Book - The brain of the tiger salamander 10

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

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Pages where the terms "Historic Textbook" and "Historic Embryology" 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 and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

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 X Cranial Nerves

Details of the peripheral distribution of the several systems of nerve components have been recorded for a considerable number of amphibian species, notably in many important papers by H. W. Norris. The first of this series was Strong's paper ('95) on the larval frog, which was followed by Coghill's description of the cranial nerves of Amblystoma, published in 1902. Their arrangement here may be regarded as typical for the vertebrate phylum as a whole, with no extreme specialization of any system. The constancy of the arrangement of these components at the superficial origins of the nerve roots in all vertebrates is remarkable, in view of the extreme diversity of both peripheral and central connections of their fibers and of the enormous differences in the number of fibers represented in the several systems among the various species. Except for the specific differences just mentioned, the chief departures from uniformity of composition of the nerve roots are the suppression in all Amniota of the large lateral-line components of the Ichthyopsida and the correlated differentiation of the cochlear apparatus in the higher classes.


The central connections of the olfactory and optic nerves and the nervus terminalis are described in the chapters relating to the forebrain and the midbrain. The other functional systems are discussed in chapters iv and v, and to those general statements some additional details of their arrangement in Amblystoma are given here.


Development

Some peculiar features of the development of the somatic motor roots were mentioned in the preceding chapter. The development of the visceral motor roots was described by Coghill, though many details remain to be filled in. The early development of the sensory systems of root fibers was studied by Coghill ('16, Paper II) and Landacre ('21 and later papers). In Landacre's paper of 1921 the embryos studied were identified as Plethodon glutinosus, but they subsequently proved to be Amblystoma jeffersonianum (Landacre, '26, p. 472). Older stages were described by Kostir ('24).


The embryological studies just mentioned were based on series of normal embryos. The conclusions reached have been checked experimentally, extended, and in some details corrected by Stone ('22, '26) and by Yntema ('37, '43), so that we now have very accurate information about the sources of the nerve cells of each sensory component of the ganglia of the V to X cranial nerves. The ganglion of the trigeminus is derived chiefly from neural crest, which also contributes some cells to the ganglia of the VII, IX, and X nerves (Landacre, '21, p. 15). Yntema ('37) found no neurons of neuralcrest origin in the facial ganglion ; but, since there is a small general cutaneous component of this nerve in adult Amblystoma, it is probable that some cells of neural-crest origin are present, as is known to be the case in some other animals. Part of the trigeminal ganglion (profundus ganglion of Landacre, '21, p. 23) is delaminated from the lateral ectoderm. The lateral-line ganglia are derived exclusively from the dorsolateral placodes of the ectoderm, and the ganglion of the VIII nerve from the auditory vesicle. The visceral ganglia of the VII, IX, and X nerves arise from epibranchial placodes. Landacre derived only the special visceral (gustatory) component of these ganglia from these placodes, but Yntema has shown that the larger part of the general visceral component also is of placodal origin. According to Yntema's analysis, epibranchial placodes give rise to general and special visceral components of the cranial ganglia, dorsolateral placodes to lateral-line components, the auditory placode to the VIII ganglion, and neural crest to general cutaneous and general visceral components. The mesencephalic nucleus of the V nerve is derived chiefly from a portion of the neural crest which is incorporated within the neural tube, though it is not certain that this is the exclusive source of these cells (p. 141, and Piatt, '45).


Survey of the Functional Systems General Somatic Sensory Nerve Roots

Here are included cutaneous sensibility of several modalities — touch, temperature, pain, and, in aquatic animals, refined chemical sensitivity. Associated with these nerves are those of deep pressure. The nervous apparatus of these various qualities of sense has not been successfully analyzed in lower vertebrates. Their fibers are mingled peripherally and also centrally, except for those of the mesencephalic V root. It is not improbable that some peripheral fibers may serve more than one of the modahties of sense as centrally analyzed.


The peripheral fibers of this system are usually described as the general cutaneous component of the nerves, though some of them are distributed to deeper tissues. Most of them enter the brain in the trigeminus root and smaller numbers in roots of the VII, X, and (probably) IX nerves. The vagal fibers of this system have wide peripheral distribution (Coghill, '02), including the ramus auricularis and other vagal branches and also anastomotic connections with branches of the IX and VII nerves. The peripheral distribution of the VII fibers has not been described. A few fibers of the sensory IX root have been seen (rarely) to descend in the spinal V fascicles. Most urodeles are said to lack a general cutaneous component of the IX nerve, though there is some evidence of it in Necturus ('30, p. 22). If the presence of these fibers is confirmed, they probably join the general cutaneous component of the vagus peripherally.


Many of the trigeminal fibers divide immediately upon entering the brain into the thick descending branches of the spinal V root and thinner ascending branches (fig. 40) of the cerebellar root. The longest course that can be taken by one of these bifurcated fibers is shown in figure 3. Some of these fibers take deeper courses, penetrating the spinal V root to enter the fasciculus solitarius (p. 148). Some of the mesencephalic V fibers also divide near their exit from the brain, with descending branches arborizing in the reticular formation of the upper medulla oblongata (p. 141 and fig. 13).


