Contributions to the Development of the Skull in Sturgeons.
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1 Contributions to the Development of the Skull in Sturgeons. By G. R. de Beer, M.A., B.Sc, F.L.S., Fellow of Merton College, Demonstrator in Zoology and Comparative Anatomy, University Museum, Oxford. With 20 Text-figures. 1. INTRODUCTION FIVE-DAY STAGE TEN-AND-A-HALF-DAY STAGE THE RELATIONS OF THE NERVES DISCUSSION SUMMARY LITERATURE CITED INTEODUCTION. WHILE studying two embryos of Acipenser stellata (kindly lent to me by Professor Goodrich) in connexion with a more extensive work of a comparative nature, it appeared to me that some of my observations would be more conveniently dealt with in a separate paper. They are accordingly set forth here. The material consisted of two embryos of the ages of five and ten and a half days. The smaller specimen was reconstructed graphically and the larger one modelled in wax and blotting-paper by the method devised by the Department of Human Anatomy. The work was done in the Department of Zoology and Comparative Anatomy at Oxford.
2 672 G. R. DE BEER TEXT-FIGS. 1 AND 2. olc olc Pig. 1. Reconstruction of embryo of Acipenser stella, five days old, seen from above. Kg. 2. As Text-fig. 1 seen from the left side. The figures 3 to 9 indicate the planes in which the transverse sections (Text-figs. 3 to 9) are taken. EXPLANATION or LETTERING. ah, abducens nerve; ac, auditory capsule; brp, basitrabecular process ; caf, carotid foramen ; cb, ceratobranchial; ch, ceratohyal; csp, craniospinal process ; da, dorsal aorta ; eba 1, 2, efferent branchial artery 1, 2 ; ema, efferent mandibular artery ; / facial nerve ; fin metotic fissure ; gl glossopharyngeal nerve
3 SKULL IN STURGEONS FIVE-DAY STAGE. The chondrocranium at the five-day stage is shown as reconstructed in Text-figs. 1 and 2. Chondrification has already set in to a considerable extent, and since many elements have been fused together it is impossible to say anything as to the actual method of origin of such elements. The relations of certain structures, however, can be made out, some being of considerable interest. The trabeculae are separate anteriorly as shown by transverse sections, Text-figs. 3 and 4, but farther back they aro connected, forming a broad trabecular plate (Text-fig. 5). Posteriorly the trabeculae have fused with the parachordals which form the basal plate on each side of the notochord. The auditory capsules are represented by their ventral and lateral walls and are connected with the basal plate. Just in front of them are the prootic incisures ; behind them tho occipital arches are forming, enclosing the metotic fissure between themselves and the auditory capsule. The occipital branchial; max & hue, combined rami maxillaris trigemini and buccalis faoialis ; me, Meokel's cartilage ; n, notochord ; oa, orbital artery; oc, oculomotor nerve; oca, occipital arcli; oof, oculomotor foramen; of, optic foramen; ole, olfactorycapsule ; olf, olfactory foramen ; ols, olfactory sac ; on, optics nerve; olf, foramen of otic nerve; ov, optic vesicle; pa, pathetic nerve ; paf, pathetic foramen ; pbhm, basal hyomandibular articulation ; pc, parachordal; pohm, otic hyomandibular articulation ; pp, pila prootica ; pphm, posterior otic hyomandibular articulations ; ppg, palatopterygoquadrate ; pr'f, prootic foramen; pv, pituitary vein; pvf, pituitary vein foramen ; rb VII, ramus buccalis faeialis ; rds, rudiment of the dorsum sellae ; rh VII, ramus hyoideus faeialis ; rhm VII, ramus hyomandibularis faeialis ; rm V, ramus mandibularis trigemini; r max V, ramus maxillaris trigemini; ro V, ramus ophthalmicus superficialis trigemini; ro VII, ramus ophthalmicus faeialis ; rot VII, ramus oticus faeialis ; rp VII, ramus palatinus faeialis ; rp IX, ramus pharyngeus glossopharyngei; rpr IX, ramus pretrematicus glossopharyngei; rpt IX, ramus posttrematicus glossopharyngei; s, symplectic ; si, sphenolateral; mil, first spinal nerve ; sp, spiracle ; spv, suprapharyngobranchial ; st, side of canal for hyomandibular nerve, orbital artery, and head-vein ; (, trabecula ; to, teotum occipitale ; tp, trabecular plate ; tr, trigeminal nerve ; Is, tecturn synoticum ; v, vein, part of orbital sinus ; va 1,2, visceral arch 1,2; vd, vena capitis lateralis; vein, vena capitis medialis; vg, vagus nerve; vr, ventral root.
