modification of a type which will be discussed in the next chapter in the description of the development of the huccal cavity in these forms. _ The first rudiment of the olfactory organ has been described as a thickening of the ectoderm. A.s in the case of other nervous or glandular developments of the cctoderm the superficial layer (Fig. 70) takes no part in its formation. Commonly it degenerates and disappears over the actual olfactory epithelium. Again, as frequently happens in the development of primitively hollow organs, the rudi ment may be for a time solid, forming a simple solid downgrowth in 128 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

which a cavity makes its appearance secondarily, the actual involution of the surface being delayed or reduced or absent (Fig. 71).

Sometimes, as is well shown in the case of Poly/pteras (Fig. 70, A), the olfactory thickenings are at first continuous across the mesial pla11e and this fact, taken in consideration with the fact that in the Lampreys the olfactory organ of the adult is unpaired, obviously suggests the possibility that the olfactory organ of Vertebrates in general was originally unpaired (Kupffer). Though this must be admitted as a possibility the evidence does not appear to be suflicient to give the idea probability .in view of the fundamentally paired character of the portions of the brain associated with the olfactory organ, even in the case of the cyclostomes where the organ as a whole has an unpaired appearance.

After the olfactory involution has become definitely established it undergoes various complications of form, differing in detail in the various groups but consisting for the most part of

lining epithelium so as to bring about an increase in its area. In the Elasmobranch these cutgrowths take the form of parallel grooves which gradually become converted into deep slits separated by thin partitions —-—- the Flo.’7l.—~Longitudinal vertical se<-,- .SChnelderi.anfO1dS' In Crossolmgrygians “on through ,..,,,w,te,.,,3 (smges instead of numerous folds with free 28-29), showing the olfactory rudi- edges complete septa are formed which "“’“‘ “S “ ‘“i"k.°"i"g °Lf “W .‘l°"1’ radiate out from an axis formed by layer of the eetoderm in which a . _ _ . . i cavity has developed secondarily. l-’he_ 01fa’Cl-‘Olly negrve and dlvlde lfhe .cavity as seen in transverse section into distinct chambers, the lining of which in turn forms deep folds. In the higher forms the outgrowths of the olfactory lining are fewer in number and the projections left between them form the turbinals which have characteristic arrangeinents i.n the different groups. Amongst the Reptiles a conspicuous development of the olfactory apparatus is the Organ of Jacobson. This arises as a pocket-like outgrowth of the lining epithelium, on its mesial side and near its ventral edge, which becomes gradually constricted off from the olfactory organ and opens into the buccal cavity in the region of the posterior nares. In Chelonians, Crocodiles and Birds this organ has disappeared except for a possible vestige in the form of a transient bulging of the olfactory lining. . A diverticulum which may correspond to J acobson’s organ makes its appearance in Lung-fishes and Urodeles but in this case it becomes gradually displaced outwards until it lies external to the olfactory


bulgings outwards on the part of the’ ll OTOCYST 129

A curious, possibly adaptive, arrangement has been noticed in late developmental stages of certain Sauropsida, where for a time the external nares are plugged by a proliferation of ectoderm (Aplm-3/ac——— ’l‘. J. Parker, Sp/wnmlon-—Dendy). Such temporary obliteration of a channel at a period of development where it is unnecessary or harmful is a phenomenon which occurs fairly frequently: examples of it will be met with later in connexion with the alimentary canal and the excretory organs.

(_)'1‘0cYsT.—'l‘he Vertebrate possesses a pair of otocysts situated one on each side of the hind—brain. Each arises in the typical fashion familiar in the invertebrates, by a sensory portion of ectoderm becoming depressed below the surface of the skin and eventually isolated as a closed vesicle. As in the invertebrates certain of the lining cells of the otocyst secrete otolithic masses of Calcium carbonate.

'l‘he otocyst of the Vertebrate however shows two developments which do not occur amongst the invertebrates. Firstly, in connexion with the primitive function of the organ, that of balancing, the wall of the growing otocyst becomes moulded into the three semicircular canals which are arranged in planes at right angles to one another. These canals have for their function the analysis of any rotatory movement into its components in these three planes. And secondly a special region of the otocyst wall becomes specialized in connexion with a new sense—~that of hearing——and grows out into a curved horn-like pocket, the lagena, which may become greatly enlarged and spirally coiled, in Vertebrates in which the sense of hearing is very acute, forming the organ known as the cochlea.

The development of the otocyst may be described as it occurs in the Fowl (liothig and Brugsch, 1902). The otocyst begins to make its appearance during the second day of incubation as a thickened area of ectoderm on each side of the hind—brain. This thickened area becomes depressed below the general surface, forming a saucershaped depression which gradually deepens till it forms a deep pit. The lips of this pit, especially dorsally, grow inwards so as to constrict the opening which is finally completely obliterated, the original open depression being thus (:0I1Ve1'te(l into a closed, somewhat pear—shaped, sac the otocyst. The wall of the otocyst remains for a time continuous through a solid bridge with the outer ectoderm (Fig. 7 2, A) but as a rule this bridge persists merely for a very short time and only a small cellular tag attached to the otocyst remains to mark its position.

As development goes on the otocyst increases in size by growth of its wall and this growth is especially marked ventrally and laterally with the result that the point which was originally connected to the ectoderm becomes displaced so as to be situated on the mesial side of the otocyst. This portion of the otocyst wall now comes to project upwards as a distinct pocket-like outgrowth the recess (Fig. 72, B, 9'). External to this a wider bulging of the wall fore VOL. 11 K 130 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

shadows the anterior vertical semicircular canal (am) and a little later a similar bulging more ventral in position-——the horizontal canal (lac). The lagena also is foreshadowed by a slight downward bulging of the floor of the otocyst.

With further development the posterior vertical canal rudiment appears also as a bulging of the otocyst wall continuous with that which will form the anterior canal (Fig. 72, C-F, The three canal rudiments come to project more and more prominently, the recess assumes the tubular. shape of the endolymphatic duct and the lower portion of the otocyst (saccule) With its projectillg lagenar pocket and endolymphatic duct becomes more sharply marked off from the rest of the otocyst (utricle). The pouch-like rudiments of the semicircular canals, as they come to project more freely from the utricle, assume a flattened form and finally the central FIG. 72.-—ll1ustrating the development of the otoeyst in the portion of the wall on

Fowl. (A-G after Rothig and Brugsch, 1902; H after each Side bulges in__

R t ' 5‘! I I e Zn") wards and fuses with

A and B, early stages; C, towards end of seventh day; 1), to- 0 wards end of eighth day; E, five days; I*‘, towards end of ninth n Other"

day; G, towards end of twelfth day; H, adult. A is a view from In llhit‘-l Way the in front, B from behind, while C-H represent the left otocy-it as gmltral pm;-fion of the seen from the left side. a. v, anterior vertical canal; h.c, horizontal - ,

canal: lag, lagena; pm, posterior vertical canal; 9', recess; s.e, Oavlty of each, Pouch endolyniphatic duct. be 0 em 6 S O b 11 terated

while the persisting peripheral part takes the form of a curved tuhe——the definitive canal. At first the space subtended by the canal is traversed by a continuous septum formed out of the fused walls but this soon disappears leaving the canal as a freely projecting arch which opens into the utricle at each end. The ampulla. appears at an early stage as a

dilatation of the canal rudiment at one end. As will already have been gathered, the three canal rudiments do II OTOCYST 131

not appear synchronously——the anterior vertical appearing first, then tl1e horizontal and finally the posterior vertical. The same order is followed in subsequent development the anterior vertical canal keeping ahead of the other two—probably a foreshadowing of the greater importance of this canal, parallel to the sagittal plane, in the function

of flight. It should be noticed that the posterior vertical canal assumes its

Fm. 73. ——De.velopn-lent of the otocyst in Lung-fishes as H(7!t‘l| in transverse sections. (From drawings by M. C. Cairney.)

A, Lepidosirerl, stage 21; H, I’-rotupterus, stage 23: (.7, l.:'pz'¢.los'z're-n, stage ‘._’.\‘. N, nut.ochm-cl; at, otocyst: rh, rhomliencephalon. In Fig. 0 the rudime-.ntol'1.he emlolympliatie duct is visible as an outgrowth from the otocyst wall dorsally and mesially.

position at right anglesto the planes of the other two secondarily. At first its rudiment is continuous with and almost in the same plane as the anterior canal but as it assumes the tubular form it swings outwards and forwards slipping, as it does so, over the horizontal canal in the way indicated in Fig. 72, F, Gr, H.

The otocyst of Vertebrates in ;__ge.ne1‘al develops along similar lines to those described for the Fowl while presenting modifications in detail. The sensory epithelium is a development of the deep layer of the ectoderm and in cases where the ectoderm is distinctly two 132 EMBRYOLOGY OF THE LOWER VERTEBRATES on.

layered during the early stages of otocyst development the superficial layer is seen to pass over the rudiment unaltered (Fig. 73, A). In Lung-fishes the cavity of the otocyst appears secondarily in the midst of an apparently solid downgrowth of the deep layer of the ectoderm (Fig. 73, B) but the examination of earlier stages (Fig. 73, A) shows that here also there is an actual involution of the deep layer although there is at first no patent cavity.

In the Elasinobranchs the otocyst retains throughout life its connexion with the exterior, the connexion hecoming drawn out into a slender tube. In Birds the recess, and therefore the endolymphatic duct, represents the remains of this original connexion, but curiously enough in certain other Vertebrates 6._(]. Lung-fishes (Fig. 73, C) the last connexion of otocyst with external ectoderm lies lateral of and somewhat anterior to the endolymphatie duct which latter here develops as an independent outgrowth of the otocyst wall. This is to he looked on as a secondary modification of the more primitive arrangement seen in Elasmohranchs. The structure named endolymphatic duet in Tel:-osts also arises as a secondary outgrowth of the otocyst wall.

The endolyinphatic duct or recess commonly persists in the adult as a conspicuous blindly ending diverticulum of the otocyst wall. In Lung-fishes and Amphibians its wall proliferates actively giving rise to projections which in the Lung-fishes and some Urodeles, e.g. the Axolotl, meet to form an irregular sac over the roof of the fourth ventricle. In the Anura the irregular thin-walled sac formed in this way spreads forwards and also laterally until it hecomes continuous ventrally so as completely to surround the 11ind—brain. An unpaired prolongation of this sac extends tailwards immediately dorsal to the spinal cord within the vertebral canal. Paired outgrowths of this extend outwards along with each spinal nerve and expand at their ends round the spinal ganglia to form the calcareous bodies so conspicuous in the adult frog. The whole system of outgrowths is conspicuous in the adult from the white otolithic particles in its interior. The vertebral portions become eventually broken up into a network of irregular tubes which is interpenetrated hy a network of capillaries (Coggi, 1889).

Somewhat similar outgrowths of the endolymphatic duct make their appearance in Sauropsida although in this case they do not undergo the wide extension that they do in the Anura. In the Geckos however they do hecome extended so as to form a large superficially placed irregularly lobed sac which covers over a great part of the neck region close under the skin (Wiedersheim).

LATERAL LINE ORcANs.——']‘hese sense-buds (neuromasts), which are found arranged in rows on the head and body of fishes and aquatic amphibians, take their origin in linear thickenings of the deep layer of the ectoderm which spread along the surface of the head and body and eventually become segmented up into separate pieces. In correlation with the function of these organs, which II N ERV 0 US SYSTEM 1233

apparently is to detect slow vibrations in tl1e water and is therefore closely allied to hearing, it is of interest to notice that the ectoderlnal rudiment from which tl1ey arise appears to be in some cases continuous at first with that which gives rise to the otocyst.

The. sense organs are in correlation with their origin at first placed superficially but as de.velopme,nt goes on they in most cases become depressed beneath the surface either in isolated pits or in continuous grooves. The latter may in turn remain ope.u or may become covered in to form tubes except where at intervals openings remain leading to the exterior. This is the condition which is reached in the adults of the majority of fishes.

'l‘he lateral line. sense organs being correlated with an aquatic habit commonly degenerate on the assumption of a terrestrial existence. Various Anura however which remain purely aquatic after metamorphosis retain their full equipment of lateral line organs. 3

ORGAN O14‘ l’INKUs.~—ln Le])'£(l0s’i7'('n. and 1"I'0to/)l6'r'us a peculiar organ of special sense. lies deeply embedded in the tissue on each side of the. head in close contact with the wall of the auditory capsule. This organ, discovered in I’7'olop/crus by Pinkus, has been shown by Agar (1906) to be developed from the eetodermal ingrowth which forms the outer end of the spiracular rudiment.

l_§_¥_E‘—-As the eye develops in the same general manner, differing only in detail, in the dilferent subdivisions of the Vertebrata it will be convenient to describe first its development in the Fowl——the Vertebrate of which it is easiest to obtain material for practical study.

The first obvious rudiment of the eye consists of a projection of the side wall of the thalamencephalon which juts out at right angles to the axis of the body and gives a characteristic ha1nmcrshape to the fore-brain region (see Fig. 231, Chap. X.). A transverse section across the head near its front end in a chick about the middle of the second day of incubation shows (Fig. 234, D) the thalamencephalon extending out on each side as the optic outgrowth.

As development goes on and mesenchyme accumulates between the brain-wall and the ectoderm the proximal part of each optic outgrowth becomes constricted, from above downwards, to form a relatively narrow optic stalk (Fig. '74, A, B, D, 0.3). The optic outgrowth is closely apposed against the inner surface of the external ectoderm and a slight thickening of the latter soon becomes apparent just where it is in contact with the surface of the optic outgrowth in (Fig. 74, B, Z). This thickening is the first rudiment of the lens. The lens-rudiment gradually becomes sunk below the general surface to form a saucer- and later a cup-shaped depression. As the rudiment becomes involuted in this way, the outer wall of the optic outgrowth also becomes 134 EMBRYOLOGY OF THE LOWER VERTEBRATES C11.

invaginated to fcmn u. cup—1ike struct;ure—the optic cup (Fig. '74,

Flu. 7v1.———]')«_:v.-I..1.nn-nt. of the eye as seen in h'aI1s\'el'.~u_- .s'«-ctions of Fowl e1nln'_vn:~'.

A, latter half ()f.\'P,('nnal .1.-ny nt‘in(:nb:1ti«-n; H, mm] of so-ennui «lay; C, 21_;(1a,ys; I), 3 «l:1_\-s: E, Intimhalf offiftth day. wt, 0_\;h'.'I'I1:11 c.-ct=0«lem'1 : I, la-nn; ~.r_, rmlixm-Ht of rye; n.s, optiv stalk; ;:.1, pi;_;'nn-n1 layer of retina. ; 7', l‘(‘.till:l ; Hm], wall of Llmlamumuo-plmlol1.

B_ and C). The cup-like lens-rudin1ent- b'ec.0mc-s g1‘a(‘l11all_y con11 EYE 135

stricted off and finally completely separated from the outer ectoderm (Fig. 74, U and 1)). '

In the meantime a marked difference becomes apparent between the two layers forming the wall of the optic cup. The layer next the cavity of the cup becomes greatly thickened its cells becoming tall and columnar: it forms the rudiment of the visual layer or retina in the strict sense. The outer layer of the cup-wall on the other hand dcgenerates, it becomes thinner and later it deposits melanin pigment in its cells. lt forms the pigment-layer of the retina.

The invagination of one wall of the optic outgrowth within the other is not confined to that portion of the outgrowth in proximity to the external ectoderm as might be supposed from the description so far. The invagination involves also the ventral wall of the rudiment towards its outer end and for some distance along the optic stalk. The result is that the wall of the optic cup is interrupted by a gap ventrally the ghoroid fissure 1—-and that the optic stalk for seine distance from the optic cup has_a deep groove along its ventral side.

The cavity of the optic cup, as is the case with cavities generally in the embryonic body, becomes filled with clear fluid secreted into it by the surrounding cells. This fluid becomes jellylike later on and forms the basis of the vitreous body.

As development goes on the eye increases greatly in size and assumes a spherical shape, the lens blocking up its opening towards the skin and the choroid fissure becoming obliterated by its lips coming together. The site of the fissure remains apparent for some time owing to the formation of pigment in the pigment-layer being delayed in its immediate neighbourhood.

As the eye increases in size the Retina for a time grows more actively than the rest so as to be thrown into wrinkles (Fig. '74, E). The lens which was a hollow vesicle becomes solid its cavity being filled up by a great thickening of its deep wall, the cells of which grow out into a tall columnar form (Fig. 74, D and E).

The essential parts of the eye as an optical instrument have now been laid down-—the lens for the production of an image, the retinal wall of the optic cup for the reception of that image and the conversion of its light waves into nerve impulses, and the optic stalk which will become the optic nerve for the transmission of these impulses to the brain. To these essential parts there are added various accessory structures developed from mesenchymatous cells which accumulate round the parts of the eye already formed. In particular there is formed a protective capsule of tough connective tissue -——-the sclerotic with its transparent portion the cornea, covered externally by the ectoderm forming the corneal

1 The term “ choroid” fissure is in reality misleading, having been adopted when the fissure was interpreted as a cleft in the choroid, in the days betore the existence of the pigment-layer of the retina was recognized. 140 EMBRYOLOGY OF THE LOWER VERTEBRATES (311.

along the deep surface of l)esce1net’s niembraiie and there settle down to form a single layer of flattened cells. ()n the deep side of this corneal endothelium a split gradually develops in the jelly-like inatrixr this contains a watery secretion (aqueous humor) and becomes the anterior chamber of the eye.. The portion of matrix lying superficial to l)eseeniet’s inenibrane becomes colonized by cells from all round its margin. lt l'oifi'ns the main portion of the cornea, while a thin layer lying next the ectoderm remains uncolonized and gives rise to Bowma.n’s membrane. VITREO U S .l‘i()L)Y.~'~,lllH‘. cavity of the optic cup is l'i'o1n the beginning filled with clear fluid which l<eeps it distended and there is no anparent reason to assume that tliis arises otherwise than by the same method as holds with the eyes of many iiivertelirates as a secretion of the surroiiiidiiig retinal cells. The fluid gradually acquires the jelly—like consistency charactei'isti(-, oi" the .i'ully—fo.r1ne(l vitreous body.