The spinal V root is large and well myelinated. It can readily be followed through the length of the medulla oblongata and for an undetermined distance into the spinal cord (figs. 87-90). Each of its fibers for its entire length is provided with a fringe of short collaterals (fig. 38), which are directed inward into a neuropil which is continuous dorsally with that similarly related with the VIII and lateralline roots, the whole forming^a common pool for the reception of all somatic sensory components (fig. 9). In the calamus region these collaterals mingle with collaterals and terminals of spinal root fibers of the dorsal funiculus and the spinal vestibular root, bulbar correlation tracts a and b, and the dorsolateral funiculus. This axonic neuropil is permeated by dendrites of the nucleus of the dorsal funiculus and commissural nucleus of Cajal.


In many of our Golgi preparations the central courses of the sensory V fibers are electively impregnated, often with no other fibers visibk- in their vicinity. Some of these from the larva have })een ilhistrated ('14a, figs. 48-51, 54; '396, figs. 4'2, 46, 47, 57-61, 67, 77). Figures 27-32 show V roots as seen in horizontal Cajal sections of the adult brain. Figure 32 passes through the two motor V roots and their nucleus; figure 40 includes three impregnated neurons of this nucleus and the bifurcating fibers of the sensory root, which are also shown in figure 38. Woodburne ('36, p. 451) saw thick root fibers of the trigeminus entering the cerebellar root; but, in the absence of Golgi sections, the thinner collaterals of the spinal root were not demonstrable.


The superior or cerebellar root of the trigeminus is much smaller than the spinal root, and at the ventrolateral border of the auricle it joins the spino-cerebellar tract (figs. 30, 31, 91). Many fibers of both tracts end here with open arborizations in a neuropil which is the primordium of the superior (chief, or pontile) nucleus of the mammalian trigeminus ; but some fibers of both tracts pass through this neuropil and continue dorsomedially into the body of the cerebellum, where they end, some on the same side and some decussating in the commissura cerebelli (figs. 31-34, 37, 91). These commissural fibers are joined by others arising from cells in the vicinity of the superior trigeminal neuropil, and many of the decussating fibers, after crossing, reach the superior neuropil of the other side, thus forming an intertrigeminal commissure. We here confirm, in the adult, Larsell's description ('32, p. 413) of the cerebellar commissure of the larva as composed chiefly of trigeminal and spinal components. In Amblystoma the superior sensory nucleus of the trigeminus probably is concerned chiefly with the proprioceptive aspects of cutaneous sensibility (deep proprioception being provided for in the mesencephalic V root). This cerebellar connection persists in man, but here the chief V nucleus has also acquired refined types of sensibility which Amblystoma lacks.


Neither the superior nor the spinal nucleus of the trigeminus has well-defined boundaries. The central cells which engage terminals and collaterals of the sensory V fibers may also have synaptic contacts with terminals of all other sensory systems that enter the medulla oblongata. There are, however, certain lines of preferential discharge for each group of sensory systems, and the segregation of local nuclei and secondary pathways for each functional system is incipient.


Lateral-Line, Labyrinthine, and Cochlear Systems

These special somatic sensory systems are closely related genetically, structurally, and physiologically, but much remains obscure about their relationships. The labyrinthine apparatus seems to be at the focus of these systems. It is very conservative, except for the cochlear part, showing relatively little change in structure and function from lowest to highest vertebrates; moreover, its physiological properties have been thoroughly explored. The lateralis system attains its maximum in fishes, persists in larval amphibians and adults of some urodeles, and disappears entirely in all higher groups, both embryonic and adult. Organs of hearing are poorly developed in fishes. Auditory functions seem to be performed by the vestibular . apparatus and also (for slow vibration frequencies) by the organs of the lateral line, which undoubtedly have other functions also.


The peripheral end-organs of all these systems are specialized epithelial structures, in contrast with the free nerve endings of the general somatic system. The vestibular end-organs of the internal ear resemble the end-organs of the lateral lines, in that in both cases there are specialized epithelial cells which are the receptive elements. The epithelium is thickened, and among the slender elongated supporting elements there are shorter ovoid cells with ciliated outer ends. These specific nerves have thick myelinated fibers, the branched unmyelinated terminals of which closely embrace the cell bodies of the specific receptive elements (Larsell, '29; Chezar, '30; Speidel, '46).


The lateral-line organs of Amblystonia are papillae, some of which are depressed in pits but are not inclosed in canals as in most fishes. Their arrangement conforms with the general pattern in fishes, with rows above and below the eye, on the lower jaw, and extending into the trunk as far back as the tail. The related nerves comprise one of the largest systems of the larva, which is reduced but not lost at metamorphosis. These thick and heavily myelinated fibers enter the brain in two large roots spiimlward of the VIII roots and three or four which enter dorsally and slightly rostrally of the VII roots. They are conventionally assigned to the VII and X pairs of nerves, though they are more properly aligned with the VIII roots.


The arrangement of these roots is shown in figures 7, 9, 89, 90. Most of their individual fibers bifurcate immediately upon entrance into the brain into ascending and descending branches with numerous widely spread collaterals. These root fibers are arranged in fascicles, which span almost the entire length of the medulla oblongata (fig. 7), except for the most dorsal of the three or four lateralis VII roots, which ends in a "dorsal island" of neuropil ("cerebellar crest" of Larsell) at the level of entrance (figs. 7, 33, 45). Lateral-line fibers have not been seen to descend into the spinal cord. Anteriorly, they enter the auricle and end here (fig. 91); none have been traced into the body of the cerebellum, though secondary lateralis fibers after synapse in the auricle enter the com. vestibulolaterahs cerebelli in company with vestibular fibers (figs. 32, 33, 34, com.cb.l.L).