4 674 G. R. DB BEER arches are incomplete dorsally, and in fact there is no roof to the skull anywhere. At the side of the fore-brain, dorsal to the eyes, are the sphenolateral cartilages. At this stage these cartilages are already connected with the rest of the skull. In front they join the olfactory capsules (Text-fig. 3) which is being formed as a lateral extension of a shelf from the trabecula beneath the olfactory sac and a smaller shelf dorsally. The olfactory nerve reaches the brain in front of the cartilage, there being no foramen. Posteriorly the sphenolateral cartilages connect with the point of junction of trabeculae and parachordals by the pila prootica (Text-fig. 5). Through the opening left between the sphenolateral, trabecula, and pila prootica there pass the optic, oculomotor and pathetic nerves, and the pituitary vein, which runs in from the jugular. Behind the pila prootica and in front of the auditory capsule, i.e. through the incisura prootica, the complete trigeminal and facial and the abducens nerves emerge. The internal carotids pierce the trabecular plate by a pair of foramina fairly wide apart, slightly in front of the pila prootica. Stretching inwards from the sphenolateral cartilages, a little in front of the pila prootica, a membrane passes across the skull in the plica encephali ventralis. This membrane is the rudiment of the dorsum sellae. Meanwhile it is important to note that the trabecular plate is continuous with the parachordals without sharp change of level. Slightly behind the incisura prootica a small longitudinal groove forms, between the lateral edge of the basal plate and the auditory capsule. Through this groove the jugular vein, the hyomandibular branch of the facial nerve, and the orbital artery run. The jugular vein is at this stage median to the branches of the trigeminal nerve (and to the buccal and otic branches of the facial), lateral to the palatine and the hyomandibular branches of the facial, lateral to the glossopharyngeal, and median to the vagus (Text-figs. 6, 7, 8, and 9). The two last
5 TEXT-FIGS lmm.. Selected transverse sections through embryo five days old. Fig. 3. Through olfactory organ. Fig. 4. Through optic vesicle. Fig. 5. In front of pila prootica. Fig. 6. Through the trigeminal ganglion. Fig. 7. Through spiracle. Fig. 8. Through glossopharyngeal ganglion. Fig. 9. Through vagus ganglion.
6 676 G. R. DB BEER nerves emerge through the metotic fissure, and just ventral to them there is a ventral root. As regards the visceral skeleton, the palatopterygoquadrate and Meckel's cartilage are formed and suspended by the hyomandibular at a considerable distance from the neurocranium ; Parker (8), indeed, calls attention to the pronounced nature of the hyostyly of these skulls. There is no trace of a basal process, nor of a basitrabecular process such as is found in the further developed stage. The hyomandibular is large and articulates with the auditory capsule lateral to the groove mentioned above. The symplectic is not differentiated. Two visceral arches articulate with the skull, and their articulation at this stage is the one which gives rise to the infrapharyngobranchial of van Wijhe (IS). 3. TEN-AND-A-HALF-DAY STAGE. Drawings of the model reconstructed from sections of the ten-and-a-half-day stage are given in Text-figs. 10 and 11. The chief changes compared with the previous stage are : (i) The completion of the trabecular plate. (ii) The connexion of the pila prootica with the auditory capsule converting the incisura prootica into the foramen prooticum. (iii) The beginning of roofing, which takes place in the region of the auditory capsules and the occipital arch. As a result of the more extensive fusion of the different elements of which the skull is composed, nerves and bloodvessels, which at an earlier stage passed through wide windows or incisures, now pierce small foramina. In front of the pila prootica the optic, oculomotor, and pathetic nerves and the pituitary vein each traverse their own foramen. The trigenu'nal nerves issue with the abducens out of the foramen prooticum behind the pila prootica. The glossopharyngeal and vagus have separate foramina as a result of the metotic fissure becoming subdivided into two. The groove through which the jugular vein, orbital artery,
7 SKULL IN STURGEONS 677 and the hyomandibular branch of the facial nerve pass is now converted into a canal by the lateral extension of the basal plate (Text-fig. 12). This corresponds with the pars jugularis of the trigeminofacial chamber (Allis). Further discussion of this is reserved for a later paper. The olfactory nerve now pierces a foramen in the olfactory TEXT-PIG. 10. Drawing of a model reconstructed in wax of an embryo, ten and a half days old, seen from the left side. capsule, showing that the skull has extended forwards considerably since the last stage and now forms a rostrum. A little in front of the pila prootica there is on each side a process extending latero-ventrally from the trabecula (Text-fig. 13). Proximally this process is cartilaginous, but at the tip it shades off into dense fibrous connective tissue which can be traced to the connective tissue surrounding the palatopterygoquadrate. It is the processus palatobasalis lateralis cranii of Sewertzoff (10).