Anioebocytes wander at a coniparatively early perioifl into the Vitreous rudiment —— i.n the Fowl embryo about tlie third day-Mark Hill (talk)and at a later period a continuous mass of inesencliyine tissue projects into it through the choroid fissure. This mass of meseiichynie develops :1. Flu. 78.~—Semi<lizigraniniatie figure of the IlPl3WO1‘l{ Of l")l(f)()d-V8SS(‘.lS COI1l3l1l1l('_)11S

l’iS‘.’°ted eye Of.“ V°””l""“"‘ ""‘b"Y". with those of the surrouiidiiig tissue. (ltima. 8 min.) to show the course of . A . . . , 5 g the optic iierve-fibres (after Asslieton, In thii llmrii l)r1m1l’1Ve \ ”rl’el)ra‘teS 1892). this niesenchyinatous mass reaches c.f,Wall of cl10I‘0i(lllssuI'e; g/,gaiiglion-cell; T10 g1‘Ud:l3 (lE‘:V(‘/lUp1l’l811l} but lll t»l1C

3 i'”"__“"i""““'~ S“I’I’.°““"3~ °““3 73 l*’"_**? “-15 Teleostei and the Sauropsida, the nerve-libres: 12.1, pigment layer of retina; n _ -_ - - _ A p(]‘r($iI-’i‘_“'-lflcéfillg ’ most highly specialized groups amongst the non—1namnialian Vertebrates, it does so and persists throughout life, as the falciform process with its 111118018-lll)1",SfOl‘ the purpose of accommodation in the one case (Teleostei), and the highly vascular, and probably mainly lllltritive, pecten in the other (_Sauropsida).

OPTIC N ERVE.—-—AS already indicated the optic nerve is not strictly speaking a peripheral nerve at all. It is a slender drawn-out portion of the brain analogous with the olfactory tract of a teleostean fish, connecting the main portion of the brain with the small highly specialized portioii which has become converted into the optic cup. Its function being a conducting one the main mass of this stalk-like portion of the brain is composed of white substance or nerve-fibres.

These fibres instead of passing outwards over the rim of the cup 11 RETI N A ' 137

RE'1‘INA.——The fully-developed retina—which it will be reinenibered is Inorphologically a specialized portion of the brain-wall -—-is an organ of extreme complexity. Its structure even in the adult is by no means completely worked out, and our knowledge of the details of its histogenesis is most imperfect. The most conspicuous feature is the great increase in thickness, the retinal cells becoming slender and columnar in form. Later on the nuclei are seen to become arranged i_n layers, this being an expression of the fact that the cells are also becoming specialized into layers of different structure and function. The details of development of these are almost completely unknown and there is here an interesting field for investigation.

The layer of visual or percipient cells lies on the proximal side of the retina, and their rods and cones—the special parts of the visual cells which are believed to have the function of converting light

, Fm. 76.— Illustrating the development of the rods in Lep2'o'om,'rc7-1-. The upper side of the. figures represent the side turned away from the lens.

A, B, C, D from stage 35 ; E, fully «Ieveiupecl visual cell at stage 38, tlxed during exposure to light: E*, similar element killed in the «l:u'l\'. 11.2‘, annul:u' vacuole; f._q, fatty glolmle.~< stuinetl black by osmic acid; ‘m.-.l, external limiting membrane; n, nucleus of visual cell; 7-, rod.

waves into nerve i1npulses——are at the ends of the cells which point away from the lens. To reach these rods and cones the light rays have therefore to traverse the whole thickness of the retina. This remarkable arrangement of the retina, precisely the opposite of what we should expect, is one of the characteristic features of Vertebrates. Its morphological significance is however at once made clear by a consideration of the main facts of development of the eye as already outlined. These, in fact, show that what becomes the proximal surface of the retina, 73.9. the surface which faces away from the lens, was originally part of the inner surface of the brain rudiment and therefore of the outer surface of the ectoderm before it became involuted to form the brain.

The visual cells develop therefore on what was originally a part of the outer surface of the. body and their rods point in a direction which was originally o1.i_twards. The mode in which the rods develop is illustrated by Fig. 7 6 which is taken from Lepidoszwnrz, (Grahain 138 EMBRYOLOGY OF THE LOWER VEIWEBRATES CH.

Kerr, 1902). Similar observations have been subsequently made in the case of Amphibians.

'J‘be first obvious step in the specialization of the. visual cell is the. appearance of a fatty globule in its protoplasm. The end of the cell turned away from the lens now grows out into a projection and pushes back the fine cuticular limiting membrane (external limiting membrane) which has developed over this surface of the retina, into a little pocket. 'l‘he oil globule which gradually increases in size passes into this pocket (Fig. 76, A, f.g) and lies in it cnsheathed in protoplasm. 'l‘hc protoplasm now becomes heaped up into a little conical protuberance (Fig. 76, B, 7') which is the rudiment of the rod. At iirst the limiting membrane is distinct over the surface of the red but gradually, as the latter assumes a cylindrical shape, its protoplasm takes on a clear structureless appearance throug_»,hout: it apparently becomes in fact converted into cuticular material. This cylinder of euticular Inaterial increases in size, assumes a characteristic appearance with alternating discs of dimmer and more transparent material as seen in the fixed specimen and the rod is complete (Fig. 76, E and Ei‘).

The rods complete their development sooner or later according as they are nearer or farther away from the optical axis ol the eye and their time of development shows great variation in dill'erent individuals. The cones in those Vertebrates in which cones are present are merely specialized rods.

LENs.—-—The lens shows in its early stages, in various groups of Vertebrates, departures lrom the normal condition as described for the Bird, of exactly similar kinds to those seen in the development of the Otocyst. In particular, the lens tends to develop out of a solid downgrowth of the deep layer of the ectoderm. This is well seen in Elasmobranchs (Fig. 77, A-E) where a rounded solid lens-rudiment is formed by proliferation of the ectoderm, this rudiment becoming isolated and developing a cavity secondarily. It is of interest to notice that even here a slight dipping down of the external surface into the lens rudiment is apparent for a time (Fig. 77, B).

In Amphibians, Lung-fishes and Teleostoinatous fishes the lens arises in a manner intermediate between what occurs in Elas1nobranchs and what occurs in Sauropsida. In the forms mentioned the lens arises as a downgrowth of the deep layer of the ectoderm (Fig. 77, F-I) and in some cases this downgrowth is simply an invagination of this layer, the only difference from the Sauropsidan condition being that here the opening of the invagination is closed by the superficial layer being continued across it (Fig. 77, J, K).

As regards the later stages in the development of the lens all that need be said is that it undergoes an enormous increase in size--by absorbing nourishment from its surroundings, for it has no bloodvessels-——the cells of the deep wall becoming greatly elongated and taking on a clear glassy appearance, while the superficial wall remains as a layer of cubical epithelial cells over the outer surface of the lens. II EYE 139

SCLEROTIC, CORNEA, CIIOROID.-—These portions of the eyeball are gradually differentiated out of mesenchyme which becomes concentrated round the primary parts of the eye. hi the case of the

cornea the first stage in the developmental process consists in the accumulation between lens and ectoderrn of a clear jelly-like secretion

Fm. 77.—-Variations in the early stages of the development of the lu_-ma‘. A-I4}, I'ri.~<ti.ur1L.-: I"-I, ._\'im_1nn (after Rab], 1898).: J, K I’hyl£o-metlwsa (after Jimlgvtt-, 189:’).

continuous, and identical in character, with that which fills the optic cup. , _ As development goes on (Knape, .1909), a thin layer of this jelly-like material, about midway between the lens and the ectoderm, becomes condensed to form the rudiment of Descemet’s membrane. Amoebcid cells from the mesenchyme round the optic cup creep en. III THE ALIMENTARY CANAL 145


becomes extended into the form of a thick-walled tube-——the rudiment of the intestine (eat). From the stage of Fig. 80, E, onwards active growth of the true tail or postanal _region is taking place, and it is noteworthy that, during this process, the endoderm retains for a considerable time its continuity with the mass of actively growing unclifferentiated tissue at the tip of the tail and becomes drawn out into a cylindrical postanal ‘gut (pay). This remains conspicuous for a time but eventually clisintegrates and disappears completely. The main mass of yolk-cells, forming the ventral wall of the middle part of the enteron, gradually shrinks in volume, as the yolk is absorbed and carried off by the circulating blood for distribution to the growing and developing ialSS11(3S of the body, and eventually the gut Wall is no thicker in this region than it is elsewhere.

BUCCAL CAV1'rY.-——The alimentary canal of the adult Vertebrate commences with the buccal cavity which is in part at least-as shown by the presence within it of placoid and glandular‘ elements corresponding with those of the skin-——ston1odae.al in its nature. The stomodaeuui however is not as a rule developed, as is so usually the case in the Invertebrates, from a simple involution of the ectoderm forming a depression of the surface below the general level. It arises rather by the walling in of an area on the ventral side of the head through »the development of ridge-shaped outgrowths. These ridges may he termed respectively the maxillary ridge and the mandibular ridge accordingly as they give rise later on to the upper or to the lower jaw.

The roof of the buccal cavity, or at least its anterior portion, is simply to be looked on as part of the primitive ventral surface of the head, delimited by the maxillary ridge on either side. The floor, on the other hand, represents the mandibular ridge (Fig. 80, H, mm) which has grown forwards in a direction parallel to the roof. The inner wall of the buccal cavity is in close contact with the anterior extremity of the endodermal alimentary tube but for a time the two cavities remain separated by a thin membranous diaphragm made up of the apposed layers of ectoderm and endoderm. This may conveniently be termed the velar membrane as the organ known as the velum in Amp/m'0a3us or I’et7°omy/zen consists simply of the remains of this membrane.

The formation of the anterior, stomodaeal, portion of the buccal cavity is seen in its simplest form in some of the lower holoblastic

,Vertebrates such as Urossopterygians, Lung—fishes or Urodele


In Fig. 69, D (p. 126) in the case of I’7*()t0/ate7°us, or in Fig. 100 (p. 178) in the case of Pol]/pie-7"ws (see also Fig. 80, H), what will become later the anterior part of the buccal roof is seen to be simply a portion of the ventral surface of the head, bounded behind by the transverse mandibular ridge———the rudiment of the lower jaw——and on each side by the longitudinal maxillary ridge.

As is well shown in the figure of Polg/pterus, and as is also the

VOL. II L 11 EYE 141

all round, as they possibly did originally, have become crowded together during the. course of evolution into a single large bundle. on the ventral side of the cup. In accordance with the general principle of economy of tissue this bundle of nerve-fibres has become sunk into a deep notch in the wall of the cup-—the choroid fissure-—-so that it passes directly to the optic stalk.

While this is probably a correct statement as regards phylogenetic evolution, matters are somewhat simplified in the development of the individual, inasmuch as the choroid fissure is brought about not by the notching of the a.lready formed cup rim but by the rim ceasing to develop at the site of the choroid fissure while it grows actively everywhere else.

As regards the development of the actual nerve-fibres, all that need be said is that they first make their appearance in the wall 01' the optic stalk ventrally and that they increase rapidly in number, passing between the epithelial cells of the stalk, loosening them out,and causing them in great part, if not entirely, to degenerate. The individual fibres certainly for “ the most part become diffel-entialtcd in a FIG. 79. Transverse sv('ii()l1 through the still open neural cmltripetfll (h-rection plate of [man palmstrzs near its anterior end, showing the

_ _ . position of the optic rudiments (E) already marked out by ‘I/.6. l'[‘01I1 l':llO 1‘£'.l;11ld: l:0- the formation of pigment (after Eycleshymer, 1895).

wards the brain, but

whether this means that they are actually sprouting out from ganglioncells of the retina as is generally believed, or on the other hand that their fibrils are simply becoming differentiated centripetally within a continuous prc—existing protoplasmic connexion, remains to be demonstrated.

EMBRYOLOGY AND THE EvoI.U'r1oNAnY ORIGIN or THE EYE.-The peculiar reversed position of the Vertebrate retina may perhaps be taken as an indication that that organ had already come into existence, though no doubt in a very simple form, at a stage in Vertebrate phylogeny when the central nervous system had not yet sunk down below the surface. It is therefore of interest that in certain Vertebrates the rudiment of the retina does actually become apparent during embryonic development at a period when the medullary plate is not yet closed in. Thus Eycleshymer (1.895) has described i11 Rana pnlustmls and in Amblg/sloma how a patch of pigment appears for a time on the surface of the medullary plate (see Fig. 79) in the position which will later on form the optic outgrowth.

Although we are perhaps justified in believing that the eye of existing Vertebrates was already present as a patch of epithelium sensitive to light in the far back evolutionary period when the fore142 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

runner of the central nervous system was still a portion of the outer surface of the body, we do not, in the present writer-’s opinion, appear to be justified in connecting up the eye of typical Vertebrates with the “eyes” of Amp/mloams or of Tunicates. It seems more probable that the eyes of these highly specialized creatures are organs which have developed independently Within their own groups.

l’ITUITARY Bonr.——'J‘o be included amongst the derivatives of the ectoderm is that enigmatical organ the pituitary body (“ Hypophysis

cerebri”). This——the “anterior lobe” of the pituitary body in '

mammalian anatomy-«arises normally as an iugrowing pocket of ectoderm on the ventral side of the head, situated as a rule close to the hinder limit of the stomodaeum but in the case of the Cyclostomes just outside its anterior boundary. This pituitary involution extends inwards beneath the infundibulum. In the Cyclostomata it retains its original form of a tube communicating with the exterior, but in the gnathostomatous Vertebrates its outer end becomes gradually eoustricted into a narrow duet which in the great majority of cases becomes finally obliterated, so that the organ new forms a closed sac lying immediately underneath the infundibulum. The wall of the sac sprouts out into numerous tubular projections between which develops highly vascular niesenchyme, providing the rich blood supply necessary to the definitive function of the organ as a ductless gland.

As regards variations in the development of the pituitary involution: it may arise as a solvld ingrowth of ectoderm (Lung-fishes, Amphibians); it may be two-lobed (Teleosts) or three-lobed (Laeertilia) in its early stages ; its external opening may become secondarily displaced up on to the dorsal side of the head (Lampreys); its inner end may come to open secondarily into the pharynx (Myxinoids). As already indicated the wall of the infundibulum in the Gnathostomata comes into intimate relation with the pituitary body in the restricted sense, forming the so-called posterior lobe, or cerebral

portion, or nervous portion, of the pituitary body.


Agar. Anat. Auzeiger, xxviii, 1906.

Agar. Anat. Anzeiger, xxxv, 1910.

Assheton. Quart. Journ. Micr. Sci., xxxiv, 1892.

Aasheton. Quart. J ourn. Micr. Sci., xxxviii, 1896.

Balfour. Phil. Trans. Roy. Soc., clxvi, 1876.

Balfour. Monograph on the development of Elasmobranch Fishes. London, 1878. Bidder und Kupfier. Untersuchungen iibvl‘ die Textur des‘Riickenmarks und die

Entwickelung seiner Formelemente. Leipzig, 1867.

Boulenger. Taillr_-ss Batrachians of Europe. Ray Society, 1897.

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Cameron. Proc. Roy. Soc. Edinb., xxiv, 1903.

Cameron. Proc. Roy. Soc. Edinb., xxv. 1904.

Ooggi. Atti Accad.Liucei, Anno 286, Ser. iv, Mom. Class. Sci. fis., vi, 1889. n NERVOUS SYSTEM 143

Cunningham and Ma.cMunn. Phil. Trmis. Roy. Soc., B, clxxxiv, 1893.

Davies. Morph. .lahrb., xv, 1889.

Dandy. Quart. Journ. Micr. Sci., xlii, 1899.

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Dandy. Phil. Trans. Roy. Soc., B, cci, 1910.

Dohrn. Mitl. zool. Sta. Neapel, viii, 1888.

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Leipzig, 1903. Hartwig, O. and R. Das Nervensystoin und «lie Sinnesorganc der Merlusen. Leipzig, 1878. Hill. Journ. Morpln, ix, 1894. His. Uutersuchtmgen iilu-r die crstc Anlagc des Wirbelthierleibes. Die erste Entwickelung (lee Hulmchcnu in) Ei. Loipzig,d.868. Kappere, Ariéns. Report XVIItl1 International Congress of Medicine. London, 1913.

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Kerr, Graham. The Work of John Samuel Budgett. Cambridge, 1907. Klinckowstrom. Zool. Jalirl). (Anat;.), vii, 1894.

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Jena, 1905.

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Scammon. Keibels Normcntaf'cln zur Entwicklungsgcsclriclitc, xii, 1911. Schwann. Mikroskopischo Untersuchungen iiber die Ubercinstimmung in der

Struktur und dein Wachsthum der Thiere und Pflauzen. Berlin, 1839.

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Voeltzkow. Abh. Senckenbcrg. naturf. Gesellsch., xxvi, 1899.

Warren. Quart. Journ. Micr. Sci., xlv, 1902.

Wenig. Anat. Anzeiger, xliii, 1913.