The exact functions served by the lateral-line organs are still imperfectly understood. The organs of the lateral lines and those of the internal ear have many similarities in embryological development, structure of the receptive apparatus, and central connections. They probably have had a common evolutionary origin from a more generalized form of cutaneous sense organ similar to the so-called "sensillae" of some invertebrates. This may be the explanation of the intimate association in the human ear of sense organs of such diverse functions as the cochlea for hearing and the semicircular canals for equilibration, both being highly refined derivatives of primitive tactile organs. The sense organs of the lateral lines are probably intermediate in function between tactile sensibihty of the skin and the auditory and equilibrating functions of the internal ear. In fishes they have been shown to be sensitive to mechanical impact, slow vibrations, and currents in the water (Parker and Van Heusen, '17; Parker, '18). Hoagland ('33) and Schriever ('35) have investigated the functions of lateral-line nerves of fishes with the aid of oscillograph records of their action currents. Hoagland finds that these organs are in a state of continuous activity and that the nervous discharge is increased by application of pressure, by ripples and currents in the water, by movements of the trunk muscles, and by temperature changes.


In Amblystoma larvae Scharrer ('32) found evidence that the lateral-line organs may participate in the snapping reaction when moving prey is seized; and, subsequently, Detwiler ('45) reports that the lateral-line organs of these larvae constitute an adequate receptor apparatus for the detection of food in motion after extirpation of the eyes and nasal organs. The central connections of these nerves suggest that they play an important part in proprioception, and this is supported by Hoagland's experiments.


The VIII nerve of Amblystoma carries fibers from the membranous labyrinth, the structure of which resembles those of fishes plus a recognizable rudiment of the cochlea. These fibers enter the brain by two closely associated roots, dorsal and ventral, each of which contains many rather fine myelinated fibers, with some very coarse fibers mingled with them. Each fiber has a T-form division within the brain, the branches ascending and descending through the entire length of the medulla oblongata (figs. 7, 87-90). The dorsal and ventral roots remain separate as far forward as the V root and backward as far as the second root of the vagus. Beyond these limits the two roots merge. It is evident that fibers of the ventral fascicle take longer courses within the brain than do those of the dorsal fascicle, but the significance of the separation of vestibular fibers into two roots has not been determined. Some of these fibers descend for a long and undetermined distance into the spinal cord, mingled with the more ventral fibers of the dorsal funiculus and those of correlation tract b. The ascending fibers enter the auricle (figs. 29, 30, 31, 91), where many of them end. Others continue into the body of the cerebellum, decussate in the vestibulo-lateral cerebellar commissure, and terminate in the vestibular and lateralis neuropil of the auricle of the opposite side (figs. 32, 33, 34).


Within the medulla oblongata the collaterals and terminals of the vestibular fibers arborize in the common pool of neuropil, which also receives terminals of the V and lateral-line roots. Most of the neurons of the second order in the acousticolateral area spread their dendrites within this neuropil so as to engage terminals of several of these fascicles of root fibers of different physiological nature (fig. 9).


There is ample physiological evidence that salamanders exhibit vestibular control of posture and movement similar to that of other animals, and this implies that there is some central apparatus that is selective for the specialized end-organs of the internal ear. Sperry ('45a) has shown that in the case of the frog this specificity is. preserved after section of the VIII nerve and its subsequent regeneration and that the precision of restoration of vestibular function is quite as exact as it has been shown to be in the case of regeneration of the optic nerve (p. 229). Since the specific functions of the several vestibular end-organs are not visibly localized in the medulla oblongata of the salamander, some other method of selection must be employed. Sperry's experiments on frogs lead him to favor the supposition that there are physicochemical axon specificities and selective contact affinities between the different axon types and neurons of the vestibular centers, a supposition which accords with much other evidence (p. 79). Differences in threshold and the time factor in the transmission rhythm may act selectively at the central synapses.


Though Amblystoma has no recognizable cochlear root of the VIII nerve, there is a primordium of the pars basilaris cochleae, which is better developed in the frog. This rudiment is lacking in Necturus, so that among the Amphibia successive stages in the early differentiation of the cochlear apparatus can be observed.


The fibers of the dorsal lateral-line VII root are shorter than those of the others, all ending in the "dorsal island" of neuropil at the posterior border of the lateral recess of the ventricle (figs. 33, 45; '446, fig. 14; Larsell, '3^2, fig. 57). These fibers, like those of the other lateralis VII roots, come from lateral-line components of all three chief peripheral branches of the lateral-line VII nerves ('14a, p. 357). The dorsal island appears to be a remnant of the dorsal neuropil (cerebellar crest) of the lobus lineae lateralis described by Johnston ('01) in fishes.


In very young larvae of the frog (Larsell, '34) the relations are similar to those of urodeles, but soon a dorsal branch of the VIII nerve (derived from the primordial cochlea) enters this area dorsally of the dorsal lateral-line root. The dorsal island of neuropil retains its individuality to the time of metamorphosis, meanwhile becoming entirely surrounded by cells which proliferate from the dorsal lip of the area acusticolateralis. The dorsal VIII root is greatly enlarged to become the cochlear nerve; it terminates in relation with the cells surrounding the dorsal island, which now constitute the cochlear nucleus. After metamorphosis is complete, all lateral-line fibers degenerate, so that the gray of the larval area acusticolateralis becomes in the adult the cochlear nucleus dorsally and the vestibular nucleus ventrally.


Without here going into the further details of this differentiation, it is evident from Larsell's studies that the dorsal gray of the area acusticolateralis of urodeles and larval anurans is, during the metamorphosis of the frog, transformed directly into cochlear nuclei.


