Book - The brain of the tiger salamander 2

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Herrick CJ. The Brain of the Tiger Salamander (1948) The University Of Chicago Press, Chicago, Illinois.

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Part I. General Description and Interpretation 1. Salamander Brains | 2. Form and Brain Subdivisions | 3. Histological Structure | 4. Regional Analysis | 5. Functional Analysis, Central and Peripheral | 6. Physiological Interpretations | VII. The Origin and Significance of Cerebral Cortex | VIII. General Principles of Morphogenesis Part 2. Survey of Internal Structure 9. Spinal Cord and Bulbo-spinal Junction | 10. Cranial Nerves | 11. Medulla Oblongata | 12. Cerebellum | 13. Isthmus | 14. Interpeduncular Nucleus | 15. Midbrain | 16. Optic and Visual-motor Systems | 17. Diencephalon | 18. Habenula and Connections | 19. Cerebral Hemispheres | 20. Systems of Fibers | 21. Commissures | Bibliography | Illustrations | salamander

Chapter II The Form and Subdivisions of the Brain


REFERENCE to figures 1-5, 85, and 86 shows that the larger; subdivisions of the human brain are readily identified in Amblystoma, though with remarkable differences in shape and relative size. When this comparison is carried to further detail, the sculpturing of the ventricular walls shown in the median section is especially instructive. It is again emphasized that the application of mammalian names to the structures here revealed rarely implies exact homology; these areas are to be regarded as primordia from which the designated mammalian structures have been differentiated. The relationships here implied have been established by several independent lines of evidence: (1) The relative positions and fibrous connections of cellular masses and the terminal connections of tracts. In so far as these arrangements conform with the mammalian pattern, they may be regarded as homologous. (2) Embryological evidence. The early neural tubes of amphibians and mammals are similar, and subsequent development of both has been recorded. On the basis of Coghill's observations of rates of proliferation and differentiation in prefunctional stages, the writer ('37) gave arbitrary numbers to recognizable sectors of the neural tube in early functional stages, and the subsequent development of each of these is, in broad lines, similar to that of corresponding mammalian parts. (3) The relationships of svipposed primordia of mammalian structures may be tested by the comparative method. In an arrangement of animal types which approximates the phylogenetic sequence from the most generalized amphibians to man, there are many instances of progressive differentiation of amphibian primordia by successive increments up to the definitive human form.

Many pictures of the brains of adult and larval Amblystoma and other urodeles have been published, some of which I have cited ('35a, p. 239). The most accurate pictures of the brain of adult A. tigrinum are those of Roofe ('35), showing dorsal, ventral, and lateral aspects and the distribution of endocranial arteries and veins. The outHnes of the brain were drawn from specimens dissected after preservation for 6 weeks in 10 per cent formahn. One of these is shown here (fig. 86 A). Figure IB is drawn from a dissection made by the late Dr. P. S. McKibben, showing the sculpturing of the ventricular surfaces. Figures lA and 85 are drawn from a wax model in which there is some distortion of the natural proportions. Not all the differences seen in these pictures and in the proportions of sections figured are artifact, for the natural variability of urodele brains is surprisingly large (Neimanis, '31). Brains of larval stages have been illustrated by many authors and in my embryological papers of 1937-39.

The somewhat simpler brain of the mudpuppy, Necturus, has been described in a series of papers as completely as available material permits, and comparison with the more differentiated structure of Ambly stoma is instructive. The sketches shown in figures 86B and C illustrate the differences between the form of this forebrain and that of Amblystoma. The monograph of 1933 contains a series of diagrams ('33&, figs. 6-16) of the internal connections of the brain of Necturus similar to those of Amblystoma shown here (figs. 7-24). In 1910 I described the general features of the forebrain of A. tigrinum, with a series of drawings of transverse Weigert sections, no. lie, which has subsequently been used as the type specimen. Though this paper contains some errors and some morphological interpretations which I now regard as outmoded ('33a), most of the factual description has stood the test of time, and additional details and reports on other parts of the brain have been published in a series of papers.