8 678 G. R. DE BEER The relations of this process are of interest. It lies lateral and dorsal to the ramus palatinus facialis and in front of the TEXT-FIG. 11. olc- hm- As Text-fig. 10 seen from above. foramen of the origin of that nerve, which therefore passes down behind it and goes forward beneath it. These are the relations which the palatine nerve bears to the basitrabecular process of other forms. The veins of this region pass dorsal to the process, as they do to a basitrabecular process. While realizing
9 SKULL IN STURGEONS 679 that any process developing in this position would bear these relations, it is possible that this is a basitrabecular process, and that remnants of its connexion with the basal process of the palatopterygoquadrate are to be found in the cord of dense fibrous connective tissue. This vestige would indicate that Acipenser was developed from forms with a basal process, and it is interesting to note that fossils belonging to TEXT-FIGS. 12 AND 13. Fig. 12. Detail of the relations of the head-vein, orbital artery, and facial nerve. Pig. 13. Transverse section through ten-and-a-half-day stage errrbryo showing the basitrabecular process. this group and possessing a basal process have been described by Stensi0 (11). The sides of the membrane representing the dorsum sellae are cartilaginous and continuous with the side wall of the skull near the pila prootica. Posteriorly this membrane is not continuous with the parachordal plate, but leaves an opening which is really a fenestra basicranialis. In the adult the dorsum sellae is fully chondrified and overhangs a cavum sacci vasculosi similar to that of Lepidosteus or Polypterus, except that in Acipenser the fenestra hypophyseos is wholly closed. Turning to the posterior region of the skull, the occipital arch
10 680 G. E. DE BEER is formed, and from it there projects on each side a craniospinal process. The occipital region is complete. In the adult a large number of vertebral elements are included in the skull, which at this stage are more or less separate. This matter will be referred to again in connexion with the ventral roots and spinal nerves. The roofing of the skull has commenced, and there are to be found at this stage a tectum synoticum, and a tectum posterius in connexion with the occipital arch. The conditions are very like those in 70 mm. Heterodontus embryos (4), although TEXT-FIG. 14. Detail of the relation of the first branchial arch, glossopharyngeal nerve, and arteries. there the tectum posterius is not quite complete. (I take this opportunity of correcting an error which I made in the paper just quoted, in calling the tectum synoticum and the tectum posterius the tectum formed by the sphenolaterals and the tectum synoticum respectively.) The hyomandibular is large, and its continuation, the sympletic, connects it with the angle between the upper and lower jaws. The visceral arches now show the two articulations at the dorsal end, the infra- and supra-pharyngobranchials of van Wijhe (12) (Text-fig. 14). A somewhat similar state of affairs obtains in Polypterus, and in that animal Allis (1) has homologized the hinder or suprapharyngobranchial articula-
11 SKULL IN STURGEONS 681 tion with the epibranchial element of the arch, expanded dorsally and so coming to have a separate articulation with the auditory capsule. In Acipenser, however, if this homology holds good, the pharyngobranchial element (infrapharyngobranchial) articulates directly with the ceratobranchial, and the epibranchial (suprapharyngobranchial) does not separate them ; for the sutures in the cartilage are as in Text-fig. 14. Both these articulations lie lateral to the dorsal aorta and median to the head-vein, although the latter does connect with a sinus lying median to the suprapharyngobranchial. Whatever the homologies of these articulations may be, they are in no way to be regarded as corresponding with the double articulation of the mandibular or hyoid arches (de Beer, 3). 4. EELATIONS OF THE NERVES. The olfactory nerve passes through a foramen in the median wall of the olfactory capsule. The optic pierces the side of the skull in a foramen which represents part of the originally wide space between the trabecula and the sphenolateral cartilage. The same is true of the oculomotor and pathetic nerves. The relations of the oculomotor and pathetic nerves to the ophthalmic nerves are important in connexion with the homologies of the latter, and will be dealt with below. The prootic foramen transmits the complete trigeminal and facial nerves and the abducens. The trigeminal has the usual three branches. Taking first the ophthalmic, which is usually called profundus (Goronowitsch (6), Kurz (7)), van Wijhe (12), although calling this nerve the profundus, expresses doubt in a foot-note as to whether it really represents that element, as does Allis (2). These doubts are well founded, and for the following reasons the nerve cannot be a profundus : (i) It passes dorsal to the oculomotor instead of between its two branches, as a profundus does. (ii) It passes dorsal to the pathetic instead of ventral to it, as is the case with a profundus.