There is no degeneratioii of these cells and rei)lacement by others. The same neurons which in the tadpole are activated from lateralline organs lose their lateral-line connections in the adult frog and receive their excitations from the auditory apparatus, with a radical change of function. That which I at one time regarded as improbable ('30, p. 60) is exactly what happens in ontogeny, and doubtless the phylogenetic history is similar, as Ariens Kappers has long maintained. Parallel with the differentiation of the cochlear nerve and nucleus in anurans, the related lateral lemniscus is enlarged and specialized in its definitive form.


In Necturus, which has no recognizable cochlear primordium, the functions of the dorsal cells of the area acusticolaterahs evidently are related exclusively with lateral-line organs. The dorsal lateralis VII root terminating in the dorsal island does not differ physiologically from the other lateral-line roots of the VII nerve, so far as known. Like them, it receives fibers from lateral-line organs distributed over the entire head ('30, p. 21). But there is an obscure indication of a lateral lemniscus. Why do the fibers of the dorsal lateral-line root end in the restricted area of the dorsal island instead of extending through the whole length of the acousticolateral area like the other lateralis roots .^ The answer is probably to be sought in the phylogenetic history of the extinct ancestors of living urodeles. In fishes the lobus lineae lateralis of this region is covered by a neuropil, which has been termed the "cerebellar crest" and which extends forward into continuity with the superficial neuropil of the cerebellum. Larsell ('32, p. 410) regards the neuropil of the dorsal island as a survival of the cerebellar crest of fishes. This is the region within which the dorsal cochlear nucleus of anurans has been differentiated; and, if, as is generally believed, the living urodeles are descendants of more highly specialized ancestors with better organs of hearing, the preservation of their dorsal island may be regarded as a vestigial record of an ancestral history now lost.


The amphibian auricle (pp. 20, 44) receives terminals of trigeminal, lateral-line, and vestibular fibers. The connections of these fibers and their secondary pathways make it clear that this area contains primordia of two quite distinct mammalian structures. One of these is the terminal station of lateraMine and vestibular root fibers, and this tissue in higher animals is incorporated within the cerebellum and becomes the flocculus, as described by Larsell. The other primordium is trigeminal, and this in Amblystoma is probably concerned chiefly with proprioceptive functions of the skin and deep tissues of the head, as indicated by its strong cerebellar connection. This connection persists in mammals but is relatively insignificant here because, as mentioned above, the enlarged mammalian superior V nucleus is concerned chiefly with refined functions of the skin that Amblystoma does not possess.

Mesencephalic Nucleus And Root Of The Trigeminus

The system of the mesencephalic nucleus and root of the trigeminus is here well developed in typical relations, with some instructive special features. Its thick, well-myelinated fibers go out with branches of the V nerve. The details of their peripheral courses in Amblystoma have not been described. Experiments by Piatt ('46) indicate that the majority of the fibers of this system, which go out from the tectum opticum, are distributed to the jaw muscles. The more caudal cells of the mesencephalic nucleus probably have other connections. No evidence has been found for supply of any eye muscles from this nucleus.


Unlike other sensory systems, the cell bodies of these neurons lie within the brain. Their arrangement and the courses of the fibers arising from them have been described in the larva ('14a, p. 361) and in the adult ('36, p. 345) and are shown diagrammatically in figure 13. These cells vary in size, cytological structure, and number. Most of them are very large and of so characteristic appearance that they are easily recognized. They are sparsely distributed throughout the tectum in all layers of the gray substance, somewhat less numerous anteriorly near the posterior commissure, and densely crowded within and adjoining the anterior medullary velum. Occasionally, they are seen in the body of the cerebellum and in the nucleus cerebelli. Ten large larvae of A. punctatum had an average of 159 of these cells, the extremes being 76 and 208 (Piatt, '45). A subsequent count by Piatt ('46) of the total number of these cells in ten larvae of 45 mm. gave an average of 261 cells, equally divided on right and left sides. Of these cells, 86 on each side are in the tectum opticum and 45 in the nucleus posterior tecti and velum medullare anterius. Individual variations in numbers of cells are large, but approximate bilateral symmetry is quite consistently present. These cells are unipolar, the single thick processes accumulating near the outer border of the tectal gray and here acquiring myelin sheaths. These fibers are directed posteroventrally in loosely arranged dorsal and ventral fascicles, which converge toward the V nerve roots.


The ovoid cell body has a smooth contour, with no processes except the single thick fiber. It is imbedded in dense neuropil and closely enveloped by a web of these fibers. Every contact of the fibers of the neuropil with the cell is a synaptic junction. This is doubtless the explanation of the wide dispersal of these cells in all parts of the tectal gray, and they are so arranged that the entire extent of the deep tectal neuropil may be simultaneously activated by excitation of the mesencephalic V system.


The striking resemblance of the cells of the mesencephalic V nucleus with those of the semilunar and spinal ganglia and with the transitory Rohon-Beard cells of the spinal cord (Coghill, '14, Paper I) has often been commented upon and is well illustrated by the excellent photographs pul)lished by Piatt. They have, accordingly, been generally regaixled as derivatives of the embryonic neural crest that have remained within the neural tube. This hypothesis has been tested experimentally by Piatt ('45), with the conclusion that neural crest is at least one source of these cells, though a possible origin from other sources is not excluded. Many observers have reported the presence of intramedullary cells of sensory type along the courses of roots of spinal and cranial nerves (Pearson, '45, cites instances), and some of these cells also may be of neural-crest origin. Others may be of autonomic type, migrating out from the brain (Jones, '45), though this is controverted.