The most conspicuous external fissures of the brain of Amblystoma are: (1) the longitudinal fissure separating the cerebral hemispheres; (2) the deep stem-hemisphere fissure; (3) a wide dorsal groove separating the epithalamus from the roof (tectum) of the midbrain; (4) the ventral cerebral flexure or plica encephali ventralis, which is a sharp bend of the floor of the midbrain, where it turns downward and backward into the "free part" of the hypothalamus; and (5) the fissura isthmi, extending downward and forward from the anterior medullary velum between midbrain and isthmus. The middle part of the fissura isthmi is at the anterior border of the auricle, which is more prominent in the larva than in the adult ('14a, figs. 1-3). Here in the adult it lies near the posterior border of the internal isthmic tissue, some distance posteriorly of the ventricular sulcus isthmi; but, like the latter, it really marks the anterior border of the isthmus, as will appear in the description of the development of the isthmic sulcus (p. 179).

The obvious superficial eminences on the dorsal aspect of the brain are the small cerebellum, the dorsal convexity of the roof of the midbrain (tectum mesencephali) , the habenular nuclei of the epithalamus, and the two cerebral hemispheres. Posteriorly of the habenulae in the early larvae is the membranous pineal evagination, which in the adult is a closed epithelial vesicle detached from the brain except for the few fibers of the parietal nerve. The lateral aspect of the thalamus, midbrain, and isthmus is a nearly smooth convexity, posteriorly of which is the high auricle, composed of tissue which is transitional between the body of the cerebellum and the acousticolateral area of the medulla oblongata. This auricle contains the primordia of the vestibular part of the cerebellar cortex (flocculonodular lobe of Larsell), and most of its tissue is incorporated within the cerebellum in mammals. On the ventral aspect there is a low eminence in front of the optic chiasma, which marks the position of the very large preoptic nucleus, and a similar eminence behind the chiasma formed by the ventral part of the hypothalamus. The latter is in the position of the human tuber cinereum but is not exactly comparable with it. Most of the hypothalamus is thrust backward under the ventral cerebral flexure as the pars libera hypothalami. The large pars glandularis of the hypophysis envelops the posterior end of the infundibulum and extends spinal ward from it, not anteriorly as in man.

The primary subdivisions of the human brain as defined from the embryological studies of Wilhelm His are readily identified in adult Amblystoma, as shown in the median section (fig. 2A).

At the anterior end of each cerebral hemisphere is the very large olfactory bulb, the internal structure of which shows some interesting primitive features (p. 54; '246). The bulbar formation extends backward on the lateral side for about half the length of the hemisphere, but on the medial side only as far as the anterior end of the lateral ventricle (figs. 3, 4). Bordering the bulb is an undifferentiated anterior olfactory nucleus, and posteriorly of this the walls of the lateral ventricle show early stages of the differentiation of the major subdivisions of the mammalian hemisphere — in the ventrolateral wall a strio-amygdaloid complex, ventromedially the septum, and dorsally the pars pallialis. In the pallial part no laminated cortical gray is differentiated, but there are well-defined pallial fields: dorsomedially, the primordial hippocampus; dorsolaterally, the primordial piriform lobe; and between these a primordium pallii dorsalis of uncertain relationships.

The boundaries of the diencephalon, as here defined and shown in figure 2A, are: anteriorly, the stem-hemisphere fissure and the posterior border of the anterior commissure ridge and, posteriorly, the anterior face of the posterior commissure and the underlying commissural eminence and, more ventrally, the sulcus, s, which marks the anterior border of the cerebral peduncle. The inclusion of the preoptic nucleus is in controversy; but, whether or not this inclusion is justifiable morphologically, its relationships with the hypothalamus are so intimate that it is practically convenient to consider these parts together. The four primary subdivisions of the diencephalon as I defined them in 1910 are: (1) the dorsal epithalamus, containing on each side the habenula and pars intercalaris, the latter including the pretectal nucleus; (2) pars dorsalis thalami, which is the primordium of the sensory nuclei of the mammalian thalamus; (3) pars ventralis thalami, the motor zone of the thalamus, or subthalamus; (4) hypothalamus. The mammalian homologies of these areas are clear, though their relative sizes and fibrous connections exhibit remarkable differences.