12 682 G. E. DE BEER Consequently it must be a ramus ophthahnicus superficial trigemini, or a part of that nerve. These relations I have verified in both the embryos studied and in a dissection of an adult specimen of A. sturio. Anteriorly the nerve leaves the orbit for the nasal capsule by a small foramen. There appears to be no profundus, even in the five-day stage, for there the relations are as just described. The ramus maxillaris trigemini runs forward in company with the buccal branch of the facial, dorsal to the basitrabecular process, and ventral to the optic nerve. The ramus mandibularis trigemini runs down to the lower jaw passing lateral to the head-vein. The abducens issues from the prootic foramen beneath the trigeminal mass and turns forward along the side of the skull to innervate the external rectus. The facial presents several points of interest. The ramus ophthalmicus superficialis runs out of the prootic foramen (as does the whole facial nerve, there being no prefacial commissure) upward and forward on the inner side of the orbit. It passes dorsal to the pathetic, but Kurz (7) figures it as passing ventral to the superior oblique muscle. This, I venture to think, is a mistake, although I have not had opportunities of examining the Jangtse species of sturgeons ; for in the sections of A. stellata and in my dissection of A. sturio the nerve in question passes over the muscle, as in all other known forms. The ramus buccalis facialis accompanies the ramus maxillaris trigemini, passing ventral to the optic nerve and distributing branches to the infra-orbital lateral line canal. The ramus palatinus facialis leaves the posterior portion of the ganglionic mass and runs ventrally lateral to the trabecula and median to the head-vein, and it passes in the fork between the internal carotid (median to it) and the efferent mandibular artery (lateral to it). Thereafter it continues its course forwards, passing ventral to the basitrabecular process. The ramus oticus facialis emerges from the ganglion and runs upwards and backwards, piercing a small foramen in the
13 SKULL IN STURGEONS 683 cartilage of the shelf of the postorbital process which projects forwards from the anterior side of the auditory capsule. The ramus hyomandibularis facialis runs back, passing beneath the head-vein (Text-fig. 15), and enters the canal in the side wall of the skull in company with that vein and the orbital artery (Text-fig. 12). In so doing it passes median to the hyomandibular cartilage, for when it emerges from the canal it is behind the hyomandibular. TEXT-FIG mm. Transverse section through ten-and-a-half-day stage embryo showing relations of the head-vein, orbital artery, hyomandibular nerve, and hyomandibular cartilage. The nerve then splits into two the ramus hyoideus facialis which runs down the postero-lateral face of the hyomandibular to the ventral regions of the hyoid arch, and the ramus mandibularis facialis. The figures illustrating the course of this nerve are discrepant in the literature of the subject, for whereas Goronowitsch (6) and Kurz (7) indicate its course by dotted lines implying that it passes on the inside of the cartilage, van Wijhe (12) shows it on the outside of the hyomandibular, though he states that it is protected by a spicule of bone. In the adult I find that this nerve passes forwards lateral to the hyomandibular cartilage (Text-fig. 10 shows the relations NO. 276 z Z
14 684 G. R. DB BEER in the larger embryo), but that for a short distance it is overlain by a thin piece of bone. Possibly it is this fact that the two above-mentioned authors have attempted to represent by dotted lines. The further course of this nerve shows that it is a ramus mandibularis internus facialis, for it passes median to the symplectic and to the ligament joining the mandibular and hyoid arches. I agree with Goronowitsch in not finding a ramus mandibularis externus facialis. The glossopharyngeal nerve emerges median to the headvein from a foramen just dorsal to the first branchial arch. It sends a ramus pharyngeus ventrally forwards and a ramus pretrematicus, which passes forward over the top of the first gill-slit and descends the hyoid arch behind the ramus hyoideus facialis, to which it gives a few fibres. The ramus posttrematicus glossopharyngii passes outwards in