Just as the typical unipolar cells of the sensory ganglia of spinal and cranial nerves have a single process, which divides into peripherally and centrally directed branches, so the mesencephalic V fibers (or some of them) divide shortly before emergence from the brain into peripheral and central branches (fig. 13). The central branches descend as far as the level of the IX nerve roots. My earlier statement ('14a, p. 362) that these fibers ."arborize among the dendrites of the motor VII neurons" is misleading, for these terminals are spread widely in the intermediate zone between the levels of the V and the IX roots.


This bifurcation of the root fibers and the fact that the bodies of the cells of the mesencephalic V nucleus are in synaptic contact with all the deep neuropil of the tectum suggest that afferent impulses transmitted by these fibers may take either or both of two courses: (1) They may pass upward to the tectum, where they activate the deep neuropil diffusely and here are in relation with terminals of the optic and lemniscus systems; or ('2) they may descend into the reticular formation of the medulla oblongata, where they act directly upon the motor nuclei and also upon the apparatus of bulbar neuromotor co-ordination (including the cells of Mauthner). These descending branches are accompanied by fibers of the spinal V root and by other fibers from the tectum and tegmentum, which end in the same field of the reticular formation (fig. 13, tr.t.h.p. and tr.teg.b.). In larvae of early feeding stages, thick uncrossed fibers, which descend from the tectum and subtectal areas into the bulbar reticular formation, are especially clearly seen, and also others which take similar courses after decussation in the ventral commissure. Some of these fibers arise from neurons of the isthmus, which are in synaptic connection with terminals of the secondary visceral-gustatory tract. These connections of mesencephalic V fibers seem well adapted to facilitate the feeding reactions, a conclusion which is supported by observations on the cat by Corbin ('40) and the literature which he cites. In Ambly stoma the field of reticular formation within which the movements of the mouth and pharynx are organized receives the descending mesencephalic V fibers, collaterals of V fibers, and fibers of correlation from the nucleus of the f. solitarius, isthmic visceralgustatory nucleus, tectum, and the underlying dorsal tegmentum.


Proprioceptive Systems and Cerebellum

Control of the course of muscular movement in process is insured by a variety of sensory end-organs, including those in muscles, tendons, joints, and the overlying skin. At the beginning of motility in the embryogenesis of Amblystoma a single peripheral sensory element (the transitory Rohon-Beard cells) may perform both exteroceptive and proprioceptive functions (Coghill, '14, Paper I, p. 199), and this may be true of some spinal ganglion .cells in the adult, though here special proprioceptive apparatus also is provided. The Rohon-Beard cells are believed to be derived from a portion of the neural crest which is incorporated within the neural tube; and the mesencephalic nucleus of the trigeminus, as just described, has a similar origin. The latter cells survive in the adults of all vertebrates, in the service apparently of co-ordination of movements involved in the feeding reactions.


In the head the membranous labyrinth is the dominant organ of this system, with participation of nerves of cutaneous and deep sensibility, and probably the lateral-line organs also. Some proprioceptive control is doubtless organized in the reticular formation of the cord and bulb, but we have little information about how this is done. From the entire sensory zone of these regions, proprioceptive influence is filtered off and directed to the cerebellum, which is the general clearing-house for these functions. Many vestibular root fibers and a smaller number of trigeminal fibers go directly to the cerebellum, and secondary fibers from the sensory zone enter it by way of the spino-cerebellar tract and bulbar correlation tracts a and b (p. 159; '44&). That exteroceptive and proprioceptive functions are not completely segregated in these brains is shown by the fact that many fibers of the spinal lemniscus (tractus spino-tectalis) send collaterals into the cerebellum ('14o, p. 376). Within the cerebellum the general somatic sensory and vestibular components of the proprioceptive system are locally segregated, the former in the body of the cerebellum and the latter in the auricle, and this localization is a primary feature of the cerebellum in all vertebrates, as Larsell has shown. This author ('45) has also made it clear that cerebellar function includes much more than proprioception, or else the concept of proprioception must be redefined in more inclusive terms. The second alternative, I think, is better, as I have suggested in an article ('47) on the proprioceptive system, from which some of the following paragraphs are taken, by courtesy of the editor of the Journal of Nervous and Mental Disease.


Sherrington ('06, p. 347) defines the cerebellum as the head ganglion of the proprioceptive system, taking as the basis for his classification of receptors "the type of reaction which the receptors induce." In his exposition of this idea he makes it clear that the proprioceptive system is segregated from other sensory systems, not in terms of the receptors involved but because the system as a whole exerts regulatory control over the action of all skeletal muscles. The criteria employed here are applied in the efferent, not the afferent, side of the arc. In view of present knowledge of cerebellar function, Sherrington's original concept of proprioception should be emphasized and amplified.


It has long been recognized that in the cerebellum of lower vertebrates the sensory inflow is of two kinds, which are separately localized, viz., (1) the vestibular and lateral-line systems in the lateral part and (2) the spinal and trigeminal systems in the median body. The second category traditionally comprises deep sensibility of several sorts, notably that of muscle spindles, tendons, joints, and some other internal end-organs. Current physiological research requires radical revision and broadening of this traditional analysis. It has been shown that in mammals different cutaneous areas, vibrissae, audition, and vision have local representation in the cerebellum, as do also various systems of synergic muscles. In lower vertebrates the cerebellum has a broad connection with the hypothalamus, implying representation in the cerebellum of olfactory sensibility also.