The posterior boundary of the mesencephalon is marked by the external fissura isthmi, the ventricular sulcus isthmi (fig. 2B,, and ventrally in the floor plate a pit, the fovea isthmi [f.i.). These are all more prominent in the larva than in the adult. This sector includes the posterior commissure, the tectum mesencephali (primordial corpora quadrigemina) , the underlying dorsal tegmentum (subtectal area), and the area surrounding the tuberculum posterius at the ventral cerebral flexure, termed the "nucleus of the tuberculum posterius." On embryological grounds and for convenience of description, this ventral area, which is bounded by the variable ventricular sulcus s, is here called the "peduncle" in a restricted sense ('36, p. 298; '396, p. 582). This is a primordial mesencephalic structure which is not the equivalent of the peduncle of human neurology. Amblystoma has nothing comparable with the human basis pedunculi, and its "peduncle" is incorporated within the tegmentum of the human brain. The III cranial nerve arises within the "peduncle" and emerges near the fovea isthmi. The nucleus of the IV nerve is in the isthmus. In the human brain there are no definite structures comparable to the amphibian dorsal and isthmic tegmentum.

The isthmus is much more clearly defined than in adult higher brains, it is relatively larger, and its physiological importance is correspondingly greater, as will appear later. It is bounded anteriorly by the sharp isthmic sulcus and posteriorly by the cerebellum, auricle, and trigeminal tegmentum. The so-called "pons" sector of the human brain stem is named from its most conspicuous component, but this name is meaningless in comparative anatomy. In man it is the pons and the sector of the stem embraced by it; but in no two species of mammals is the part embraced by the pons equivalent; and below the mammals the pons disappears entirely. The medulla oblongata, on the other hand, is a stable structure, extending from the isthmus to the spinal cord, and for it the shorter name "bulb" is sometimes used, especially in compounds.

I outlined the development and morphological significance of the urodele cerebellum ('14, '24), and this was followed by detailed descriptions of the development and adult structure of this region of Amblystoma by Larsell ('20, '32), whose observations I have subsequently confirmed, including his fundamental distinction between its general and its vestibular components.

Some features of the larval medulla oblongata and related nerves have been described ('14a, '396) and, more recently ('446), additional details of the adult, particularly the structures at the bulbospinal junction. Much remains to be done to clarify the organization of the medulla oblongata and spinal cord.

The cranial nerves and their analysis into functional components (chap, v) were described by Coghill ('02). The embryological development of these components also has been extensively studied (chap. x). The arrangement and composition of these nerves are fundamentally similar to those of man, with a few notable exceptions. The internal ear lacks the cochlea, which is represented by a very primitive rudiment; a cochlear nerve, accordingly, is not separately differentiated. There is an elaborate system of cutaneous organs of the lateral lines, whose functions are not as yet adequately known. These are supplied by very large nerves commonly assigned to the VII and X pairs, though it would be more appropriate to regard them as accessory VIII nerves, for all these nerve roots enter a wide zone at the dorsolateral margin of the medulla oblongata known as the "area acusticolateralis." There is no separate XI cranial nerve, this being represented by an accessorius branch of the vagus. The XII nerve is represented by branches of the first and second spinal nerves. The first spinal nerve in some specimens has a small ganglion ; the second nerve always has a large dorsal root and ganglion. In this connection a passage in the comprehensive work on the anatomy of Salamandra by Francis ('34, p. 134) is worthy of mention: "After making due allowance for the absence of a lateralis component in the adult salamander, the correspondence between the cranial nerves of this animal and those of Ambly stoma is very close indeed."

The configuration and mutual relations of the gross structures just surveyed can be seen only in sections, of which many, cut in various planes, have been illustrated in the literature. Only a few selected examples are included in the present work, with references in subsequent chapters to many others. For general orientation the following figures may be consulted : a series of selected transverse sections from the spinal cord to the olfactory bulb (figs. 87-100); a series of horizontal sections through the middle part of the brain stem (figs. 25-36); a few sagittal sections (figs. 101-4). Figures 6-24 show the chief fibrous connections of each well-defined region of the brain stem.

The diencephalon, mesencephalon, and isthmus have the form of three irregular pyramids oppositely oriented (fig. 2A). The broad base of the diencephalon extends from the anterior commissure to the hypophysis, and the apex is at the epiphysis. The tectum forms the base of the mesencephalic pyramid, and the apex is at the ventral tip of the tuberculum posterius, which borders the ventral cerebral flexure. The base of the pyramidal isthmus is formed by the massive tegmentum isthmi of each side and the median interpeduncular nucleus in the floor plate. It narrows dorsally into the anterior medullary velum between the tectum and the cerebellum.

The middle sectors of the brain stem — diencephalon, mesencephalon, and isthmus — contain the primordial regulatory and integrating apparatus controlling the fundamental sensori-motor systems of adjustment. The most important peripheral connections are with the eyes, and these in most vertebrates play the dominant role in maintaining successful adjustment with environment. From this topographical feature it naturally followed that, during the course of phylogenetic differentiation of the brain, the chief centers of adjustment of the other exteroceptive systems were elaborated in close juxtaposition with the visual field in the midbrain and thalamus.