Winkler. Arch. Entw. Mecln, xxix, 1910. CHAP'l_‘l+3R III THE ALIMENTARY CANAL

THE alimentary canal or enteron‘ of the V crtebratc consists of a tube passing from the mouth to the anus. The wall of this tube is known technically as the splanchnopleure in contradistinction to the somatopleure or body-wall (Ballour). It consists of an inner lining epithelium, the endodcrm, cnsheathcd in a complex coating of mesoderm——the splanchnic mesodern1———consisting of connective tissue, blood-vessels, lymphatics, nerves, and coelomic or peritoneal epithelium.

As is commonly the case in other metazoa the cndodermal lining is in the Vertebrate more or less encroached upon at’ the oral and anal ends of the tube by the spreading inwards of ectoderm. The parts of the tube which come thus to be lined with ectoderm are known as stomodaeum and proctodaeum (L-ankester, 1876) while the intervening region lined by cndoderm is known as the mesenteron. In the Vertebrata there is very slight development of proctodaeum but an important section of the buccal cavity is, as will be seen later, stomodaeal in its nature.

It is also customary in embryological writings to use the somewhat loose expression foregut for the anterior portion of the alimentary canal (reaching back to the pylorus or to the opening of the bile-duct), which in the meroblastic vertebrates becomes differentiated oil‘ from the yolk-sac comparatively early in de velopment. . _ . A good idea of the blocking out 01 the main regions of the

alimentary canal in one of the lower vertebrates is got by inspecting sagittal sections of embryos and larvae at different stages of development such as those shown in Fig. 80. From the gastrula stage (A) on to the stage illustrated in Fig. 80, C, the endoderm forms a simple sac with its opening posterior (anus) and with its ventral wall greatly thickened owing to the fact that its cells contain the main store of yolk. From the stage of Fig. 80, D onwards the foregut (f.g) becomes gradually constricted oil‘ in a tailward direction from the mass of yolk, while at the opposite end of the

body, correlated with the outgrowth of the posterior trunk region of

the embryo and the backward shifting of the anus, the yolky mass 144 152 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

Wards of the communication between olfactory and buccal cavities, a process which reachesits extreme in the Crocodilia where the palate extends back to about the level of the glottis.

STOMODAEAI. GLANDS.———Whereas in the majority of Fislies the stomodaeal lining possesses only isolated gland-cells, in the airbreathers on the other hand there are developed definite multicellular glands. These originate as a rule from solid down—growths of the

F10. 85.-View of the roof of the mouth in three species of Lizard (A, 19'_(/«ernw Ifingjivf ; B, Mabuia. qmfnqmflaemfata; U, Lygosonm. ‘l“ll.f(.’.S'('(’I'l.S‘), illustrating the shifting back of the communication between nose and month. (_ After Voeltzkow. 1899.)

rh, recess into which primitive posterior nan-s open ; pal, palatim.-. ; pt, pterygoid ; tr, transverse hone; no, vomer.

lining epithelium which develop a cavity secondarily. In Urodeles there is, as already mentioned, a special aggregation of these glands forming the gland-field in front of the tongue, while a single gland of considerable size develops from the roof of the mouth in the region between the olfactory sacs (lnterniaxillary or internasal gland).

In terrestrial Reptiles glands are present in numbers on ‘the roof of the mouth (Palatine), beneath the tongue on each side of the middle line (Sublingual) and along the edge of the month just external to the row of teeth -(Labial). The poison glands are specialized and enlarged labial glands of the upper jaw except in 146 EMBRYOLOGY 014‘ THE LO\V'ER VI|+}l't'l.‘EBRA’l.‘el'<}S (“.11.

case with I’roto1;le'2--u..s:, the huccal roof‘ in froiit, that is to say in the neighbourhood of the mesial plane, 1)&Lb'SGH without interi-upticm into the external skin: in other wo_rds the maxillary ridge is not continued to the mesial plane so as to meet its fellow. In later stages

I~‘1o. 80.——Sagitt9.1 sections through P()l;/p/.(:.-e:l.s‘.

A. 3t9-L'.0 14.: 13. St--".‘-W W: C. Stage 20: 0, stage 2: ; E, stage-24 +. (1., mos; m-, :ll.1'llI--llt.I'l‘()Il ; e-ml, "-l1‘l"J"1<‘J‘||l1 "71’: ‘‘“l'‘_‘(‘- W‘ ll"-.\' 3 f-’’- ‘‘”\'“.V H!‘ forvln-uin: f.!7. fun-gut: N. uo1..nclmr(l 2 2).,/I. l""i"“"‘.V "*1" (If hruin ll-mr; pin, pnneul rmlivm-n1"; .-_:_-, ¢-;u-i1_\' of spinal cum"! ; 3/, yolk,

the roof of the mouth would be hidden in a view from the ventra side owing to the forward growth of the lower jaw. ' The anterior portion of the buccal cavity in Urodele A11l1)l'1il)ifl.l1S arises in a manner essentially similar to that descrihed above. In the G-ymnophiona and the Amniota a characteristic 1'nodifi.cation of the mouth margin is‘ brought ahout hy the fact that, as III BUCCAL CAVITY 147

already mentioned, the maxillary ridge is cut across by the olfactory groove and so divided into the outer maxillary process and the inner median nasal process, the latter of which is continuous with its fellow across the mesial plane, forming with it the so-called

fronto-nasal process (see Chap. X.).

Fm. 8OA.~-—eS:t;;'lll:I.l Ht'('-ll()IlH txhroligh .I‘u/_:/}af:‘:'u.s".

1.‘, _\.1_ug., 3.3; G‘ smge -39; H, St:l‘L‘D‘[| :;-_>_ n, anus; u_«-, :ll|l.f‘l'l0l‘ (-onnnissllrn; 4-lo, optic cliiusrnu:

l clones.‘ ml enlmic c:l\'it.- : 1-]. heart : hm. halu-nnlar u-onnnissui'e: l1'., li\'<'l': m.r. m:m«lil.ul:u* r-i«lgo- , . . , Y _ _ _ 2,, pjt;ujt;n~y -;m-ulutimi ; pm, [_'M)h‘l.('l'lH1‘('l)]]1l|)iSfil|1‘!'; ,.n._:7, pH.~4l..'{ll:ll _-.;ut.: yum, pzuu-I-o-:it'Ir rudiment‘; /"rm. pineal rudiim-.nt.; 5’, .<t«mi:u:ln : y, yolk.

It is of interest to notice that in various Vertebrates the buccal opening is at first elongated in an antero-posterior direction instead of from side to side. Such is the case with Scylliuqn (Sedgwick, see Fig. 81) and ’1'o'rpedo amongst Elasinobranchs. In these cases the slit-like mouth is bounded on each side by a longitudinal ridge. 148 EMBRYOLOGY or rm: LOWER VERTEBRATES (:11.

Later on each ridge becomes sharply bent, about the middle of its length, in such a way as to give the buccal opening a rhomboidal shape and at the same time to mark oil’ the ridge into a maxillary portion in front and a mandibular portion behind. In Anura a somewhat similar arrangement is found.

“ENnonEuMAL” SECTION or BUCCAL CAvrrv.-—'l"‘he fully developed buecal ea.vity has incorporated in it a posterior portionvarying in relative extent in dil'l'erent Vertebrates—which is derived not from the ectoderm but from the anterior portion of the “endodermal” enteric rudiment. The simplest way in- which this portion becomes added to the anterior portion is seen in those Vertebrates in which the anterior part of the cnteric cavity is patent throughout development. In this case the velar membrane simply r u ptures——-its reinnants soon becoming absorbed-and the stomodaeal cavity is thrown into open communication with ‘ the cnteric cavity. This is the case in certain Anura (Rana) and in Amniota.

Fm. 8l.—--Ventral \'lt‘\\‘ of head region of embryos of Sag‘:/lliu-nz ¢-mu}-u/u. (After Sedgwick, 1892.)

A, 7—8 mm. ; 13, Sll_L','l)ll_\-' more :ulv:uu-ed than .\ ; C, H -12 mm. ; I), '16 mm.

brat-es no velar membrane is present, owing to the fact that the foregut either becomes solid for a time (Pol;/pteru.s, Fig. 80, D—Gr) or is so at the beginning (Teleostei, Urodela, Lepirlosvlren and Protopterus). In such cases the peripheral layer of the yolky foregut rudiment gradually assumes an epithelial character and the yolk along its middle breaks down, so that a cavity arises—continuous with the stomodaeal cavity and forming the hinder section of the definitive buccal cavity. The proportion which this posterior portion bears to tlfe anterior section derived directly from the outer surface is very different in different groups. It apparently attains its maximum" in Teleosts where

-it forms practically the whole of the. buecal cavity.

' Points of critical importance to the germ—1ayer theory are raised in this connexion by the fact that teeth, organs belonging originally to the outer surface, are developed in this posterior region of the buccal cavity from yolky “ endederm.” This is well seen in a Urodele, ‘or a lung-fish such as Lepidomlren or Protopterus (Fig. 82). The attempt is made to get round this difficulty by assuming that the layer of epithelium which makes its appearance over the surface of the buecal rudiment, and in relation with which the teeth develop, is really an ingrowth from the ectoderm.

In many V erte- T III BUCCAL CAVITY 149

It is, as a. matter of fact, quite continuous with the ectoderm,

FIG. 8‘2.—Sagittal section tl1rou;;l1 lu-.:ul I't’gi0Il of a Protopturus larva (Stage 33).

Inc, buccul ts-uvit-y: h.I, :ml<-riur l_u_nn1<l:u‘_\' of tongue; N, nulm-lnm‘41: pin, pine":-al lmtly: /W-I‘. pm-uphysi.-.: l’iI., pit: 5t.:u-_y bc«l_\': Th, tllymitl ruuliment; Lu, H.-rtum «-ptimluv. Th.-. p()sil.inn nr dvlllul rudiments is in<li<-.atml by Hue hm upwzu-d pr(r_ic:(:l.i()nS of the dOI".~m| wall of the buccal cavity.

but exaniinution of carefully prepared celloidin sections (Fig. 83) shows that at its inner end the epithelium passes by imperceptible

A 8

FIG. 83.—Sagittal N'(_‘llHllH t.h1'ough the 1'egi<_n1 of the lulucul cavity of (A) Lcpi¢.io.s£'rc1t, stage 30, and (B) .lmI:[.;/.s-Iowa, 7'5 mm. in i(‘ll§'.'_,'iiI.

b.c, bu(‘c::l opitllvlilllll ; 4'-cl, l‘L'tmlBl.'lll : _I/, .s'(_)litl Illziss of yolk-(.'I-ll.~: in pu.\'itiun 01' i.|ll(.‘('2tl vzivity.

gradations into the ordinary yolky endoderm, with no trace of the sharply defined edge which it would possess were it a 1uyer__of 150 EMBRYOIJOGY OF THE LOWER VERTEBRATES CH.

ectoclerm pushing its way inwards. It extends inwards simply by a process of delamination from the yolky “ endoderm.”

The real lesson to be learnt from these cases is that the charactcrs of one gcrm—layer are liable to spread over its boundary into l3C.5]‘l‘ll'.()Ty belonging to another layer or, in other words, that the territories of the various layers are liable to be separated by an indefinite debatable zone rather than by a mathematically sharp li.ne. It follows that the apparent position of an organ-rudiment in relation to such a boundary is not necessarily to be taken as

Fm. 84. —-Sagittal sections illustrating the development of the tongue in l_.l1'm_lclc..~'.

.\ and I5, Triton; C, Sula.-armndra (after Kallius, luol); _«_/.1‘, gland tie1d;__M, mandibular arch ; 7».I, priuuu-y t.ongLu.-.

giving any definitive proof as to which of the two cell-layers that organ belongs to.

Tim 'I"<mcUE.——The tongue is a portion of the buccal floor which becomes demarcated off from the rest by a split formed by a downgrowth of the lining epithelium of the mouth. is mode of development is well illustrated by what happens in Urodele Amphibians_as described by Kallius. Here tlwru develops first a primary tongue, ensheathing the anterior and ventral portion of the hyoid arch (Fig. 84, pt), which becomes marked off, except at its hinder end, by a deep groove in the floor of the mouth.

A liorseslioasliaped thickening of the buccal epithelium now III BUCCAL CAVITY 151

develops external to, and parallel with, the groove bounding the primary tongue, and consequently lying on the floor of the month between the primary tongue and the lower jaw. The thyroid involution is situated between this thickening and the tip of the tongue.

The ectodermal thickening develops numerous glands, each originating as a solid ectodermal down-growth, and is known as the gland-field. Externally it is bounded by a shallow groove. Later on the cleft or groove separating the gland-field from the primary tongue becomes obliterated by fusion ol‘_its walls, and the gland-field becomes raised up in a dorsal direction (Fig. 84, B) the tongue-tip shrinking backwards so that eventually the demarcation between primary tongue and gland-field disappears (Fig. 84, 0). Meanwhile the groove bounding the gland-field externally becomes deepened. It forms the outer limit of the definitive tongue which is thus a compound structure, its tip and edges developed from the original gland—field, its postero-median part from the primary tongue.

In the fishes the tongue remains non-muscular and non-glandular: it is simply the primary tongue. In the Axolotl the tongue appears also to be a primary tongue, the gland-field making a transient appearance as a rudiment but eventually undergoing atrophy (Kallius).

In the Amniota the tongue is, as in the terrestrial Urodeles, a compound structure, the primary tongue rudiment becoming fused with an elevation of the floor of the mouth lying in front of the Thyroid rudiment. This elevation, called by His the tuberculum impar, represents morphologically the gland-field of the Urodeles.

The tongue of Cyclostomes is remarkable for its complexity: it has complex muscular and skeletal arrangements and on its surface it develops the horny spines which function as teeth and simulate teeth in their appearance. In Bdellostoma. the tongue develops as a cushion-like swelling of the floor of the mouth at an early period while the velar membrane is still intact. In J’et9°0m_2/zen, on the other hand, it does not develop until the time of metamorphosis.

It has already been shown how the olfactory organs come to communicate with the buccal cavity by the posterior nares. In the Amniota these become sunk into a recess in the roof of the mouth and in the higher Reptiles, as in the Mammals, this recess becomes shut off from the buceal cavity by a horizontal shelf which grows in from the side and meets its fellow to form the palate. How this has come about in evolution is illustrated by the three Lizards shown in Fig. 85.

In ontogeny the mode of origin may be similar,’ the palatine outgrowths meeting and fusing with one another in the middle line (Crocodiles) or, as happens more usually, a median ridge or--septum extends backwards from between the primitive posterior nares: and the palatine processes meet and fuse with its ventral edge. In the two cases the physiological result is the same—-the shunting back170 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

twists upon itself, in such a way that points upon its ventral surface would move towards the embryo’s right side. (In other words the lung-rudiment rotates about its long axis in a counter-clockwise direction as seen from behind, its front end remaining fixed.) The

two lobes are the right and the left lung-rudiment but on account of

the rotation just mentioned which extends through more than 180° the left lobe at this stage represents what was originally the right side of the rudiment.

The two lungs of Lepiclcisiren or Prrotoptems are thus reversed in

A 5 C D

Fm. 96.-—-Dissections of mid-gut of L8})?:d()8t’I‘8‘?2- at stages 32 (A), 35 (B), 36 (C), and 37 (D), showing the modelling of the intestine and also the later stages in the development of the lungs. Seen from the dorsal side. ~

c.c, eloaeal caecum ; int, intestine; (.1, left lung; (Ii, liver; mun.d, Wolfllan duct; pan, pancreas ; ph, pharynx; r.(, right lung; sp, spleen.

position-—-the right lung of these forms being homologous with the left of other Vertebrates. An important detail is that in early stages the original right lung, '£.e. the definitive left, is decidedly larger than its fellow (Fig. 95, B). In later stages this inequality disappears, the smaller lung overtaking, the other in its growth (Fig. 96). .

In the ease of most individuals the lungs assume their dorsal position simply by growing directly tailwards, the oesophagus being pushed out of the way towards the left side (Graham Kerr, 1910). In certain specimens however, which doubtless in this respect retain I11 PH ARYN X 153

Ifeloderma. where they are the enormously enlarged sublingual glands.

Similar localized developments of the buccal glands occur in Birds and some of them may reach a great size as, for example, the enormous sublingual glands of the Woodpeckers.

PIIAI’.YN.\'.-—-The part of the alimentary canal which follows immediately behind the lmccal cavity is highly characteristic from the fact that in Vertebrates it is concerned with the function of breathing. The special organs which are developed to carry out this respiratory function fall into two groups one represented by the Lung‘——adapted for respiratory exchange with the atmosphere, the other by the Gills~—-adapted for respiratory exchange with gases in solution in the water. As the balance of probability is in favour of the latter being the more archaic they will here be considered first. .

The gills are seen in their most typical and familiar form in the various groups of Fishes where there is present upon each side of the pharyngeal region a series of visceral clefts—-slit-like openings leading from the pharyngeal cavity to the extei-ior—-—separated from one another by masses of solid tissue known as the visceral arches or gill septa. The walls of the clefts are highly vascular and their surface is commonly raised into conspicuous plate-like projectionsthe respiratory lamellae —which serve to increase the area of respiratory tissue.

In the most archaic arrangement, seen in Elasmobranch fishes, the front lip of each cleft, except the first, is prolonged backwards to form a small valvular flap overlapping the external opening. In the Holocephali, Teleostonii, and Dipnoi the anterior one of these flaps, that projecting back from the hyoid arch, becomes greatly enlarged to form the operculum which overlaps not merely one but the whole series of clefts lying behind it. Correlated with this the outer portion of each succeeding septum, which in the Elasmobranch gave origin to its valvular flap, has disappeared, leaving only the portion lying next the pharyngeal cavity.