In brief, cerebellar control of muscular movement employs practically all modalities of sense represented in the action system of the animal. The function of the cerebellum as the "head ganglion of the proprioceptive system" is not to pattern the muscular response (for these functions are localized elsewhere) but to facilitate its execution ; and this facilitation employs all available sensory experience. Many organs of sense perform simultaneously both exteroceptive and proprioceptive functions. Sherrington's fruitful analysis of the action system into interoceptive, exteroceptive, and proprioceptive components was not based upon the specificities of the receptive organs, considered either anatomically or physiologically; but, on the contrary, the distinction was drawn in terms of what the animal does in response to sensory excitations. The interoceptive systems are defined in terms of internal adjustments, chiefly visceral. The exteroceptive systems are those which evoke adjustments of the body or its members to events in the external world. The proprioceptive systems are ancillary to the activities of the musculature in maintenance of tonus, posture, and regulation of the action of synergic groups of agonist and antagonist muscles in appropriate strength and sequence.


Proprioception, therefore, must be defined not in terms of the modalities of sense employed but in terms of the results achieved. Cerebellar proprioceptive control is accomplished by the application of all relevant types of sensory inflow to specific and successive muscular activities which may be in process from moment to moment; and the definition of "proprioception" must be formulated in terms of the motor response rather than of the sensory systems involved. The proprioceptive system, accordingly, includes all peripheral endorgans and nerves and all central adjustors in the spinal cord, brain stem, cerebellum, and cerebral hemispheres that collaborate in the co-ordination and synergizing of muscular activity in process. In a recent conference with Dr. Larsell he suggested to me that, in view of the inadequacy of current conceptions of the true nature of the proprioceptive system and the faulty connotations of the term in present usage, it might be better to avoid the word hereafter and replace it by the more inclusive name, "proprius system."


The preceding comments on the proprioceptive system apply, mutatis mutandis, to Sherrington's exteroceptive and interoceptive systems also. In his original definitions of these terms, Sir Charles was careful to insist that each component of each of these three subdivisions of the total pattern of behavior must be viewed in its entirety as a unitary act and that the significance of these acts can be understood only in terms of their reciprocal relationships with one another and with the total action system of the animal. The critical feature of each of these acts is the end-result, the actual behavior exhibited. The names originally given to these three classes of functions put the emphasis on the receptive organs, w^here it does not belong. Some obscurity and confusion may be avoided if the unity of these several components of behavior is recognized in their nomenclature. The exteroceptive systems, viewed in their entirety, are somatic, the interoceptive systems are visceral, and the proprioceptive systems are ancillary to all muscular activity and, accordingly, may be termed proprius. Sherrington's terms, "exteroceptors," "interoceptors," and "proprioceptors" are suitable names for the receptive organs, with the qualification that the same organ may, on occasion, activate somatic, visceral, or proprius responses.


Visceral Sensory And Gustatory Nerve Roots

General visceral sensory fibers of wide peripheral distribution enter the brain by the vagus roots, and the IX and VII roots contain smaller numbers of similar fibers from the mucous surfaces of the mouth and pharynx. Taste buds are widely distributed in these mucous surfaces, and the gustatory fibers are indistinguishably mingled with the general visceral fibers peripherally in the roots of the VII, IX, and X nerves and centrally in the f . solitarius, more of them entering the brain anteriorly than posteriorly. This mixed group of peripheral fibers, as a whole, is quite distinct from all other functional systems and it was termed by the earlier students of nerve components in lower vertebrates the "communis system" because all its fibers converge into a single central bundle, the f. communis (Osborn, '88). This we now know is homologous with the mammalian f. solitarius. The peripheral and central arrangements of the chemoreceptors illustrate some general principles which will next be examined.

Chemical Sensibility

The peripheral terminals of the sensory fibers of the V to X cranial nerves take three forms: (1) The fibers of the general somatic sensory and visceral systems have free nerve endings within or beneath epithelium or widely spread in deeper tissues. (2) The end-organs of the special somatic sensory systems are differentiated epithelial structures of the internal ear or lateral lines with receptive hair cells, which are shorter than the surrounding supporting cells. (3) The chemoreceptors of the gustatory (special visceral sensory) system are budlike epithelial structures, which resemble the naked lateralline organs but differ from them in that the specific receptive cells are slender, elongated elements, which span the entire thickness of the epithelium. The fibers which innervate them are generally thinner than those of lateral-line organs and are less myelinated or unmyelinated.


Those species of fishes which have taste buds abundantly distributed in the outer skin and also naked organs of the lateral lines not inclosed in pits or canals present both morphological and physiological problems of great diflSculty ('03, '03a, h). In the earlier literature all these cutaneous organs were termed indiscriminately "terminal buds," with resulting confusion which was not clarified until the nerve fibers which supply them were found to belong to different functional systems. The fibers supplying lateral-line organs, wherever situated, converge centrally into the acousticolateral area, and fibers supplying taste buds,whether in mucous surfaces or in the outer skin, converge into the f. solitarius and its nucleus. The separation of the gustatory from the lateral-line system of cutaneous sense organs by the anatomical method has been confirmed by physiological experiments performed by the writer, G. H. Parker, and others.


Though this distinction is perfectly clear in some species of fishes, in others there are transitional forms of "terminal buds," and much remains obscure about the functions of these various types of receptors. The problem is complicated by the fact that in fishes the skin is everywhere very sensitive to a large variety of chemical substances (Sheldon, '09; Parker, '12, '22; Ariens Kappers, Huber, Crosby, '36, chap, iii; for a more general discussion of the chemical senses see Moncrieff, '44). The skin is sensitive, in general, to different substances from those which activate the olfactory organ and taste buds, but there are some puzzling exceptions.