Here they are interpolated between the primary sensory and motor apparatus of the medulla oblongata and spinal cord below and the great olfactory field and suprasegmental apparatus of the cerebral hemispheres above.

In all lower vertebrates the roof of the midbrain, the tectum, is the supreme center of regulation of motor responses to the exteroceptive systems of sense organs. The hypothalamus is similarly elaborated for regulation of olfacto- visceral adjustments. The patterning of motor responses for both these groups of receptors is effected in the cerebral peduncle and tegmentum. In the region of the isthmus, between the tectum and the primary vestibular area of the medulla oblongata and above the tegmentum, the cerebellum was elaborated as the supreme adjustor of all proprioceptive systems.

At the rostral end of the brain, within and above the specific olfactory area of the cerebral hemisphere, there gradually emerged a synthetic apparatus of control, adapted to integrate the activities of all the other parts of the nervous system and to enlarge capacity to modify performance as a result of individual experience. In the lowest vertebrates this "suprasensory" and "supra-associational" apparatus, as Coghill termed it, is not concentrated in the cerebral hemispheres, but it is dispersed, chiefly in the form of diflfuse neuropil. In the amphibian cerebral hemispheres this integrating apparatus is more highly elaborated than elsewhere, with some local differentiation of structure. The hemispheres are larger than in fishes, and the primordia of their chief mammalian subdivisions can be recognized. A dorsal pallial part is distinguishable from a basal or stem part of the hemisphere, though the distinctive characteristics of the pallium are only incipient. There is no cerebral cortex, and, accordingly, the mammalian cortical dependencies in the thalamus, midbrain, and cerebellum have not yet appeared. The primordial thalamus is concerned chiefly with adjustments within the brain stem, though precursors of the thalamic radiations to the hemispheres are present.


The lateral ventricles of the cerebral hemispheres have the typical form except at the interventricular foramen, where the amphibian arrangement is peculiar. The anterior and hippocampal commissures do not cross as usual in or above the lamina terminalis, but in a more posterior high commissural ridge ; and between these structures there is a wide precommissural recess, into which the interventricular foramina open. This results in some radical differences from reptilian and mammalian arrangements of the related fiber tracts and membranous parts, as elsewhere described (p. 291; '35). The third ventricle is expanded dorsally into the complicated membranous paraphysis and dorsal sac. Ventrally, the great elongation of the preoptic nucleus gives rise to a large preoptic recess between the anterior commissure ridge and the chiasma ridge, and in front of the latter there is a lateral optic recess (fig. 96), which in early larval stages extends outward as far as the eyeball, as a patent lumen of the optic nerve ('41), an arrangement which persists in the intracranial part of the nerve of adult Necturus ('41a). In the hypothalamus the ventricle is dilated laterally ('35a, p. 253; '36, figs. 10-14), and posteriorly it is a wide infundibulum with membranous roof and thin but nervous floor and posterior wall. The latter is the pars nervosa of the hypophysis and is partly enveloped by the pars glandularis (figs. 2, 101; '35a, p. 254; '42, p. 212 and figs. 56-65; Roofe, '37). The aqueduct of the midbrain is greatly expanded dorsoventrally. Its ventral part is contracted laterally by the thick peduncles and tegmentum, and the dorsal part is dilated as an optocoele. The sulcus lateralis mesencephali marks its widest extent, and tectal structure reaches far below this sulcus. The fourth ventricle is of typical form except anteriorly, where the wide lateral recess with membranous roof extends outward and forward to cover the whole dorsolateral aspect of the auricular lobe (figs. 90, 91 ; '24, p. 627). The rhombencephalic chorioid plexus is elaborately developed in interesting relation with the peculiar endolymphatic organs of this animal ('35, p. 310). The ventricular systems of adult Triturus (Diemyctylus) and of larval and adult stages of Hynobius have been described and illustrated with wax models bySumi('26, '26a).