The cleft lying in front of the hyoid arch—-the spiracle is usually modified, its respiratory tissue having been reduced and even its opening being diminished in size or completely absent, but its general relations in the adult are such as to permit of no doubt as to its serial homology with the clefts behind it.

Most usually there are on each side six clel'ts——a spiracle and five branchial clefts~ —but there is reason to believe that there was a greater number present in primitive Vertebrates——seeing that the number of persistent clefts becomes on the whole less as one ascends the vertebrate scale and that here and there among the more archaic forms a greater number than the usual is found (Bdellostoma, up to 14, Notidanus cinereus 7, N. griseus 6).

In a few of the more archaic Vertebrates there develop during larval life, in addition to the visceral clefts with their respiratory 154 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

lamellae or internal gills, respiratory organs of another type——-—the external gills. As there is some reason to believe that these are more ancient organs than the gill-clefts they will here be considered first although they are much less familiar than the clefts with their internal gills. The branchial organs will therefore be considered in the following order: (1.) External gills, (II.) Visceral clefts, (III.) Internal gills. (L) Ex'1‘1«3RNAL GI[.I.S.—~Tl1e true external gills are organs which are commonly confounded with the ordinary or internal gills developed in the walls of the gill-clefts. They appear however to be quite independent of these in their origin and they would probably have attracted more attention and interest than they have done had it not been for the fact that they occur in their typical form in only three subdivisions of the Vertebrates (Crossopterygii, Dipnoi, Amphibia) and that two out of these three groups comprise animals of extreme rarity, the developmental

mz_]V stages of which have not

been generally accessible

to emhryologists. 9-9-17 The typical External “C a W gill is a projection from ' ' the surface of the body - on the outer side of a

visc.eral arch. It consists of a core of mesen chyme with a covering Flu. 86.—-Diagrammatic longitudinal section through the (,f ectodenn; it is LI-a_

early rudiments of the external gills of Lepidosircn (Stage 25). versed by a vascular loop

e.g, external 1.',lll; end, endoderm; ma, \lHCel-‘ll arch; consistlng of ,the nlaln

m-, visceral cleft rudnm-nt. aortic avrcll Whlch P333353

out to its tip and then

doubles back; and it commonly has a pinnate form, paired projections

growing out so as to increase its respiratory surface. It is provided

with muscles by means of which the possessor is able to flick it sharply backwards so as to renew the water in contact with it.

The external gill as a rule is without any special skeletal support but in the larval Polypterus a short rod of cartilage projects into its base, and in the extinct Dolichosoma of the Gas coal of Bohemia there was apparently present a well-developed segmented skeleton within the substance of the external gills.

The external gill develops as an outgrowth from the tissue of the visceral arch at a period at which the clefts are not yet perforated. It arises as a bulging of the surface (Fig. 86) and in the author’s opinion the endoderm of the cleft rudiments takes no part in.its formation. At the same time it is only right to state that the prevalent opinion in the past has been different. The outer surface of the visceral arch in the region where the external gill will develop is covered by a layer of cells thicker than the neighbouring ectoderm, and in some cases this thickened portion of the ectoderm shows in its

e.g.I There is however no definite evi III EXTERNAL GILLS 155

deeper portions a rich deposit of yolk, so as to look exactly like the yolk-laden encloderm. Grcil explains this appearance by supposing that true endoderm cells actually spread outwards and replace the deep layer of the ectoderm, so that the external gill-rudiment would be partly endodermal in its nature.

dence of any such process taking place and the present writer would interpret the appearances as mean~ ing simply that the ectoderm covering the external gill-rudiment becomes thickened, and stores up a supply 01' yolk‘ in its deeper layers, as a physiological preparation for the active processes of growth which are about to take place as the external gill rapidly increases in length. In this he agrees with Marcus (1908).

The general appearance of the developing external gills is well seen in Hypogcopms (Fig. 87) or in Lepidoswlren (Fig. 200). In Lepvlolosiren there are present four B‘.1<_:, 37.---Hypogeophis eIul)i'y0s showing upon each side of the body. At ‘l3’,°1?1§“°“t_ ‘if89}}‘“ “"“""““l gm“first the four are quite independent ( W m“’_ ") _ of one another but as development .,.;-;;ii;...;.;‘l:;1i:,l.‘.‘,‘.. ""‘«i~§.. ’.’.;...§i?{Z.‘{‘ ..“.f.§1‘,‘..‘ ...if.’£; g0(-3S 011 they b£‘.COII18 raised UPOII EL projecting in Bfi-mu the hyoid 8.I‘(‘ll, and also conlu-1011 base SO as to give the from the mandibular arch in front of it, are

__ . _ . p0ssil)l_\' u-xiurnal gill rudiments which do not 3:PP93—T3'l1(39 of 3' 3111819 Organ wlth go on with their development.

four branches (Fig. 200, B-E). The distribution of true external gills amongst the main groups of Vertebrates is shown in the following table:


,—-.-—-q-——.._.—_.__—j__..._ . __ - .. .- ._ . ...--..- -.


l 3 V I. II. III. I\'. ‘V. ‘ ' VI.” ' iscvral .\l'L'lI. ' _ . . . l-‘irsl ' .\'.4-Hnltl 'l‘ llI'( u Four‘: M‘l'"1lb“l‘w‘l Hymd‘ Jlr:1m-hi:ll. Iii‘.-lnuliinl. 3 Bram-hinl. 3 ll:'.'ui(.-lii:Il.g Elasmobranchii. . ; Crossopterygii . . 5 x . lhpnoi. . . . g x x x x Amphibia . . . - 'v.*" 2:. x y x x i Amniota . . ' i 4 I 1

r:..\'o'sLi_~,'iul. In those animals in which they are well clovoloped the external gills are for a time the main functional breathing organs. They are 156 EMBRYOL()GY OF THE LOWER VERTEBRATES CH.

richly vascular and the renewal of the water in contact with their surface is provided for by a well-developed muscular mechanism by which they are sharply flicked from time to time, or, in early stages, by rich ciliation ol"tl1eir surface as in the Frog (Assheton, 1896) or 6'73:/ptolzramz/ms (Smith, 1912). They are as a rule merely temporary organs. As the respiratory function comes to be sufficiently performed by other organs their circulation becomes sluggish, their tissues moribund. They become invaded by leucocytcs and eventually unclergo complete atrophy. in .l’o~otopm~us distinct vestiges persist for a prolonged period while in various Urodeles they remain functional throughout life.

The external gills, highly vascular and projecting freely into the surrounding medimn, present tempting objects for attack by other organisms. They are therefore extremely liable to injury, and correlated with this they present a high power of regeneration. in correlation also with the same fact we find that they tend to be eliminated from development in certain members of groups which are as a whole characterized by their presence. Such is the ease in the Amphibia where they are characteristic of the group in general but where in particular cases they are reduced (II;z/la n;'rb0'rea) or completely absent (}>’ovmb'mator) although we must believe they were present in the ancestors of these forms.

This tendency for the external gills to become eliminated from development in the process of evolution raises the interesting morphological question: were External Gills at any period more widely distributed amongst Vertebrates than they are at present? And, if so, are their vestigial representatives still to be found in any cases where they no longer develop as functional respiratory organs?

This interesting problem, which offers an inviting field for research, has not yet had sufficient attention devoted to it. Even if it were the case that external gills once existed in the ancestors of forms in which they are no longer present as functional organs there is always the possibility if not probability that their disappearancehas been so complete as to leave no observable trace. Nevertheless such vestiges might persist and are worth looking for.

Under these circumstances it is of interest to note that already certain structures are known which are interpretable as vestiges of once-present external gills. Thus in Gymnophiona what appear to be transient rudiments of mandibular and hyoidean external gills make their appearance during development (Fig. 87, B). Again in the case of the Mandibular and Hyoid arches of Urodeles, on which no functional external gills develop, Driiner (1901) has found what appear to be vestiges of the muscles of external gills. Again in the larvae of various Urodeles there occurs in connexion with each mandibular arch a curious styliform projection known as the balancer, from the fact that the larva balances itself upon them as upon a pair of limbs (Fig. 88, b). Each of these has a vascular loop within it and it in fact appears to be the modified external gill of III . EXTERNAL G-ILLS 157

the mandilmlar arch which has lost its respiratory and taken on a supporting function.

While external gills occur within three main subdivisions of the Vertebrates, namely Teleostomatous fishes (Crossopterygians——the most a.rchaic of existing Teleostomes), Lung-fishes, and Amphibians, there are two main groups-—Elas1nohranchs and Amniotes---in which they are conspicuous by their absence. Having regard to the tendency of the organs in question to disappear (as in the cases already alluded to amongst the Amphibia) their absence in a special group would not in any case constitute strong evidence that they were never present in the ancestors of that group. As it happens however there is in the two groups mentioned a definite cause which seems quite competent to account for the disappearance of external gills, namely the development of'_ a new organ —— the yolk - sac with its highly developed vitelline network of blood-vessels»--which in addition to its primitive

function Inust neces- 88.%l‘hii'eie larval (_lt:l't'l()})lllt‘lll. of a ‘l'l(f\\'loW

sarily also function as it famiu/us) as seen from above. (After Egert, very efficient organ of '

respiratory exchange and what looks like :1 posit-rior 4-..\'tc-rnal gill is the ]w(:L-()1‘fll limh. SO render 311)’ Pre'eX-1st‘ In l"ii-_:.s'. ll and (l flu-1-Xternal _«_;'ill:~' lmve l)l',‘(‘ll cut away leaving ing respiratbry organ no only tll(‘ll,'l)-‘mill .~'i-urnps.

longer necessary.

Taking into consideration the presence of external gills in three archaic groups of Vertebrates it seems to the present writer to be clearly indicated that these organs are a very ancient characteristic of the Vertebrate phylum. The only alternative indeed is to regard them as having become evolved independently in the three groups in which they occur. It is diflicult to accept this as in any way probable having regard to the similar morphological relations of the organs in question.

It might be suggested that somewhere on the course of a large blood-vessel, such as an aortic arch, would be a most natural place for the development of a new respiratory organ. Such a suggestion however is entirely fallacious for simple physical reasons: for new breathing organs will tend to become evolved -not on the course of a

b, lnilaiurei-; !'.§I,i'_\t91‘l1:ll gillol'lir.-1. ln'anchial:1rch. In l«‘i_«,v-. A ' 158 EMBRYOLOGY OF THE LOWER V ERTEBI-LATES (311.

large vessel where the quantitative relation of surface to volume in the blood-vessel is at its minimum but rather where there is present a rich superficial network of capillaries, in which the ratio in question is at its maximum. .

(IL) VISCERAL CLEFTS. --The visceral clefts develop in what appears to be the most archaic method in Lampreys and Elasmobranehs Where each arises as a lateral pocket (visceral pouch) of the pharyngeal wall which meets and fuses with a., much shallower, ingrowth of the ectoderm, the apposed portion of cndoderm and ectoderm breaking down so as to bring about a free communication between pharynx and exterior. Each cleft thus consists of a, usually much larger, inner portion lined with endoderm and an outer portion lined with ectoderm.

The most frequent type of modification of this probably primitive mode of cleft development is that so usually met with in the development of hollow organs, namely that the cleft-rudiment, instead of being a hollow pouch from the beginning, is for a time in the form of a solid lamina of endoderm, which only at a later period develops a cavity in its interior and becomes an open cleft. This modification is found in Teleostomatous fishes, Lung-fishes and Amphibians.

111 the young Elasmobraneh the gill-clefts are at first long slits "traversing the whole dorsi-ventral extent of the lateral wall of the pharynx. Each septum or arch grows back at its outer edge to form a valvular flap overlapping the cleft next behind it. In most cases this backgrowth fuses with the next septum at its dorsal and ventral ends so as to reduce the external opening of the cleft to a comparatively small dorsi-ventral extent.

In all Gnathostonies, excepting the typical Elasmobranehs but including the Holocephali, the hyoidean backgrowth becomes greatly enlarged to form the operculum which overlaps the whole series of clefts behind it. Correlated with this the outer portions of the subsequent septa with their backgrowths become reduced. I11 these cases we frequently find a marked tendency for the edge of the opercular backgrowth to become fused with the body so as to restrict the size of the opening behind it. Thus in the Eel the opercular opening becomes reduced to a small persistent ventral portion, while in S3/mbmncltas the same holds but in this case the two openings have fused together to form a small ventrally placed median

ore. P A similar condition to this occurs in the tadpole of Discoglossus while in other Anura the persisting opening is displaced to the left side. Finally in Amniotes the fusion of opercular margin with bodywall takes place along its whole extent so that the branchial region becomes completely enclosed (see Chap. X.).

SPIRACLE.-——The spiraele or hyomandibular cleft always shows a considerable amount of modification. In Elasmobranehs its dorsal portion alone becomes perforate, although fusion of the pouch with the ectoderm takes place throughout its whole dorsi-ventral extent. .the Amniota the distal portion of the

I I r GILLS ' ' _ 159

hespiratory lamellae develop only on its anterior wall and these, as development proceeds, become vestigial forming the pseudobranch. In Teleostean fishes the spiracular pouch (Fig. 89 A, cc. I) flattens out and disappears (Goette) so that the pseudobranch (pa) on its anterior wall comesto lie on the inner face of the base of the operculum and appears to belong to the second cleft (Fig. 89, B). In Lung-fishes the soli.d endodermal rudiment never becomes perforate. It becomes gradually reduced during development while "its outer ectodermal portion becomes, as already indicated, converted into a special sense-organ. In Anurous Amphibians and in

cleft rudiment becomes greatly dilated to form the tympanic cavity, while the proximal part forms the relatively narrow Eustachian tube.

Just as the varying condition of the spiracle indicates a tendency for this cleft to undergo reduction so a similar but still more marked tendency exists for the gill clefts to become reduced at the other (posterior) end of the series. This is illustrated in the first place by the reduction in the number of functional clefts seen in passing from the lower Vertebrates to the higher. It is also frequently manifested in developmental stages. Thus 81110118317 the Amphibia we find Flu. 89.—-Horizontal sections through that in the Gry1llI'l()pl1l0Ifl& (Hyp0g(3- Salmon embryos explaining position Ophis, Marcus) 3 rudilnentary 7th cleft of pseudobranch. on inner surface of

_ . . operculum. (Atter (Joctte, 1901.) makes its appearance though it never _ ' L. ‘ reaches the eehederm, while the 6th ...;i;Z'.'..i‘.i1'.?."i...:f:I?f:...:f:f:...?:II%‘:'§1..?鑧?'.;....:iZ.; lS 0p9Il £01‘ 3. time. III UFOdBl8S EL l and II; II;/,l1_yoi«l ar«.'.l1; -Ti-, ope-rculum; rudiment appears and is for a time :"{"\"i"“l'jl‘-I3"Cf:-¥.g1*ll1tl'3'IIx2 1»-'vwlobw'=tnc1»; connected with the ectoderm but does °’ W” (T ' not become perforate, while in Anura this cleft appears only as a small and transient rudiment which never reaches the ectoderm.

(III.) INTERNAL G1LLs.——’_l‘he internal gills or respiratory lamellae arise as ridge-like or, at first, finger-like projections of the cleft lining. The chief matter of dispute regarding their development has been the question whether they belong to the endodermal or the ectodermal portion of the cleft lining. In cases where, as frequently happens, the lamellae begin to develop after the cleft is completely formed, the appearances are sometimes in favour of the one sometimes in favour of the other interpretation. Goette (1901) in fact goes the length of regarding the lamellae as being of endodermal origin in the case of the spiracle and ectodermal in the case 160 EMBRYOLOGY 0 F THE LOWER Vl1‘.lt"El3l\’.A'l‘l+]S (‘.11.

of the succeeding clefts, so that the spiracular pseudoln-ancli would on a strict interpretation of the germ-layer theory not be serially homologous with the other gills.

In the present writur’s opinion, as already indicated, such ul)S61‘vations upon the first origin of organs which develop in the region of the blurred boundary between two layers are not to be taken as afihrding evidence ol' any serious importance in regard to the morphological nature of such organs. Greater weight however seems due to evidence obtained from cases where the hrst traces of gill laniellae are visiblq; at a period before the bounding inmnbrane of the cleft is ruptured, when the cleft consists still of two distinct pnnches—ene eetoderinal, the other endodermal——separatcd by a still eeuiplete partition. Such is the case in Aci_pc'nscr and (ioette shows that in this case the laurella-rudiments arise outside the

partition from what is undoubtedly an ectodermal surface (see Fig. 90, g.l).

Pl’ :3" '|‘he same discussion extends to the ' general lining cl’ the cleft~—as to how

go. much of the lining of the adult cleft is

/ ectodermal and how much endodermal.

-7" }octte and Morofl'(1902) hold that only

|"1u.90.—~ll0rizontal:-.m~1ionthrough the portion of Lhe cleft -in the innuebmwhial reg.“ M. ymmg AOL d1ate_ IlBlg'lll)Olll‘l100(‘l of its pharyngeal peust-r showing the ('('f()de‘[‘[[]a1 opening 18 to be regarded as endodermal, <(>‘I3:.:':It1e01'1f)1(I)*51s)i1l1am011ne- (Atter all therest. being ectodermal. But here ‘ ’ ‘ ° again 11] view of the blurred character l.ll'iiI"‘ll‘.'ll”,Iiill,:i|l\(ill«l:ii(ill?:i:;‘,]ii;:.:iI('lii.llfllll: (.)f the boundary betvlreen the two layers p;,, ..,...._,. .,,~,,1...,_,..x_ it seems hardly profitable to speculate on the matter.