For instance, the gurnard fishes (Prionotus, Trigla) have three rays of the pectoral fin which are mocUfied to serve as "feelers" in the search for food on the floor of the sea. Somewhat similar filamentous pelvic fins of the gourami, codfish, and several other teleosts are abundantly supplied with taste buds with the usual functions and nervous connections ('00, '03; Scharrer, Smith, and Palay, '47); but the free pectoral fin rays of the gurnards have no taste buds, and yet it has been shown (by the authors last mentioned) that these fin rays are sensitive to the same sapid substances as are the cutaneous taste buds of other fishes and that the reactions also are similar. These authors, in tracing the central courses of the large nerves which supply these free fin rays, find that these fibers have central connections similar to those of the pectoral fins of other fishes, belonging, that is, to the general cutaneous system. They do not enter the f. solitarius. They present evidence also that some secondary fibers from these general cutaneous centers connect centrally with the superior gustatory nuclei of the isthmus and hypothalamus, just as do the true gustatory fibers arising in the nucleus of the f, solitarius. This is interpreted to mean that these nerves of general cutaneous chemical sensibility are so specialized that they can serve typical gustatory reactions, though they do not connect peripherally with taste buds.


These observations seem to show that some peripheral fibers of the general cutaneous system, without specialized receptive end-organs, may acquire functions substantially identical with those of cutaneous taste buds and that such fibers have central connections similar to those from taste buds. It is evident that no rigid categories can be recognized here in terms of our conventional classification of "the senses" or of their organs, a principle illustrated also by Whitman's ('92) observations on the cutaneous sense organs of the leech, Clepsine, to which reference is made on page 84. Nature is not bound by our rules of logical analysis.


Taste buds within the mouth are interoceptors, but similar buds in the outer skin of fishes are typical exteroceptors, used in the selection and location of food, as are also the free nerve endings of the general cutaneous nerves that respond to chemical excitants. It is evident that all these nerve endings co-operate with the nerves of ordinary tactile sensibility in the normal process of finding food. That this cooperation is intimate and in some cases indispensable has been shown by Parker ('12) in the case of the catfish, Ameiurus. In this fish the skin has general chemical sensitivity to acid, alkali, and salt, a sensitivity which is served by general cutaneous nerves. In the skin there are also innumerable taste buds which are innervated by fibers which enter the f . solitarius. The general chemical sensibility is preserved if the taste buds are denervated, but the specific gustatory function of the taste buds is lost if the general cutaneous innervation of the surrounding skin is eliminated. A similar relation prevails with taste buds within the mouth, for these have a double innervation; and in man the gustatory function is abolished if the trigeminal innervation of the tongue is surgically destroyed, even though the specific innervation of the buds remains uninjured; this loss, however, is temporary, and after a few weeks gustatory function returns (Gushing, '03).


Amblystoma has no cutaneous taste buds, but the mouth cavity is abundantly supplied with them. They are especially numerous on the palate among the vomerine teeth, and these buds have a peculiar accessory innervation — a compact skein of circumgemmal fibers of uncertain origin ('256; Estable, '24). These fibers separate from a plexus related with the ramus palatinus and may be derived from a trigeminal anastomosis; but this has not been demonstrated.


The tactile, general chemical, and gustatory systems are as intimately related centrally as they are peripherally. All taste buds of all animals, wherever found, are supplied by fibers which discharge centrally into the nucleus of the f. solitarius or its derivatives. In those fishes which have cutaneous taste buds with exteroceptive functions the central connections of these buds differ from those of buds within the mouth which have interoceptive functions. These details need not be given here ; the interested reader is referred to a recent paper ('446) and references there given. These differences are explained by the fact that stimulation of interoceptive taste buds evokes visceral responses, but excitation of exteroceptive buds is followed by somatic movements for capture of food.


In Amblystoma, as in man and all other vertebrates, all fibers from taste buds enter the f . solitarius. Most fibers of all modalities of general cutaneous sensibility of the head enter the sensory V nucleus; but a small number of them pass through this nucleus to enter the f . solitarius, thus providing for integration of general somatic sensory and gustatory sensibility. The prefacial f. solitarius carries gustatory impulses forward into the neuropil of the superior trigeminal nucleus in the auricle. A third and much more extensive provision for bringing general cutaneous and both general and special visceral sensibility into physiological relation is at the bulbo-spinal junction (chap. ix).


The preceding analysis illustrates the intimate physiological relationship which exists among the various modalities of sense which may be concerned with the resolution of mixed sensory experience in the interest of securing the appropriate responses. The integrating apparatus is spread from the peripheral end-organs throughout the central nervous system. Within this machinery for conjoint action there have been differentiated the specific sensory and motor systems, that is, the analyzers. The first step in this analysis is the separation in the central adjustors of the visceral from the somatic systems. Thus the fibers of taste and general visceral sensibility converge into the f. solitarius, well separated from all the somatic sensory systems which are assembled more superficially. This segregation obviously has arisen because of the radical differences in the courses taken by the efferent fibers from visceral and somatic receptive fields to visceral and somatic effectors, respectively.