The ventricular surface of both larvae and adults is clothed with very long cilia. These are not preserved in ordinary preparations and in our material are seen only in Golgi sections, where their impregnation is erratic and local ('42, p. 196). They are most frequently seen in the infundibulum and optocoele under the tectum. In the vicinity of the posterior commissure the ciliated ependyma is thickened (subcommissural organ of Dendy), and to it the fiber of Reissner is attached ('42, p. 197). This thick, nonnervous fiber extends backward through the ventricle to the lower end of the spinal cord and, like the cilia, is apparently an outgrowth from the internal ependymal membrane.


The meninges of Amblystoma were described in 1935. This account shoukl be compared with that of Salamandra pubhshed in 1934 by Francis, whose description was based on the investigation of Miss Helen O'NeiU ('98), done under the direction of Wiedersheim and Gaupp. In Amblystoma the meninges are intermediate between the meninx primitiva of the lower fishes and those of the frog. Over the spinal cord and most parts of the brain a firm and well-defined pachymeninx, or dura, closely invests the underlying undifferentiated pia-arachnoid. The meninges of the frog have been described by others, and recently Palay ('44) has investigated their histological structure in the toad. The most interesting feature of these amphibian membranes is their intimate relation with the enormous endolymphatic organ described by Dempster ('30) and the associated blood vessels.

The vascular supply of these brains is peculiar in several respects. The distribution of arteries and veins has been described by Roofe ('35, '38), and I have added some details from the adult ('35) and the larva {'Md). The endocranial veins form a double portal system of sinusoids of vast extent and unknown significance. Between the cerebral hemispheres and the epithalamus the nodus vasculosus (Gaupp) is permeated by a complicated rete of sinusoids, which receives venous blood from the entire prosencephalon— chorioid plexuses, brain wall, and meninges. The efferent discharge from this rete is by the two oblique sinuses, which pass backward across the midbrain to enter a similar rete of wide, anastomosing smusoids spread over the chorioid plexus of the fourth ventricle and the lobules of the endolymphatic organs. This rete also receives the vems from all posterior parts of the brain, meninges, and chorioid plexus. The common discharge for all this endocranial venous blood is by a large sinus, which emerges from the cranium through the jugular foramen and joins the jugular vein. These membranous structures are readily observable in the living animal without serious disturbance of normal conditions, and they provide unique opportunities or experimental study of some fundamental problems of vascular

^\\' wSomted out by Craigie ('38, '38a, '39, '45) that within the substance of this brain the penetrating blood vessels are arranged in two ways-a capillary net of usual type and simple loops, which enter from the meningeal arterial network. Our preparations confirm this observation and also the fact that the vascular pattern varies in different parts of the brain. Both isolated loops and the capillary net may be seen in the same field, as in the dorsal thalamus (fig. 44), or one of these patterns may prevail, with few, if any, instances of the other. In the tectum and dorsal tegmentum of the midbrain, for instance, the tissue is vascularized by simple loops with only occasional anastomosis (fig. 48), while in the underlying peduncle and isthmic tegmentum the vascular network prevails, with occasional simple loops. In the meninges and chorioid plexuses only the network has been observed.

The telencephalic and diencephalic chorioid plexuses have an abundant arterial blood supply through the medial hemispheral artery; but the elaborately ramified tubules of the paraphysis seem to have no arterial supply or capillary net, the accompanying vessels being exclusively venous sinusoids ('35, p. 342). The same seems to be true of the endolymphatic sacs ('34c?, p. 543). The chorioid plexus of the fourth ventricle has abundant arterial blood supply. In all plexuses the capillaries unite into venules, which discharge into wide sinusoids, which ramify throughout the plexus and have very thin walls. All arterioles of the chorioid plexuses are richly innervated, but it has not been possible to get satisfactory evidence of the sources of these nerve fibers ('36, p. 343; '42, p. 255; Necturus, '336, p. 15).

The enormous development of the chorioid plexuses and associated endolymphatic organ of urodeles is apparently correlated with the sluggish mode of life and relatively poor provision for aeration of the blood. In the more active anurans the plexuses are smaller; but in the sluggish mudfishes, including the lungfishes, with habits similar to those of urodeles, we again find exaggerated development of these plexuses. Existing species in the border zone between aquatic and aerial respiration are all slow-moving and relatively inactive. The enlarged plexuses and sinusoids give vastly increased surfaces for passage of blood gases into the cerebrospinal fluid; and, correlated with this, the brain wall is thin everywhere, to facilitate transfer of metabolites between brain tissue and cerebrospinal fluid. Massive thickenings of the brain wall occur in many fishes and in amniote vertebrates, but not in mudfishes and urodeles.