In certain fishes the gill-lamellae are for a time prolonged outwards into long threads which project through the cleft opening into the surrounding fluid. Such is the case in the embryos of F.lasn1ebranchs, in which it is only the lamellae upon the posterior face of each arch that become prolonged, those on the anterior face not projecting beyond the edge of the septum. Eventually the projecting part of the filament disappears while its attached basal portion becomes the definitive lamella. In a few Teleosts a similar temporary modification of the lamellae takes place ——~perhups the best example being Gymnarclms (Budgett, 1901; Assheton, 1907. See Fig. 199).

EVOLUTIONARY HISTORY or rm-1 BRANLIHIAL RESPIRATORY ()RGANs.——-As regards the early evolutionaryhistory of these branclnal respiratory organs one very generally accepted View looks upon the visceral clefts as being the most primitive, the internal gills as having developed next, and the external gills as being due to secondary extension of respiratory tissue outwards from the clefts. It seems however, bearing in mind what we now know regarding the development and distribution of external gills, at least equally ii’ llnl. III LUNG 161

more probable that the evolution of these organs has been in the opposite direction.

On this latter hypothesis the external gills would be regarded as the primitive respiratory organs, inherited probably from prevertebrate ancestral forms. The evolution of clefts between their bases would be explicable as an arrangement for pumping water over the surface of the external gills, while it could be readily understood that the respiratory tissue would then tend to spread inwards along the lining of the clefts, where it would be both advantageously situated for carrying out its breathing function and, at the same time, protected from the dangers to which external gills are exposed. The development of respiratory lamellae to increase the area of this respiratory tissue on the wall of the cleft would be a further and natural development.

The chief difficulty in the way of accepting this as a working hypothesis lies in the existence of animals admittedly near the base of the Vertebrate scale—such as Amp/2/ioxus and the Cyclosto_ mata-—in which there are no external gills and no vascular yolk-sac to account for their disappearance. This difficulty is undoubtedly a serious one but on the whole the present writer is inclined to think the difficnlty is not so great as to justify the immediate rejection of the hypothesis: it becomes less formidable when it is borne in mind that the forms mentioned although evidently archaic in some of their characteristics bear in others equally convincing evidence of high specialization. _

LUNG.—-In all the groups of Gnathostomata excepting the Elasmobranch fishes the pharyngeal wall develops a great outgrowth which, as will become apparent later, is to be looked upon as homelogous throughout the series and as primarily respiratory in its function-——the lung. The lung appears in its most familiar and typical form in the tetrapod Vertebrates and its development in these will accordingly be considered first.

Here in an early stage of its development the lung is in the form of a pocket of the pharyngeal floor projecting downwards in the mid—ventral line. This pocket commonly makes its first appearance as a longitudinal groove or gutter in the floor of the pharynx at about the level of the last ‘visceral cleft. The groove becomes constricted off from behind forwards, so as to form a blindly ending pocket communicating in front with the pharyngeal cavity by a narrow opening—the g‘lottis—and extending back immediately ventral to the pharynx. The blind end of the pocket grows actively tailwards and becomes deeply bi1obed—-—the two lobes becoming respectively the right and left lung, while the unpaired portion connecting them with the glottis becomes the trachea or pneumatic duct.

While the lung passes in its early history through stages corresponding on the whole with those described there are differences in detail in different groups-—-the most conspicuous of these variations


being, as is so often the case in the development of hollow organs, that the rudiment is at first solid and the cavity appears secondarily in its interior. This is the case in various anurous amphibians and in Jlepiolosofirevz and .1’-r0t01ate'/"as.

It has been indicated that the lung is primarily a ventra.lly placed pocket of the pharyngeal wall, that is to say its wall is a portion of splanchnopleure. It follows that the cavity of the lung is lined by endoderm while its outer layers (connective tissue, bloodvessels, muscles, etc.) are composed of splanchnic mesoderm.

As regards the further development of the lung, the main steps are concerned with its respiratory function and have to do with the increase of the respiratory surface. In such an animal as the Newt, where the lung retains a relatively primitive condition, the endodcrmal lining grows equally as the organ increases in size, so that even in the adult the lung has the form of a simple sac with smooth endodermal lining. In a Frog or a Lizard, however, growth activity is specially marked at particular spots so that at these spots the cndoderm forms outward bulgings into the covering of splanchnic mesoderm.

In these Sauropsida in which the pulmonary apparatus reaches its highest degree of evolution (Tortoises, Turtles, Crocodiles and Birds, in an ascending series) these pockets of the endodermal lining become more and more extensive, and more and more complicated, so as to give rise to a thick spongy mass, which forms the bulk of the lung, surrounding the now relatively small clear central space. The latter, forming as it does an apparent continuation of the bronchus or paired portion of the trachea, is spoken of as the intrapulmonary bronchus. Further the respiratory function becomes concentrated towards the terminal portions of the pockets, their proximal portions forming simply conducting channels-— branches of the intrapulmonary bronchus.

In the Chameleons, towards the end of development, a number of the endederm outgrowths bulge out beyond the general level of the surface of the lung upon its ventral side. These persist in the adult as large diverticula which when the animal blows itself out are inflated with air. In the embryos of Birds similar outgrowths make their appearance, four from each lung, but in this case as development goes on the outgrowths continue to increase in size and form the characteristic air-sacs of the adult bird.

THE LUNG or BIRDs.—-—As the Birds, in correlation with the intensely active metabolism as indicated e.g. by their high body temperature, stand pre-eminent amongst Vertebrates in the high stage of evolution which has been reached by their lung, the ontogenetic development of this organ will be followed out in a little more detail (Moser, 1902; J uillet, 1912).

In the Fowl the pulmonary diverticulum of the pharyngeal floor makes its appearance about the beginning of the third day. By the end of this day the rudiment is bifurcated at'its hind end, each lobe III LUNG 163

being the rudiment of a lung in the restricted sense and containing a prolongation of the enteric cavity lined by tall columnar endoderm cells. Outside the eiidoderm is a thick layer of inesenchyme and this in turn is covered by columnar coelomic epithelium.

The endoderm-lined cavity is destined to become the main intrapulmonary bronchus—-the mesobronchus. This remains unbranched until the fifth day when its cndoderm begins to bulge out, near the point where it enters the lung, to form the first entobronchus. During further development a. series of three other entobronchial outgrowths sprout out from the external surface of the inesohronchus close behind the first outgrowth. The four entobronchi so arising are closely contiguous and form a longitudinal row (Fig. 92, El-E4).

A set of similar outgrowths make their appearance spaced out along the mesial side of the mesobronchus posterior to the entobronchi: these are the rudiments of the ectobronchi. A third set of outgrowths on the lateral 0 side of the mesobronchus ejcf. are the rudiments of the Z‘ small secondary lateral bronchi (Campana). Of these sets of outgrowths the first and second are the most important and they are arranged in a slightly spiral row along the wall of the meso 51: bronchus.

The mesobronchus, as FIG. 9l.—_Diagraiii illiistratiiig the arrangement of the it grows in length main air-passages in the lung of the Fowl as seen 3

h b from the mesial plane. (After J uillet, 1912.) assumes a Somew a ' l(’ is‘ c .. uni‘ an eii'.0i« 'm-shaped curvature. by M’ l'its?‘.1...;o§i3o:.:iii§?',..i,-,',....r:£.,.;~.)i.¢l.i.m" which the Group of ecto- ~

bronchi are: carried towards the (1'lO1‘Sa.fl facéa fof the lgng while the entobronchi are nearer the ventra sur ace c . Fig. 91 . Both ectobronchi and entobronchi grow rapidly parallel with and close to the surface of the lung-rudiment. They soon produce secondary branches as projections of their walls and these secondary branches increase greatly in length traversing the substance of the lung at first close to its median surface and, later, deep down in its substance as well—-—the eiitobronchial branches growing in a dorsal and the ectobrauchial in a ventral direction.‘

The two sets of branches fits their t1% 1E:p‘pI‘01f1it(3l1 1(l)I1e another Iarg seen to alternate in position ( ig. 91). en t ey ave approac e closely each branch bifurcates and its two tips become closely apposed to the two tips belonging to the other serieswhich lie closest to them. About the thirteenth day these apposed tips become completely fused and their cavities continuous so that there is now

I/I///‘I/l-:’I"'.. T '


established a series of channels running in a dorsiventral direction through the substance of the lung aml communicating dorsally with the ectobrcnchi and ventrally with the entobronchi. The channels in question are termed parabronchi (Fig. 91, par). These are embedded in an abundant matrix of mesenchymc which from about the tenth day becomes divided up into more or less prismatic masses each having in its axis an individual parabronchus—the prisms being delimited from one another by the development of intervening blood-vessels. The mesenehyme which constitutes the inner portion of this sheath round each parabronchus becomes later replaced by a layer of smooth muscle fibres.

At about the same period as the fusion of the parabronchial tips takes place, the Wall of the parabronchus begins to grow out into numerous little pockets arranged in radiating fashion. These extend outwards, perforating; the muscular sheath, and at a short distance from the parabronchus divide into branches which in turn elongate and become the air-capillaries of the fully developed lung. Judging from adult structure it would appear that the tips of these fuse with others to form the continuous air-capillaries so that the latter would be formed much in the same way as the parabronchi but it has not been possible, so far, to demonstrate this by actual observation.

The essential features of the development of the Bird’s lung as above outlined may be summed up in the statement that in this type of lung the diverticula of the intrapulmonary bronchus, which in other Vertebrates end blindly, become here joined together tip to tip to form continuous tubular channels. To allow this arrangement to function efficiently an apparatus is needed to force the air throu h the system of respiratory tubes: such an apparatus is provi ed by the air—sacs.

AIR-SACS.-—-The ventral part of the lung-rudiment is for a time formed of a thick mass of mesenchymatous tissue which has been termed by Bertelli the primary diaphragm, from the fact that it becomes continuous along its lateral margin with the side wall of the splanchnocoele, so as to form a kind of floor separating off the lung from the splanchnocoele which lies ventral to it. The air-sacs arise as outgrowths of the bronchial cavities and are on each side four in number: the first or most anterior giving rise to the cervical sac, the second by bifurcation to interclavicular and anterior thoracic sacs, the third to the posterior thoracic and the fourth to the abdominal sac. The rudiments sprout out into the substance of the primary diaphragm and become greatly distended within it, bulging out ventrally amongst the viscera so that the ventral layer of the diaphragm becomes stretched ‘out into a thin membranous wall delimiting the cavity of the air-sac on its ventral side. The dorsal part of the primary diaphragm, lying above the air-sacs, persists as the floor of the lung or secondary diaphragm (ornithic diaphragm of Bertelli, pulmonary aponeurosis of Huxley). III T AIR-SACS 165

The air—sac rudiments sprout out (Fig. 92) from the main pulmonary cavities-—the cervical from the first entobronchus, the interclavicular and anterior thoracic jointly from the third entobronchus, the posterior thoracic and the abdominal from the mesobronchus. Later on additional secondary communications between the air-sac cavity and the pulmonary cavities are established (except in the case of the cervical air-sac) by means of the recurrent bronchi of J uillet. These arise in the ordinary fowl about the tenth day of incubation in C3,. the form of outgrowths of the wall of the air-sac either near its tip (interclavicular and anterior thoracic) or just before it emerges through the general surface of the lung (posterior thoracic and abdominal) as shown in Fig. 92.

These outgrowths burrow into the superficial layer of the lung, branch and become joined up, in a manner the details of which have not yet been worked out, with the system of parabronchi. The communications are visible in suitable preparations of the adult lung as groups of openings, each group leading in into the lung from the appro- /0’ ./ priate air-sac——those of the interclavicular and anterior 05thoracic lying towards the FIG. 92.——])iagranuuatic view of the right lung of lateral edge Of ’Dl]6 ventral a Fowl embryo of the tenth day as seen from

surface of the lung, about the “:9 V°‘:"“‘(j{%:éri11;1::fi%::i'1s1 ;>1'is_iI{Ihe0fflt)1l:<; . a r-sac . c '-, ~ level of the attaclllllent of entobronchi are shaded.

the bronchus’ and those of rib, abdominal air-sac; at, anterior thoracic air-sac: the POSl73ri0r th0ra»0i0 and car, cervical air-sac; 14."! and 164, llrst and fourth entoabdonlinal sacs near bronchi; tc, iiiterclapicular air-sac‘; -nies,tn:)¢sst)ll;1;otrl1sch1is;

    pl, pUHl3('3I'10I‘bl'|0I‘8a('alL fllI"8{lC, T, I‘l,LllII‘0-ll P01. 1 ...

close to the direct opening between it and the corresponding air-sac. It would appear that the function of these recurrent channels is to conduct the air forced out of the air-sacs in the expiratory effort through the system of air-capillaries, the muscular coat of the parabronchi doubtless playing an important part in directing the passage of the air through the system of air-capillaries rather than through the parabronchi themselves. a The formation of the air-sacs does not exhaust the remarkable

proliferative powers of the wall of the lung in Birds. Further out III A IR—‘I'._LA DDER 167

FIG. 93.-—-Development of the air-bladder of n Teleost. (After Moser, 19,,4.)

A, Jmodeus, 5 mm., longitudinal section; B, Rh-Od¢'ll.$', 6 mm., longitudinal S(‘(!U()lI2 (.‘., Rlmdemz, 7 mm., trans-vt-rse section, showing small pouch-like mxtgrowtli of pneumatic duct; uml, emlu«lu'r1|1; cut, enteric cavity; 2, uir-bladder; Ii, liver; N, notochord: mt, pronephric chmnbur; p.41, pm-.Iu1m.tic duct; '_l/, yolk. 168 EMBRYOLOGY OF THE LOWER VERTEBRATES (in.

to form a kind of diaphragm perforated in its centre and capable of being thrown into vibration by air being forced from one chamber into the other so as to function as a sound-producing organ (e-._g. Gurnards). Other outgrowths may develop: thus for example in many Siluroids numerous branched projections are formed along each side of the air-bladder.

The air-bladder rudiment is at its first appearance in some cases approximately dorsal in position (Selma). In Jihodeus Moser (1904) has shown that the diverticulum is at first on the right side of the alimentary canal. The same observer found that during the early stages of development of the air-bladder the portion of alimentary canal from which it springs undergoes a process of rotation about its long axis in such a direction that a point on its dorsal surface is carried towards the left side.

Although the actual development has been worked out only in a few cases, we may infer safely from the adult relations (Rowntrce, 1903) that the amount of this rotation differs greatly in different

.members of the group Teleostei. Thus in Siluroids and Cyprinodonts

the glottis or pharyngeal opening is in the adult still to the right of the mesial plane; in others such as the genera 0smer'us, Olupea, Olwrocentrus it is practically median; in still others such as Mormyrids, Characinids, Gymnotids and Cyprinids it has passed the mesial plane so as to lie upon its left side, while in the case of the Characinids Jllacrodon, Erythmlnus and ]}r’b'ias'i'na the glottis has come to be completely lateral on the left side. This rotation of the gut in the region of the glottis is of much morphological importance as will be shown later.

In the young Rhodeus, 7 111111. in length, Moscr finds that a wellmarked diverticulum from the pneumatic duct is present (Fig. 93, 0). Later on it gradually disappears. A similar diverticulum occurs in Salmo and in the Carp, and in all probability in numerous other Teleosts: its morphological significance will be discussed later.

ACTINOPTERYGIAN GANOIDS.——In these fishes the development of the air-bladder takes place on similar lines to that described for Teleosts. In Amda the additional detail has been made out that the rudiment is at first in the form of a longitudinally placed groove which becomes constricted off from the alimentary canal from behind forwards just as frequently happens in the case of the typical lungrudiment of air - breathing Vertebrates (Bashford Dean, 1896; Piper, 1902). A rotation of the section of alimentary canal in the region of the glottis takes place similar to that which occurs in the Teleost.

LUNG-FISHES.-—In the adult Oeratodus an organ occurs which is equally lung and air-bladder. It forms an unpaired sac lying dorsal to the splanchnocoele just like a typical air-bladder, but the pneumatic duct, instead of opening directly into the alimentary canal dorsally, passes round the right side and opens by a ventrally placed glottis. In Lepidosiren and Protopterus the general arrangement is m i LUNG _ 169

the same except that here the organ is deeply bilohed: a right aml a left lung or air-bladder occupying the place of the single organ of 0'e'ratodus.

The meaning of the ventral position of the glottis in these Lungfishes, and, in fact, the morphological nature of the whole organ, is

Flo. 94.--Transverse sections through the endoderm of the pharynx showing an early stage in the development of the lung.

A, Polypterus, B, (}'era,tmIu.,g, and O, Bmn..h1',nato1' (O aTl5er Goette, 1875). 1, lung-rudiment; ph, pharynx.

demonstrated by the examination of early stages in development. In these the organ is found to be a perfectly typical lung-rudiment (Fig. 94, B)-——a mid—ventral projection from the pharyngeal floor of precisely the same kind as that found in te_trapodous vertebrates (C).1

Fm. 95.——Views showing early stages of the lung-rudiment of Protopterus as seen from the ventral side (stages xxxii, xxxiv, xxxv).

e.g, external gill; I, lung; oes, oesophagus; pan, dorsal pancreas; ,2. f, pectoral limb; Th, thyroid ; v.c, visceral cleft rudiment. (Cut surfaces are inclieatml by uniform light tone.)