front of the suprapharyngobranchial articulation of the first branchial arch (Text-fig. 14) and descends behind the arch. A ramus supratemporalis was not found in the sections. The branches of the vagus, which emerges lateral to the headvein, were not studied. Beneath the vagus there is at this stage one ventral root. Behind the occipital arch a dorsal root and ventral root unite to form a mixed nerve. Cephalization must then be far from complete at this stage. The dorsal ganglion belongs to Piirbringer's segment x (5), Sewertzoff's (9) fourth myotome, and the ventral root anterior to the occipital arch must be the transient to of the same series. 5. DISCUSSION. The relations of the ramus hyomandibularis facialis are important. For if the conditions in the sturgeon (Textfig. 16) are compared with those in the Selachian (Text-fig. 17), it is obvious that the only difference lies in the dorsal articulation of the hyomandibular. As shown in a previous paper (3), the so-called hyomandibular may have one of two different
15 SKULL IN STURGEONS 685 dorsal articulations, both of which are shown diagrammatically together in Text-fig. 18. The hyomandibular of the Selachian pohjxx,., r I ac f pbhnx' i TEXT-ITOS ohmf rnnvd \ r-hvii lim hm Diagrammatic representations of the relations of the hyomandibular nerve and cartilage in Kg. 16. Acipenser. Fig. 19. Holostean. Kg. 17. Selachian. Kg. 18. Hypothetical type. Kg. 20. Polypterus. represents a basal articulation and the nerve and the head-vein pass lateral to it. The articulation of Acipenser is comparable to an otic process, formed by a modified branchial ray-bar, and tho nerve and the vein pass median to it. The z z 2
16 686 G. E. DB BEER nerve then passes out freely behind the posterior surface of the hyomandibular cartilage. If in this condition another branchial ray-bar were to plaster itself on to the hyomandibular from behind, the nerve would issue between them through a foramen, and the condition characteristic of Holostei (Textfig. 19) would be produced, as suggested by Allis (1). It is therefore of interest to note that the Holostean condition cannot be derived from the Selachian, whereas it can from the Chondrostean. The same is true if the Holostean hyomandibular was derived from the Ohondrostean type, by the nerve eating forwards into the cartilage. The conditions in Polypterus (Text-fig. 20), in which the ramus hyoideus passes behind and the ramus mandibularis in front of the hyomandibular, cannot be derived from the Holostean type unless either the nerve or the cartilage has changed. This is of interest in view of the tendency to regard Polypterus as related to the Palaeoniscoids and so to the sturgeons. 6. SUMMARY. 1. Acipenser stellata of the age of ten and a half days has a process which by its relations suggests that it is a basitrabecular process, and it may represent the vestige of the basal articulation of the palatoquadrate. 2. The so-called profundus is a ramus ophthalmicus superficialis trigemini, the profundus being absent. LIST OF LITERATURE CITED IN THIS PAPER. 1. Allis, E. P. " On the origin of the hyomandibula of the Teleostomi ", ' Anat. Rec.', 15, " The ophthalmic nerves of the gnathostome fishes", ' Journ. Comp. Neur.', 30, de Beer, G. R. " Studies on the Vertebrate Head, Part I", ' Quart. Journ. Micr. Sci.', 68, " Contributions to the study of the development of the head in Heterodontus ", ibid. 5. Fiirbringer, M. " Ueber die spino-occipitalen Nerven ", ' Festschr. v. C. Gegenbaur', 1897.
17 SKULL IN STURGEONS Goronowitsch, N. " Das Gehirn und die Kranialnerven von Acipenser ruthenus ",' Morph. Jahrb.', 13, Kurz, E. " Untersuchungen zur Anatomie des Kopfes des Jangtsestores ", ' Zeit. f. Anat. u. Entwicklungsgesch.', 75, Parker, W. K. " On the structure and development of the skull in sturgeons ", ' Phil. Trans. Roy. Soc.', Sewertzoff, A. N. " Die Entwickelung der Occipitalregion der niederen Vertebraten ",' Bull. Soc. Imp. Nat. Moscou ', " The place of the cartilaginous Ganoids in the system and the evolution of the Osteichthyes ", ' Journ. Morph.', 38, Stensio. ' Triassio fishes from Spitzbergen', Vienna, Wijhe, J. van. " Ueber das Visceralskelett und die Nerven des Kopfes der Ganoiden und von Ceratodus", ' Niederl. Arch. f. Zool.', 5, 1882.
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