Subsequent stages are illustrated by Figs. 95 and 96. The lung rudiment at first a rounded knob (Fig. 95, A) grows backwards and soon becomes bilobed (B). The figure does not bring out one important fact namely that the lung-rudiment as it grows backwards

1 The projection is at first solid in the case of Lcpvidoseren and Protopter-us. III CEMENT-ORGANS . 179

head on each side as shown in Figs. 100, A, and 197, C, 0.0. A longjtudinal section through the centre of the organ at about this stage (stage 26, Fig. 101, E) shows that the organ is covered hy the ordinary 2-layered ectoderm. Round the lip of the opening at its

Flo. l0l.——Illustrating the development of the cement-organ of l’oly_pterus. B represents part of a transverse section, the other figures portions of horizontal sections.

A and B, stage 20; C, stage 23; D, stage 24; E, stage 26. mo, cement-organ. The darker tone indicates ectoderm.

free end, the superficial layer of ectoderm stops, while the deep layer seems to dip down as a deep involution to form the secretoryepithelium (c.o) which lines the cavity. All the appearances seem to point to the secretory epithelium being ectodermal in its nature. How deceptive these appearances are will be gathered from an inspection

of ‘ig. 101, A-E. III LUNG 171

the archaic mode of development, the lung-rudiment (Fin. 97, Z) describes a spiral curve round the oesophagus so that the bifurcated

FIG. 97.———Porti0ns oi‘ l.l‘{Ll1SV8I'S0 sections through :1 Lepiulosiren larva (stage 34) to illustrate the eli:u1gin;_:' relations of lung to gut from at short distance behind the glottis l2tliW:ll'1lH. In .\ l.h«- lung is ventral to the :Llirn(-.ntary canal _; in B it is directly to the riglit ; in (3 it has lm_-mm: displaced dorsally ; while in D (where it is commencing to bifurcate) it has come to he llll(l-(iflrfial in position.

.4, aorti; gt, glomerulus ot'pron«_-phros; I, lung; N, notochord; ues, oesophagus.

hinder end of the rudiment, which will give rise to the lungs in the restricted sense, comes to lie dorsal to the alimentary canal. ~ The lungs continue their tailward growth in the substance of the 172. EMBRYOL()GrY OF THE LOWER VERTEBRATES OH.

dorsal mcsentery (Fig. 97, 1)) but eventually the portion of this mesentery containing the lung and dorsal to it becomes greatly thickened from side to side and finally merges completely in the roof of the splanchnocoele, so that in the adult condition the lungs lie completely outside the body-cavity——between it and the vertebral column.

In Uemtodus (Gregg Wilson, 1901; N cumayr, 1904) the lung is at first, as in the other two lung—fishes, ventral in position (Fig. 94, B) but in this case the originally left lung, which in Lepidostrevz, and I’7"utopte'rus is for a time during development reduced in size, seems to have disappeared almost entirely, being represented only by'a small and transient rudiment. Further detailed studies of the early stages in the development of the lung of Uemtoclus are much needed to make clear the origin and fate of this vestigial left lung. But it seems clear from what is already known that the monopncumatic condition of Ceratndlzzis has come about in evolution through the suppression of the originally left lung.

As the lung completes its development, its cavity becomes encroachcd upon by two median longitudinal ridge-like ingrowths, one dorsal and the other ventral. It used to be supposed that these marked an incipient division of the l11ng into a right and a left half so as to bring about the condition seen in Leptdostren or Protopter-as —the monopneumatic condition being supposed to be the more nearly primitive. It will have been gathered from what has been said that this point of view is no longer tenable and that the n1onopneumatic condition of Cemtoalus is to he looked on as secondary and not primary.

CROSSOPTERYGIANS. — Of the two surviving examples of the Crossopterygian ganoids—the most archaic existing members of the Ganoid-Teleostean stem—a few stages in the development of the lung have been investigated in Poly/pterras (Graham Kerr, 1907). In the earliest stage observed the lung—rudi1nent was in the form of a midventral groove formed by an outgrowth of the pharyngeal lining (Fig. 94, A, Z). This groove becomes deeper and towards its posterior end widens out ventrally so as to have a .L-shape in transverse section.

Posteriorly the lung-rudiment grows back into a pair of horn-like projections——the rudiments of the right and left lung. These extend backwards in the connective tissue of the splanchnopleure and they very soon show a marked inequality in their rate of growth the left lagging behind the right. As growth goes on this inequality becomes more and more marked, so that in a larva of about 30 mm. in length the right‘ lung extended right back to the cloaca while the left projected back only about 3 mm. behind the glottis.

In these later stages another important feature is to be noticed, one which is correlated with the fact that the air-filled lung necessarily acts as a float in an aquatic animal. This feature is that the lung tends to assume a position symmetrical about the median plane. Thus in the anterior region where both lungs are present they are m AIR-BLADDER 173 ,

situated laterally, balancing one another, while farther back where only the right lung is present this shifts towards the mesial plane until it is symmetrical about that plane, lying in the dorsal mesentery (Fig. 98, A and B).

EVOLUTION on THE Am-BLADDER.-—-'l‘he facts that have been enunciated above, with regard to the development of the lung in Dipnoan and Crossopterygian fishes, are of much morphological interest. When pieced together with what has been said regarding the development of the air-bladder of Teleostcan fishes they afford data from which the evolutionary history of the Teleostean airbladder can be traced out with a high degree of probability. That history may be stated in a few words to have probably been as follows:

1. The primitive condition was that of a lung, communieating with the pharynx by a ven- ' trally placed glottis ——-for we have seen that the‘ embryonic rudiment of the organ in the most archaic forms possessing it is a typical lun,r_f-rudiment.

2. The organ became bilobed, growing back into a

right‘, lung and a, left FIG. 98.-—S_ections through the lungs of a larva of hula. Polypterus 30 mm. in length. ,__,.

'3_ In the for-Ins 1 f1:,1lnO!'O1l;llbeI'€0I‘l; Ba more postplrior; 1.4, aorta; mg, enteron ;i Ll, . . e ung; no 00101‘ ' opn Opls xonvp nos: 1». 1-, pm monary ve us; Wh]-ch took to 3' rnl, right lurig; 1:, lntcrrenal vein.

purely swimming

existence, and became specialized in the direction of adaptation to this, l)l]_(_‘.1‘(‘. ('..'Hn(__‘. about an asymmetry of the lungs, the right lung increasing and the left lung diminishing. Why this should have happened is not yet absolutely certain: it may probably have been in adaptation to active movements of ‘lateral flexure, for we see the same thing taking place in Grymnophiona, Snakes and Snu.l<o—like Lizards. That it has been the right rather than the left lung which has increased in size, is probably correlated with the rotation of this region of the alimentary canal in a counter-clockwise direction as seen from behind (seep. 168) which would tend to interfere more with the circulation through the left lung than with that through the right, by lengthening the course of the left pulmonary artery. Steps 174 EMBRYOLOGY OF THE LOWER VERTEBRATES GIL

in the development of this asymmetry are seen in Poly/ptems and in the Lung-fislics.

4. In purely aquatic creatures the dictates of adaptation would naturally cause the air-filled lung to assume a dorsal position. An initial phase of this is repeated in Polyptems where the right lung has become dorsal and median in its hinder portion. In the Lungfishes a further step is takcn—--the whole of the lung becoming dorsal except the pneumatic duct which still remains to mark out the path by which the lung moved dorsalwards round the right side of the alimentary canal.

That the movement dorsalwards was round the right side was no doubt due to the right lung being predominant and the left reduced in size. In the case of Oezatodus the predominance of the original right lung has been retained, the other being completely obsolete except for a short period during development. In Lepidosvlzen and Protopterzzs, on the other hand, the lopsidedness disappears, the original left lung regaining during ontogeny its primitive equality in size with its follow.

5. In the Actinopterygians——those fishes which show the highest degree of evolution in adaptation to a swimming mode of 1ife———the lung has in the course of its evolution passed through similar stages to those exemplified by Poly/pterus and Oeratodus. Here again only the original right lung persists as the air-bladder, the vestige of the left lung being possibly represented by the little diverticulum found by Moser upon the pneumatic duct in early stages of development} In the Actinopterygians a further step onwards has been made in that the glottis has assumed a dorsal position. This is fully explicable by the rotation which this part of the gut has undergone, aided no doubt by the principle of economy of tissue which would tend to bring about a shortening of the unnecessarily long pneumatic duct. In some cases there still persist vestiges of the ancient cellular respiratory lining of the swim-bladder (ag. LeZn'asz'na, Ezytlmnas).

6. Finally in the Physoclistic forms-——the most highly specialized of all-—the swim-bladder has become completely isolated from the gut, its respiratory function has gone and it subserves a mainly hydro static function. The outline given above represents a scheme of evolution which

in the light of modern research has a high degree of probability. Of course as in all such evolutionary speculations there exist details which are still difficult to explain. While most of the facts of comparative anatomy fit in well with it, some do not——such as, for example, the nerve-supply and the blood-supply of the air-bladder of Am1Ia——-but it may be anticipated with considerable confidence that these difficulties will be lessened or disappear with the progress of

research. ' See p. 168. This matter affords an interesting subject for further research. III . THY R0 ID 17_5


THYROID.——The Thyroid gland arises as a mid-ventral outgrowth of the pharyngeal or buccal floor about the level of the Hyoid

FIG. 99.—Sagitta1 set-.t..i0ns through :mturior portion of :llilllI.‘Hl:U'_\' Uttlllll of l.¢jlm'do.w'n-1 illustrating the (l(‘.\'L‘l()plll('.lli- of the 'l‘hyroi«1.

A, I}, C from specinuyns of sttlgn 30; I), :-'et.‘l;.,'- 3| ; 'I‘h, thyroid: I, t.on:.rn¢-_

arch. In those Vertebrates in which the pharyngeal rudiment is solid at this stage the thyroid outgrowth is also solid at its first appearance (Fig. 99, A, T/2,) and develops its cavity secondarily by eytolysis. 176 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

The Thyroid becomes gradually constricted off from the pharynx (Fig. 99, B and C) remaining for a time connected by a narrow stalk or duct with the pharyngeal or rather buecal floor just in front of the primary tongue (see Fig. 82, p. 149). This stalk of attachment becomes nipped across and the thyroid forms a mass (Fig. 99, D) or vesicle rounded in form or somewhat elongated in an antero-posterior direction lying in the mid-ventral line beneath the pharynx and just in front of the ventral aorta.

The originally simple vesicle undergoes a process of sprouting and division by which it becomes converted into a mass of rounded vesicles, each possessing a wall composed of a single layer of cubical epithelial cells and separated from its neighbours by highly vascular mesenchyme which penetrates in between the vesicles to form the stroma of the organ.

During later development the Thyroid undergoes characteristic changes of form in different subdivisions of the Vertebrata. Thus in Teleosts it frequently assumes a more or less diffuse character, the follicles being distributed in the neighbourhood of the ventral aorta and roots of the aifcrent branchial vessels. In the Amphibia and Amniota the organ becomes deeply constricted into two laterally placed lobes which may remain connected or may become separated, so that it assumes a paired character as happens in Amphibians

and Birds. With the processes of differential growth involved in the develop ment of the neck, the thyroid may undergo considerable displacement from its point of origin. Thus in adult Lizards it lies across the trachea well forwards from its hind end while in other reptiles and in birds it lies farther back close to the roots of the great arteries.

It is now generally accepted that the clue to the _phylogenetic history of the Thyroid is afforded by its development in Petromyzon (W. Muller, 1871). Here there develops a mid-ventral outgrowth of the pharyngeal floor, forming a short gutter in the branchial region, the lining of Which is composed partly of glandular cells which secrete a sticky mucus and partly of cells which bear powerful flagella. Morphologically this gutter is the same as the endostyle of Ampkiowus and during larval life its function is also similar: it appears to be in fact simply a shortened up endostyle. The slit-like pharyngeal opening becomes gradually reduced in length till it forms

merely a small pore. _ At the time of metamorphosis the pore becomes obliterated so

that the organ becomes a closed vesicle underlying the pharynx. This vesicle divides up into a number of small vesicles and its mucous secretion accumulates in their interior as a colloid substance like that of the Thyroid vesicles of the Grnathostomata. In a word, the endostyle of the Ammocoetes stage becomes the Thyroid of the adult, and there seems no reason to dpubt that the same has happened in phylogeny and that the thyroid of the Vertebrate is 111 BRANCHIAL BU DS 177

simply the modern representative of the endostyle of the protochordate ancestor.

An interesting feature is that while the physiological importance of the thyroid in the modern Vertebrate is that of a ductless gland for the production of internal secretion to be absorbed by the blood, it still goes on producing the mucous material used by the far back protochordate ancestor for entangling food particles, though that substance is no longer, owing to the disappearance of the duct, discharged into the pharyngeal cavity.

BRANCIIIAL BUDs.——There make their appearance in the develop ing Vertebrate a series of bud-like proliferations of the endodermal epithelium of -the branchial clefts which may be known as branchial buds. They appear at the upper and lower angles of the clefts and the series shows its fullest development in the Lampreys, where buds develop at the dorsal and ventral angles of all the clefts. In the majority of fishes investigated they have been found to appear at the dorsal angles of all the clefts eficept the first; in Urodele Amphibians at the dorsal angle of . clefts and at the ventral angle of II., III. and IV.; in Anura at the dorsal ends of I. and II. and at the ventral ends of ll.-V.; in Lacerta at the dorsal ends of I.-III. and the ventral ends of III. and IV.; in Gallus at dorsal and ventral ends of III. and IV.

The morphological significance of these organs is still completely obscure. Physiologically some of them appear to be of importance during the later stages of development preceding sexual maturity inasmuch as they give rise to that often bulky organ the Thymus. This arises by the fusion together of more or fewer of the dorsal buds, the others undergoing no further development. Thus in Lepvldosvlren (Bryce, 1906) dorsal buds III. and IV. develop into thymus while II. and V. undergo no further development: in Oeratodus (Grreil, 1913) II., III. and IV. give rise to Thymus while V. and VI. do not develop further: in H3/pogeopltds II., III., IV. and V. give rise to Thymus while rudiments on I. and VI. atrophy.

In regard to the much discussed histogenesis of the thymus all that need be said here is that the originally solid epithelial rudiment becomes in -the course of development loosened out into a sparse reticulum interpenetrated by mesenchyme richly traversed by bloodvessels and crowded with leucocytes.

The ventral buds, where they occur, become constricted off from the branchial epithelium forming simple rounded masses of epithelial cells (Amphibians) or they may be subdivided up by intrusive connective tissue into solid portions (Reptiles) or hollow vesicles (Birds). The small organs so formed are termed by their discoverer Maurer epithelial bodies: their physiological significance is quite unknown.

There normally develops in the Vertebrate either on both sides or only on the left side a small pouch-like diverticulum of the pharyngeal wall close to the ventral edge of the last gill cleft, whatever the number of this be in the morphological series. The


divert culum becomes" separated from the pharynx and commonly gives 'se to numerous rounded vesicles somewhat resembling those of the yroid in appearance. The organ thus formed was named by van Be melen who discovered it in Elasmobranchs--—suprapericardial body—— iile Maurer has termed it the postbranchial body. Nothing is delini ely known regarding either its function or its evolutionary history, though it is someti.mes regarded as representing a vestigial last gill—pouch. A curious point is the tendency of the organ to unilateral development it makes its appearance only upon the left side in a large number of cases (Aca.nthz'as, Lepidosirevz and 1’7‘0t0pz1e'ms——-see Fig. 109, B-—most Urodeles, some Lizards).

CEMENT ()1z.m\Ns or 'J;m.sosroMA'i'oUs FlSHES.———-It has long been _

FIG. l00.—— Ventral views of Polyptcrus larva to show the cement-organs. A, Stage 80; B, Stage 33; c.o, cement-org:-m ; «.71, olfactory ox-gun; m, mouth ; V, ventric-le of heart.

known that the larvae of Actinopterygian ganoids possess cementorgaus on the head in front of the mouth. Balfour (1881) wrote of this as “ a very primitive Vertebrate organ, which has disappeared in the adult state of almost all the Vertebrata; but it is probable that further investigations will show that the Teleostei, and especially the Siluroids, are not without traces of a similar structure.”

The organs in question were generally regarded as being developed from a thickening of the ectoderm. Miss Phelps (1899) lirst stated that they originated from endoderm (Amie) and the present writer, at the time ignorant of her work, was greatly surprised to find himself forced to this same conclusion by the examination of I'5udgett’s material of Poly/pterrus.

The cement-organ of Poly/pterus (Graham Kerr, 1906 and 1907.), when at the height of its development,_ forms a stout cylindrical structure with a deep hollow at its free end, projecting from the 188 EMBRYOLOGY OF THE‘ LOWER VERTEBRATES

FIG. 108. Illustrating early development of the liver in Birds. A, 47-hour chick; B, 52-hour chick; C, 50-hour chick (after Brouha, 1898); D, fourth-day chick; E, 7 mm. embryo of the Roseate Tern--Sterne paradi.«n'aca.-(after

Hammer, 1807). M 1, rudiment of anterior (“1eft") bile CH.

portion of the rudiment. The gall bladder originates as a bulging of the floor of the bile-duct towards its anterior end. A The formation of the posterior and longer section of the bile-duct, Which will be extrahepatic in the adult, lagsin its development behind the anterior portions of the rudiment. Such differences in the time of appearance of different parts of the hepatic apparatus——1iver, gall-bladder, bile-duct—-—are to be looked on as mere secondary modifications of development,——the

primitive condition being that i

of a simple pocket of the gutwall such as persists in Am’phioasus.

SAUROPSIDA.-—-The hepatic apparatus here again makes its appearance as a longitudinally situated pocket of the morphologically ventral Wall of the gut. In birds this is situated at first on the anterior wall of the yolk—stalk (Fig. 108, A). The diverticulum grows actively into an anterior (dorsal) and a posterior (ventral) pocket (Fig. 108, C, Z73. 1 and Z7}. 2) while the intervening portion becomes flattened out and incorporated in the gut-wall.

There thus come to be two distinct liver-rudiments an anterior and a posterior. Of these each sprouts out at its end into irregular projections which eventually fuse and form a spongy mass, surrounding the cavity of the ductus

duct; bd°. posterior (“risht") bile-duct; ent, cavity or venosus, and havingin its

fore-gut; gb, rudiment of gall-bladder; la‘. 1 and 2, anterior and posterior liver - rudiments; pa.‘n,\ dorsal rudiment of pancreas.

meshes blood-spaces which 180 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

The first rudiment oi’ the organ is seen to bee simple pocket-like outgrowth of the gut-wall (A, c.o): this becomes more and more prominent (B, C): it becomes gradually constricted oh" at its base from the gut-Wall, its cavity becoming isolated first Finally it separates completely from the main endoclerm and its outer end undergoes fusion with the deep layer of the ectoderm. lts cavity then opens to the exterior and the fully functional condition is reached——the endodermal origin of the secretory lining being for a time betrayed by the conspicuous persistent yolk granules in its cells.

It will be noted that the exposed side of the secretory epithelium, that on which the secretion is extruded, is that which originally faced inwards towards the lumen of the alimentary canal. In other words the direction in which the extrusion takes place is morphologically the same as that of any other part of the glandular lining of the gut-wall.

As is the case in other forms the cement—org-an is a transient, purely larval, structure. About stage 31 (Fig. 197, D) degeneration commences: the gland shrivels up, the gland-cells becoming more slender and dark pigment making its appearance in their interior, the epithelium becomes penetrated by ingrowing blood-vessels, its cell-boundaries become indistinct. The process of atrophy goes on rapidly and by stage 36 (Fig. 197, F) the organ has completely disappeared.

An interesting variation from the normal course of development is found in specimens in which the cement-organ rudiments are more or less approximated to one another. This variation reaches its maximum in occasional individuals in which they are completely fused and form an unpaired structure, continuous across the mesial


P In the actinopterygian Ganoids the cement—organ develops along the same general lines as those just indicated. In the Sturgeons the development has been worked out recently by Sawadsky (1911) in Acipenser ruthenus. Here the organ forms a rounded projection, very much in the same position as that of Polypterus, but in this case each becomes divided by a groove so as to form two rounded knobs. These knobs eventually grow out to form the tactile barbels of the adult, the secretory epithelium being carried out on the surface of the barbel as it grows.

The secretory epithelium is here also endodermal, its rudiment being the gut-wall immediately dorsal to the position in which the mouth will develop later and being continuous across the mesial plane. The unpaired condition which occurs in Polypterus as a variation is thus normal in the case of the sturgeon. As the head increases in length the secretory epithelium becomes carried out on its ventral surface, looking just as if it were the thickened ectoderm of this surface. Finally the paired condition comes about, ‘the lateral

parts of the secretory epithelium coming. to be supported by the knob-like projections already mentioned. III CEMENT-ORGANS 181

Am/ia is of special interest in regard to its cement-organs as it was in this form that their endodermal origin was first announced.‘ The organs are for a time in the form of a pair of rounded knobs, one on each side, but these take on a crescentic shape so that together they form a circular wall, interrupted anteriorly and posteriorly. Each organ contains a pocket-like projection of the gut—wall which takes on a somewhat sausage-like form in correlation with the curved shape of the organ as a whole. This endodermal sac separates from the main endoderm and becomes constricted across, so as to form°a curved row of closed vesicles from six to ten in number. Each vesicle fuses with the ectoderm and develops an opening to the exterior so that it takes on the appearance of a cup at first deep and narrow, later shallow and wider, its lining continuous with the deep layer of the ectoderm.

When the larva reaches a length of 13-14 mm. it makes less use of its cement-organ and the latter commences to degenerate, sinking beneath the surface with which, however, it remains connected by a narrow tubular channel. By about the 20 mm. stage this has disappeared and soon there is no trace of the organ to be found even in sections.

In Lepidosteus the organ appears to be similar while in the other ganoids its development still remains to be worked out.

These cement-organs are of special interest and importance for more than one reason. In the first place they are of importance in revealing a quite unexpected pitfall in the way of the investigator trained to have implicit faith in the germ-layer theory, for they show how a particular organ may become transferred from one g'erm—layer to another even though not belonging to the transitional zone where the two layers are continuous. A very common modification of ontogenetic development consists in the slurring over or even omission of particular stages in early development. Were this to happen in the case of the early stages in the development of the cement—organ say of Polypterus, it is easy to see that the organ might have every appearance of being purely ectodermal in its nature, although it is, as a matter of fact, endodermal.

It appears to the present writer quite possible, if not probable, that this modification has actually come about in the Dipnoi and Amphibians, and that the cement-organs of these groups, although they develop from the ectoderm in those forms which have been investigated (p. 79), are really homologous with the cement-organs of the Teleostomi, their cndodermal stage having been eliminated from ontogenetic development. Further investigations are needed in the Amphibia——to see whether no trace exists, in any member of the group, of an original connexion with the endoderm.

As regards the original nature of these organs it is impossible to arrive at any certain conclusion. Arising as they do in the form

‘ Phelps (1899). The actual discovery seems to have been made by Rcighard. Cf. Reighard and Phelps (1908). 182 EMBRYOLOGY OF THE LOWER VERTEBRATES 011.

of endodermal pockets, they obviously recall gill pouches on the one hand and coelenteric pouches on the other. Their position suggests a pair of preniandibular gill pouches: their function, that of forming an excretion (cement), perhaps indicates rather coelomic afiinities and the present writer suggested (1906) their possible correspondenee with premandibular head cavities of other Vertebrates. Reighard and Phelps (1908) hornologize them wi th the anterior pair of head-cavities of Elasmobranchs while van Wijhc (1914) sup

l+‘m. I02. -Larva of Sa'rr_'.('u_l¢I..r_t(?s amlon. (After Budgett, 1901.) P‘-’I't3 3' homology With"

the ciliated organ of Amphiowus.

Altogether these cement-organs are very interesting and puzzling structures and would well repay further investigation. A thorough comparative study should be made of their development in the archaic Crossopterygians and of their possible homologues in Elasmobranehs.

Little is known regarding cement-organs in Teleosts, though it is proliable they will be found to occur in various tropical freshwater fishes. Budgett ' s (1901) found a large P, _ cement-organ on the he . I « , head of the larva of the '1 /if/“‘jX~” Characinid Sarcodaces odéie (Fig. 102, 0.0). Ina A 0 / ( larva believed to be that 9 ' of the Mormyrid IIype7°o- lg J

«an, or-ment-organ.

pisus babe he found six ’ ‘( Well-marked cement 6. glands on the head which 1 . in this case secrete fine " U threads by which the

larva hangs suspended ' ' F 1' 103 ——Teleostean l as in“ )()‘8l to be those of in the water until the "' p " s ““’*°' *1’! ~“ ’_

lk . _ _ _ ,. II;/_,;er0pos1ts bebe, suspended from the rootlets 111 the

18 H11_St‘3d t1_1P (15 1gd' nest. (From Budgett, 190].) . 8 670 18 3.11

Gymnarclms also possess similar organs—-very small in the latter case 0

(Assheton, 1907).

The organs in these various fishes present, the appearance of being ectodermal thickenings: we have as yet no information as to whether, as may be suspected, they really originate from the endoderm.

DIGESTIVE TRACT. —- The respiratory region of the alimentary canal is succeeded by the true digestive _.tract and this shows more or less pronounced differentiation into successive portions-

oesophagus, stomach, intestine and its subdivisions, cloaca. In correlation with the digestive and assiniilative function of the intestinal endoderm this serves during early stages as the favourite storehouse of food-yolk, and the concentration of yolk in the abapical portion of the unsegmented egg is to be looked on as a foreshadowing of the fact that this portion of the egg will later become the endoderm. .

In the holoblastic Vertebrates the mass of heavily yolked endoderm cells becomes, as it were, modelled into a tubular shape by the

Fnz. 104. ----Illustrating the modelling of the yolk in .I¢.-/4././¢_:/u/;/u'.s-. (After Sarasins, 1889.)

A and B illnslmlu the sauna st::;.:«-, 13 representing a view from the-. dorsal side. The small—celle«.l epithelial port.-inn or the g-nt.-\m,ll is seen passing down the centre of l"i_«_;. ll. (3, I). and }*3r'np1"t-sent later stages «h-awn from the ventral side; F (7 cm. embryo) vent:-o-lateral view frmn the right side.

reciprocal activity of endoderm and splanchnie mesodermg the rudiment so formed undergoing active growth in length and differentiation of structure while the yolk is being assimilated.

In the two most archaic groups of holoblastic gnathostomes, the Crossclptm-ygians and the Lung-fishes, a feature of special interest is the development of the spiral valve. In Lepiciosiren, as is indicated by Figs. 105 and 106, this takes its origin by the solid mass of yolk-laden endoderm l)(‘('_fi(‘)llllllg modelled into a right-handed spiral coil——the deep incision xvhich separates successive turns of the spiral being filled up by ingrowing mesenchyme belonging to the splanclmic mesmlerni. There can be little doubt that this is a secondarily Il'l()(l.lllt__*.(l. mode of development, but nevertheless it is probable that the spiral coiling of the endodermal rudiment is to be explained as a repetition of_ an ancestral condition in which the intestine as a whole was long and spirally coiled.

An important feature of such a spiral coiling of the gut rudiment is that it would necessarily tend to bring about a twisting of the

Flu. 105.~--l')issm-t.ion.s- of young In-1)i<lo.<in-..ns of stages 32 (A), 35 (B), 36 (C), and 37 (D), lmm I.lu_: vi-ntral side to show the modelling of the intestine.

g.b, gall-l')la_(lder; Ii, liver;

alimentary canal just in front of the spirally coiled portion in a counter-clockwise direction as seen from behind, vie. a movement in which points on the ventral side of the alimentary canal would become shifted towards the 1-iglit side. A_s.a]ready indicated such a twisting of this region of the alimentary canal actually does take place in development causing the lung rudiment to shift dorsally round the right side of the alimentary canal.

In the more richly yolked Vertebrates the Ventral ‘[N)1'lJl('lllS of the gut-Wall are more and more clogged up with yolk and this results in a greater and greater concentration of developmental activity in the dorsal wall. This is clearly indicated by transverse sections through the developing gut of Vertebrates wl1i_ch though rich in yolk are still holoblastic. Such sections (Fig. 107) show the dorsal wall of the gut to consist of small active cells arranged as a columnar epithelium, while the side walls and floor consist of large coinparatively inert yolk -laden elements. It is only as development goes on, and as the yolk is consumed, that the epithelial small-celled character gradually spreads ventrally.

In the actually meroblastic Vertebrates, the heavily yolked portions of the primitive gutwall never undergo segmentation at all, unless possibly as regards a thin superficial layer. They remain as a continuous mass of yolk, round which the epithelium gradually spreads. In this case the formation of all the important organs of the alimentary canal is concentrated in the dorsal. portion which heeomes gradually folded off from the main mass of the yolk. This folding-off process takes place most actively in the anterior region, so as to form the tubular l'ore- gut, and also posteriorly, the intermediate portion remaining for a time as a longitudinal groove opening ventrally towards the yolk. As the lips of this groove‘ gradually coalesce at each end the communication between the gut cavity and the,yolk becomes gradually narrowed down to the tubular cavity of the yolkstalk situated at first behind the liver but later becoming shifted forwards by differential growth. Eventually this becomes obliterated and the definitive alimentary canal becomes completely isolated from what remains of the yolk. In many Telcostean fishes this isolation takes place at a very early stage in development. . _ _ The alimentary canal is, in correlation with its dlgestive function, necessarily a highly glandular organ. Primitively the secretory functions are carried out by unicellular glands, scattered about amongst the other epithelial cells of the endoderm, but in the Vertebrates, as in all the more complex Metazoa, special concentrations of gland cells and of secretory activity take place in localized portions of the enteric wall. Each of these specially glandular patches undergoes a great increase in its area, which causes it to bulge outwards as a simple or much subdivided Fro. l07.—'l.‘ransverse section through bind and complicated pocket’s forming

FIG. 106.—Dissection of Lepidosiren larva of stage 35.

t.o, tectum o1m2cunz.. pm, pronephros oc.r, occipital rib

u 1

o. c, auditory capsule Ii, liver l, lung ht, heart h, hemisphere

portion of intestine of a larva of Ich- flu CllSl':lIlCl: glandular appendage Of

thytlfih-1:8. (After Sarasins, 'l‘he the alimentary canal_ stage of development was that shown in

Fig, 104, F. ' The sheath of splanchnic LIVER‘ _"_Of these 81a’I?d“1‘“' megodgrm is omit,ted_ appendages, 1n the (3359 _Of Verte brates, the most ancient appears to be the liver, which is already present in Amp}:/ioasus. In this animal the liver originates in ontogeny (Hammar, 1893) as a pocket-like outgrowth of the alimentary canal wall on its ventral side and slightly posterior to the hind end of the pharynx. Apart from increase in size and relative narrowing of its base of attachment the liver in Amphiomus undergoes no further complication but retains its extraordinarily primitive pouch-like condition throughout life.

In the holoblastic Craniates the liver arises similarly as a ventral projection of the alimentary canal wall. This shows the customary modifications in correlation with the presence of yolk, arising in some cases in the more primitive fashion as a hollow pocket (Lampreys, many Amphibians, Cemtodus), in others (many Amphibians, Lep1Sdosiiren and I’-rotopterms) as a solid knob of yolk-laden cells (Fig. 105, Z73). This grows rapidly in size, as it uses up its food-yolk, and becomes constricted off from the main mass of yolk by ingrowing mesenchyme, until its attachment becomes narrowed down to a slender stalk-—-the rudiment of the bile-duct.

The pouch-like rudiment of the liver undergoes an active process of sprouting into numerous secondary pockets, each of which becomes greatly elongated and branched, and gives the gland a tubular character. This character may be retained throughout life (Lampreys) but normally the tubules undergo anastomosis so as to form a network of trabeculae. While this is to be regarded as the primitive mode of development of the tubules it is to be noted that they more usually in actual fact show the modification of development which we have learned to associate with the presence of yolk, being at first solid and taking their origin not by a process of outgrowth but rather by a process of modelling by ingrowing mesenchyme.

In the meroblastic Vertebrates also the liver may be described as originating from a mid-ventral outpushing of the enteric wall. Variations occur in detail, in correlation with the varying relations of the hepatic portion of enteric wall to the fore-gut and yolk-sac. If this part of the gut-wall has already been folded off from the yolk-sac and incorporated in the fore-gut, then the early stages of development of the liver divertieulum pursue their normal course. If, on the other hand, it still forms part of the yolk-sac wall, the hepatic rudiment makes its appearance as a projection from this, and it may be in its first beginnings paired, its two halves separated by the longitudinal slit by which the cavities of the definitive gut and the yolk-sac are still continuous.

ELASMOBRANCHII.——The hepatic divertieulum at an early stage bulges out to form a conspicuous outgrowth on each side anteriorly ——the rudiments of the right and left lobes of the liver. The median portion between these becomes in its anterior region converted into secretory tissue while its posterior part becomes the bile-duet, with its dilatation the gall-bladder.

In Acanthzas (Scammon, 1913) the first rudiment of the liver, which makes its appearance at a time when this region of the enteron is not yet floored in but opens freely into the subjacent yolk-sac, is distinctly paired. In view of the unpaired condition in Amplmloxus and the holoblastic Craniates there can be little doubt that this condition in Acanthvlas is a secondary modification as indicated above. Secondary pockets soon make their appearance on the wall of the secretory portion of the rudiment, and grow actively into elongated and much-branched tubules. These fuse together secondarily to form the network characteristic of the fully developed liver. This network is bathed by the blood of the vitelline veins (see Chap. VI.).

After the embryo (Acamthias) has reached a length of 25-28 mm. the walls of the tubules, or trabeculae of the network,increase greatly in thickness so that both their own cavities and the intervening blood-spaces become relatively reduced and the organ assumes the compact definitive condition.

Whereas the tubules become throughout the greater part of their extent secretory in function the proximal portions, each common to a group of tubular branches, functionmerelyas ducts. These communicate with the main bile-duct formed from the posterior and median of the genital portion of the peritoneal epithelium with the peritoneal funnels, or with the nephrostomes, were in the form of open ciliatecl grooves or gutters on the surface of the peritoneum, that later on these became closed in to form tubular channels, and that in actual ontogenetic development in the modern amphibia the development from the coelomic epithelium has become obscured except for traces now at one end now at the other.

At their distal ends the cell-strands in the male can be traced gradually farther and farther into the genital fold until they come into immediate relationship with the cell-nests of gonocytes. In the female of Urodela and Anura the strands do not spread so far into the genital fold, nor are they, even in early stages, so well developed as in the male.

The fatty body is developmentally simply a portion of the genital fold which becomes specialized as a store-house of fat. In

Anura it is the progonal portion which undergoes this differentiation

while in Urodeles and Gymnophiona the rudiment of the fatty body is continued backwards as a ridge along the mesial face of the genital fold throughout its extent.

The fat is stored in the connective tissue of the organ, the fat cells being usually interpreted as immigrant mesenchyme cells which have invaded the rudiment by its base of attachment. It has also been suggested that these fat cells are peritoneal in their origin (Abramowicz, 1913)——a suggestion of obvious interest in view of the general tendency in the animal kingdom for potential germ~cells to undergo degeneration in order to provide nourishment for the germcells which become functional.


The development of the functional testis out of the genital fold is seen in peculiarly simple and diagrammatic form in the Gymnophiona. Here the strands of the urinogenital network, as they sprout into the interior of the testis, anastomose together along its axis so as to form a central canal——around which, embedded in the stroma of the organ, lie the rounded nests of gonocytes. Fusion takes place between each gonocyte-nest and the wall of the central canal and then each nest develops a cavity in its own interior and becomes a hollow ampulla opening into the canal at its inner end.

Various modifications of this simple scheme are to be found. In Grymnophiona themsel.ves ampulla—formation becomes suppressed except in localized regions between successive vasa etferentia, so that intervening portions of the testis are sterile and form merely thin tubular eonnexions between the bead-like fertile portions. Again the ampullae vary in shape: they may be elongated and tubular (Discoglossas) or, as in the majority of cases, flattened against one another by pressure. The “axial” canal again may lie close to the surface: it may become greatly branched, as in most Urodeles, or may form a complicated network as in most Anura.


In the differentiation of the ovary (Bouin, 1901) the most important points to be noted are the following. As regards communicate with the just -mentioned vessel. This spongy mass, the trabeculae of which are at first solid and only secondarily develop a lumen, forms the secretory portion of the liver, while the proximal portions of,the outgrowths persist as the two conspicuous bile-ducts of the adult bird (Fig. 108, D, E, bcl. 1 and M. 2). In such birds as possess a gall-bladder this is formed by a dilatation close to the point of junction of the posterior hile-duct with the gut-wall (Fig. 108, I), E, gb).


The pancreas, though in the adult a single structure, arises typically from three distinct rudiments, each of which is at first a simple pocket-like outgrowth of the splanchnopleure. One of the rudiments (cf. Fig. 80, H) is situated dorsally a little posterior to the stomach, the other two, which appear somewhat later, are ventral and arise as outpushings of the hepatic diverticul11m in the region of the bile-duct. The ventral pancreatic rudiments are commonly paired, arising one on the right and one on the left of the hile~duct.

The three rudiments increase in size, secretory tubules sprout out from them and the two ventral rudiments become carried in a dorsalward direction, up the right side, by the rotation which the gut undergoes in this region (see p. 168). The right ventral rudiment comes in contact with the dorsal rudiment and fusion takes place—all three rudiments forming a single organ the three—1'old origin of which is indicated by its three communications with the alimentary canal.

Such may be considered the typical mode of development of the pancreas, but important variations in detail occur in the different groups. In Cyclostomes and Elasmobranchs only the dorsal pancreas is known to occur. Its development in the former group requires further investigation. In Elasmobranchs it arises as a longitudinal groove of the enteric wall dorsally and a little posterior to the opening of the bile-duct. It becomes constricted off’ from before backwards and in accordance with the rotation of the alimentary canal it becomes shifted to the left side and ends up by being ventral.

In Crossopterygians the three typical rudiments appear (Fig. 80, H) but their development has not been followed in detail. Eventually the pancreatic complex extends forwards beneath the liver and completely fuses with it forming a tlfick layer over its ventral surface in the region near the opening of the bile-duct.

In Actinopterygian Granoids also (Piper, 1902; Nicolas, 1904), the pancreatic complex derived from the original three rudiments becomes fused with the substance of the liver, only its posterior dorsal portion remaining extrahepatic. The main duct of the pancreas is the persistent stalk of the right ventral rudiment which opens into the gall-bladder formed by the dilated terminal part of the bile-duct. Of the two other pancreatic ducts the left ventral apparently atrophies entirely, while the dorsal is said in the case of Am/ia to disappear but in the Sterlet (Acipenser ruthenus) to persist.

In Teleosts the early development agrees closely with that of the ganoids, only a doubt exists whether the definitive pancreatic duct (Duct of Wirsung) may not be formed by a fusion of the two ventral ducts rather than by the persistent right duct alone. During later stages great difl'erenees arise between dilferent members of the group. l n some (Silwrus, Esow) the complex forms a single compact gland, in others (flcomber, U3/_7)7"in'w.<¢) it becomes divided i.nto a number of independent lobes, in others, including the majority of the more familiar Teleosts, it becomes greatly branched and is diffused in the substance of the dorsal mesentery while in still others (Labridae, Syngnr.rt7tus) the condition resembles that of the ganoids a large part

of the organ being intrahepatic (Laguesse, 1894).

FIG. 109.-—-Dorsal View showing l'udiIm:nts of 1 orsal p:nu:reas .-mil luring in l:u'v:1c of Protopterus (stages 32 and 34).

I, lung; op, opercnlum ; pied, dorsal pancreas; p.b, pnstbranchial body; p.f, pectoral limb; rudiment.

In Lung-fishes the three typical rudiments make their appearance. In Protopterus the dorsal rudiment (see Fig. 109, A, pad) is a solid outgrowth (hollow in Lepidosiren) from the gut-wall, usually rounded in form but occasionally elongated in an antero-posterior direction as in the specimen figured (Fig. 109, A). The attachment to the gut becomes rapidly constricted to a narrow stalk and a cavity develops in the interior of the rudiment. The ventral rudiments appear a little later, as solid projections one on each side of the attachment of the bile-duct to the gut. The two ventral rudiments, as they increase in size, meet and fuse dorsal to the bile-duct, and later on the dorsal surface of the right ventral rudiment comes in contact and fuses with the ventral surface of the dorsal rudiment. The stalks of the three rudiments remain as three ducts, the two ventral opening just posterior (original right rudiment) and anterior (original left) respectively to the opening of the bile,-duct, while the dorsal opening is situated at the extremity of the spout-like pyloric valve.

The general course of development in Lepidosiren is similar and in both it is characteristic that the pancreas never bulges beyond the mesodermal coating of the splanchnopleure. It remains embedded throughout life in the gut-wall and is consequently not noticeable in an ordinary dissection.

In Oeratoalus (N eumayr, 1904) the development of the pancreas is similar though here the left ventral rudiment, which in Protoptems is smaller in size than the right, remains rudimentary.

The Amphibia are of special interest from the fact that it was a member of this group (B0m.b7Inat0r) in which Goettc (1875) first observed the origin of the pancreas from three separate rudiments. Groeppert (1891) was able to extend the observation to various other Amphibians, both Urodele and Anuran, and to show that in Urodeles the dorsal rudiment retains its duct, opening just behind the pylorus, while in the Anura this duct disappears. In both cases the ducts of the two ventral rudiments undergo fusion to form a duct of Wirsung which opens into the bile-duct.

In Reptiles (Lace7~ta-—-Brachet, 1896) the right ventral and the dorsal rudiments fuse to form the definitive pancreas, the left ventral atrophying (cf. Lung-fishes). According to Brachet the duct of the dorsal rudiment does not disappear but fuses with that of the right ventral to form the definitive pancreatic duct.

Birds show three rudiments which undergo fusion into a complex in the normal fashion, all three ducts remaining functional and conspicuous in the adult. Suppression of the left ventral rudiment occurs as an occasional variation.

The observed facts of development of the Pancreas clearly justify the conclusion that this organ of the modern Vertebrate has arisen in the course of evolution from three originally separate diverticula of the glandular enteric wall-~—-a pair arising from the hepatic pouch and the third from the dorsal wall. The precise localization of the rudiments at comparatively distant points of the enteric wall point to the probability that the nature of the secretion was originally different in the case of the ventral pancreas from that of the dorsal.

PYLOBIC GAECA.—The caeca which are present in the pyloric region in many actinopterygian fishes arise as simple outgrowths of the gut-wall. The interesting suggestion has been made (Taylor, 1913) that the simple circle of these caeca, which is apparently their most primitive arrangement, corresponds morphologically with the curious valve found in various fishes (Amia, Lung-fishes, Symbmnchus, Anguilla, etc.) in which the pyloric end of the stomach is prolonged back into a kind of spout which is ensheathed by the anterior end of the intestine. The circular prolongation forward of the intestinal cavity round the gastric spout might clearly give rise to a circle of pyloric caeca simply by_ subdivision into a number of separate portions each of which continued to open into the gut cavity at its hinder end.

RECTAL GLAND.——ThlS organ, which occurs in Elasmobranchs, arises as a simple pocket-like outgrowth of the gut-wall. The superficially similar caecum of Lung-fishes will be dealt with in connexion with the renal organs.


In the more archaic Vertebrates the ducts of the excretory organs open into the terminal part of the intestine which is thus a cloaca. It is believed by many that the excretory ducts originally opened at the hind end of the trunk independently of the alimentary canal and it is natural to suppose that the openings of the ducts have become gradually shifted first into close proximity to the aims and finally on to the lining wall of the alimentary canal. This again suggests that the cloaca may really be a proctodaeum—~that the skin has been involuted to form its lining and that with this involution the renal openings have also been carried inwards.

Unfortunately the facts of ontogenetic development do not so far as can be seen at present fit this simple and attractive hypothesis. The cloaca is, except for a small portion close to its opening, of purely endodermal origin——the renal ducts open on what is part of the primary entcric wall. A suggested explanation of this fact dilfering from that mentioned above will be found in the chapter dealing with the renal organs.

A cloaca seems always to be developed though in some cases (e.g. Teleostean fishes) it flattens out and disappears later so that the renal organs and the gut come to have independent external openings.

The bursa Fabricii, a conspicuous glandular appendage of the dorsal Wall of the cloaca in young birds, has usually been regarded as proctodaeal in its origin but it is now known to arise in ontogeny from vacuolar spaces in a solid projection from the cloacal rudiment, dorsal to the stalk of the allantois (Wenckebach, 1888) and would therefore appear to belong to the mesenteron rather than to the proctodaeum.

The anal opening of the Vertebrate, as may have been gathered from Chap. II., is to be regarded as representing morphologically a portion of the gastrular mouth or protostoma. In a large number of Vertebrates however the opening arises in ontogeny not in this way but rather as a secondary perforation, although even in such cases the perforation arises in the line of the closed protostoma.

Temporary Occlusion of the Alimentary Canal

The alimentary canal is, in correlation with its function, a hollow tube. In a large number of Vertebrates, however, there are more or less extended periods of development during which the cavity is completely absent, either throughout the length of the canal or in certain portions.

In its simplest condition this occurs as a special case of the temporary absence of lumen so frequently found in the ndevelopment of eventually hollow organs from a richly yolk-laden rudiment. An idea of how it has come about will be got from an inspection of the various stages of the development of the alimentary canal of Poly/pterus as shown in Fig. 80 on p. 146. During early stages the archenteric cavity is seen to be widely patent throughout, except that there is no mouth opening. During the later stages of development, immcdiately prior to the canal becoming functional, its walls throughout the region between the fore-gut and the cloaea become closely apposed, so as almost entirely to obliterate the cavity. Later on the walls recede from one another and the lumen becomes again patent.

It would obviously be merely a slight accentuation of this modification of development for the cavity to be completely obliterated for a time. A still further modification would be brought about by the omission altogether of the original hollow stage from the ontogenetic record. This actually- occurs in the case of the fore-gut in those Vertebrates in which this region of the enteric rudiment is yolk-laden: where, on the other hand, the yolk is practically completely concentrated in the mid-gut region as in meroblastic Vertebrates it does not occur as a rule.

The most striking temporary occlusions of the alimentary canal during development have to do with its terminal apertures. Thus there is not a single existing Vertebrate, so far as is known, in which the mouth opening persists from the gastrular stage, or in which even any connexion has so far been traced between the definitive mouth opening and the protostoma. In every case, even in A'2n,p/viowus, the mouth opening develops comparatively late as a secondary perforation. This modification of development is in the present writer’s opinion to be attributed to the entire dependence of members of the Vertebrate phylum upon food-yolk during early stages of their development, the need for a functional mouth having thus disappeared.

The anteroposterior extent of this occlusion of the alimentary canal in the region of the oral opening differs in different subdivisions of the phylum. It may include a large part of the stomodaeal as well as the cndodermal portion of the buccal cavity as in the Lung-fishes (p. 148) but more usually it is confined to the boundary between the two, 7§.e. to the site of the original mouth opening the closely apposed ectoderm and endoderm being at this level continuous across the site of the future opening as the velar membrane’ (p. 145). The secondary perforation by which the alimentary canal comes to communicate with the exterior at its front end is in the case of some larval Vertebrates (e.g. Lapidosdren) closely correlated with the commencement of pharyngeal respiration but where the development is embryonic it commonly still takes place long before the.existence of any obvious functional need (ag. Chick, fourth day). At its hinder end the archenteron is, as has been shown in Chap. I., widely open to the exterior in all the lower Vertebrates during early stages and in various cases this opening can be traced either into direct continuity, or into less direct but still clear relationship, with the anal opening. The explanation of this lesser degree of modification of the development of the anal opening as compared with the mouth may probably be associated with the less accentuated delay in the functional need for this opening. At stages long before ingestion or inspiration takes place by the mouth, the formation of waste products during the digestion of the yolk necessitates an outlet from the entcrio canal at its hinder end. Where obliteration does take place during still earlier stages this is probably correlated with the fact that the need of the opening is still non-existent.

It is of interest to notice that obliteration of the anal opening which is of a directly adaptive significance may take place at a later stage. Thus in Lr,p2Talos2Iq°e71. during about the lirst two weeks of larval life, when large numbers of practically motionless larvae are lying crowded together in the nest, the anal opening, which had been continuously patent in earlier stages, is closed, so as to prevent the poisonous excretory products from finding their way out. So also in the case of the Elasmobranch embryo enclosed within its egg-shell. In the Amniota the perforation of the anus is delayed to a relatively late period doubtless for a similar reason.

It is characteristic of the phylum Vertebrata that the anal opening no longer occupies its primitive position at the extreme end of the body but has become shifted forwards along the ventral side. This shifting has probably come about with increased specialization for swimming by lateral flexure of the body, the withdrawal of the alimentary canal with its surrounding splanchnocoelic cavity frrim the hinder portion of the body, leaving the space they occupied free for increased development of the lateral muscles. This shifting forwards of the anus, leading to the differentiation of a distinct postanal or tail region, has occurred in all Vertebrates, least markedly in the more archaic groups. It reaches its maximum in some members of that group of Vertebrates which is above all others highly specialized for active swimming, the Teleostei, in some families of which the anus has actually assumed a jugular position.

During the actual ontogeny of the Vertebrate the process by which the anus comes to occupy a position 1nore or less distant from the tip of the tail region is somewhat modified from that which probably occurred during phyletie evolution. We do not find that the anus remains at the tip of the tail during the growth in length and that it then gradually shifts forwards along the ventral side. What happens is that the opening at an early stage assumes a ventral position and that the tail region proceeds to sprout out dorsal to it. The process will be understood from an inspection of Fig. 80 (p. 146). In B the anus is at the binder end, in Cit has 111 THE ALIMENTARY CANAL 195

assumed a ventral position being overhung by the bulging tail rudiment, in D, E, 14‘, G the tail rudiment is seen to be extending actively past the position of the anus, the specially actively growing tissues being indicated by the darker shading.

In Fig. 80, G, a feature is well shown which occurs in the embryos of most Vertebrates—-—the postanal gut (pay). It was shown in Chap. I. how a connexion - the neurenteric canal - existed in some Vertebrates between the cavity of the enteron and that of the neural rudiment at their posterior ends. Here, in the postanal gut, we have such a connexion still persisting in a drawn-out form though, as in the present case, it may be a solid strand of yolky cells and not a hollow tube. The postanal gut is a purely transitory structure which at a relatively early period of development disintegrates completely.

In endeavouring to determine the morphological significance of the postanal gut it is necessary to bear in mind that the Vertebrate in early stages develops from before backwards and that the growth in length by the addition of new segments takes place at its hinder end where there is a mass of actively growing embryonic tissue forming a kind of “growing point.” The tissue of this, although to the eye quite undifferentiated, contains the elements which form all the various tissues such as nerve cord, notochord, myotomes, alimentary canal, etc. As growth goes on these gradually become differentiated out, the differentiation always proceeding from before backwards. If we now look at such a young Vertebrate as that shown in Fig. 80, Or, we see the typical Vertebrate structure, including alimentary canal (pay) extending right back practically to the tip of the tail: it is only at the extreme tip that the various organs merge together into unditl‘erentiated embryonic tissue. The only striking peculiarity is that the communication of the alimentary canal with the exterior, the anus, is not in the midst of the growing tissue of the tip, as it would be, for example, in a young Chaetopod worm, but well forwards on the ventral side.

This peculiarity, in the writer’s opinion, finds its explanation in the development from before backwards already alluded to. The appearance of the anus at a point relatively far forwards means that it and the organs related to it such as the excretory d11cts complete their development at an earlier period of time. As it is of functional importance that the organs in question should do so, in contradistinction to the purely motor arrangements farther back, we see a physiological reason why evolution should have brought about a development of the anal opening in its anterior position from the beginning, and the elimination of those stages in which it was situated farther back.

As regards the phyletic evolution of this part of the enteron, we may sum up probabilities as follows: that the alimentary canal with its surrounding splanchnocoele originally extended to the hind end of the body: that the anal opening came to be shifted on to the 196 EMBRYOLOGY OF THE LOWER VERTEBRATES III

ventral wall of the canal: tliat; it then underwent; a. gradual shifting forwards a.long the ventral side: that as it did so the now

postanal portion with its sphmchiiocoelc gradually atrophied the position they occupied becoming filled mainly with muscle. '


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Textbook Chapters: 1 Formation of the Germ Layers | 2 Skin and Derivatives | 3 Alimentary Canal | 4 Coelomic Organs | 5 Skeleton | 6 Vascular | 7 Internal Body Features | 8 Adaptation to Environmental Conditions | 9 General Considerations | 10 Common Fowl | 11 Lower Vertebrates | Appendix


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