In general, the gustatory fibers tend to end near their entrance into the brain, and the general visceral fibers to descend toward the lower end of the system. In elasmobranchs the nucleus of the f . solitarius is locally enlarged, with a separate lobe for each of the nerves of the gills. These enlargements, which show as a beadlike row in the wall of the fourth ventricle, are probably chiefly gustatory. In the carp and some other teleosts with enormous numbers of taste buds, there are separate enlargements of this nucleus known as facial, glossopharyngeal, and vagal lobes. These are known to be largely gustatory in function. In other species of teleosts there are various modifications of these arrangements. In some birds with very few taste buds the f . solitarius is clearly double. A very slender medial bundle carries the few gustatory fibers and the much larger lateral bundle, the general visceral fibers (Ariens Kappers, Huber, Crosby, '36, p. 370). In Amblystoma, as in mammals,. none of these specializations have occurred, and the visceral sensory system as a whole retains its primitive characteristics.

Somatic Motor Nerve Roots

These roots in Amblystoma comprise only fibers for the extrinsic muscles of the eyeball in the roots of the III, IV, and VI nerves. As previously mentioned, all peripheral motor neurons are mingled with those of the motor tegmentum and are usually indistinguishable from them except in cases where their axons can be followed into the nerve roots. The cells of the nuclei of the eye-muscle nerves are fairly clearly segregated, and in some reduced silver preparations they react specifically to the chemical treatment (fig. 104) ; but even here their dendrites are widely spread and intertwined with those of tegmental cells, so that both kinds of neurons would appear to be similarly activated by the neuropil within which they are imbedded. The oculomotor nucleus lies in the posteroventral part of the peduncular gray (figs. 6, 18, 22, 24, 30, 31, 104). The nucleus of the IV cranial nerve lies about midway of the longitudinal extent of the isthmic tegmentum and far removed from the oculomotor nucleus (figs. 61, 104). The thick IV root fibers (most of them myelinated) ascend along the outer border of the gray to decussate in the anterior medullary velum in the usual way.


As mentioned in chapter xiii, the sensory zone of the isthmus contains cells of the mesencephalic V nucleus and others which send axons peripherally to meninges and chorioid plexus. Some of the latter go out with the IV nerve roots to unknown destinations. It is possible that some of these cells are secondarily displaced neurons of the motor IV nucleus, similar to those described by Larsell ('476) in cyclostomes. There is no definite evidence that this condition exists in urodeles; and, indeed, all connections of the cells lying within and adjoining the superior medullary velum require further study.


The floor plate of Amblystoma throughout its length contains a special type of ependymal elements and the cell bodies of some neurons. These neurons do not invade the floor plate from the basal plate, but they develop within this plate intrinsically, as was first pointed out by Coghill ('24, Paper III). In the adult medulla oblongata there are few of them at any one level, but they constitute a definite nucleus raphis, which is enlarged in some places, notably so in the interpeduncular nucleus. Most of the cells of the nucleus of the VI nerve are median, as in Necturus ('30, p. 14). These cells in ordinary preparations cannot be distinguished from others of the nucleus raphis except by observation of axons emerging in the VI nerve root. They are distributed sparsely in the ventral raphe and adjacent to it between the levels of the VII and IX nerve roots ('445, fig. 2). They emerge usually by two widely separated roots, though more rootlets are sometimes seen.

General Visceral Efferent Nerve Roots

Preganglionic fibers for unstriatcd muscles and glands leave the brain in the III, VII, IX, and X roots, probably with the IV nerve and its environs (p. 181) and perhaps with the parietal nerve (p. 235). In other vertebrates, fibers of this system have been described as leaving the brain with the optic nerve, with the nervus terminalis, and independently from other regions of the brain for the meninges. Our material is inadequate to reveal satisfactorily either the central connections or the peripheral courses of any of these fibers, so that this topic remains to be clarified. The large unmyelinated hypophysial nerve belongs in this system, as described on page 244.

Special Visceral Imotor Nerve Roots

The striated muscles related with the visceral skeleton of the head — jaws, hyoid, branchial arches, and their derivatives in higher animals — belong in a special category (p. 69). These muscles are visceral in phylogenetic and embryologic origin and primitively in function, but in all craniate Chordata they have acquired the same striated structure as somatic muscles, as well as various degrees of somatic function. They occupy, accordingly, an ambiguous position and are sometimes termed "special somatic muscles" ('22, '43). Their innervation is of similarly intermediate character. In Amblystoma these motor fibers are thick and well myelinated and arise from large cells of motor type which are more or less clearly segregated in separate nuclei. These nuclei lie laterally of the somatic motor nuclei and well separated from them.


This system of fibers is represented in the V, VII, IX, and X pairs of cranial nerves. Their peripheral distribution has been described by Coghill ('02). Their large motor nuclei are imbedded in the tegmental gray, with no clear boundaries. Their approximate positions in the larva are shown as projected upon the floor of the fourth ventricle in 1914«, figure 1; but, as seen in other figures of that paper, their dendrites ramify widely among those of the tegmental neurons. This indicates that both kinds of cells are activated from the same sources.


The motor V nucleus lies more laterally than the other members of this group. A Golgi impregnation of three of its elements is shown in figure 40. From it two roots arise, one from its posterior end and one farther forward. There are two well-separated motor nuclei and roots of the VII nerve, the roots emerging ventrally of the VIII root. The cells of the anterior nucleus are scattered among similar cells of the tegmentum near the level of exit from the brain. The posterior nucleus is farther spinalward and is the anterior part of a well-defined column of cells, which also includes the motor IX and X nuclei. The motor VII root fibers pass forward dorsally of the f. longitudinalis medialis (fig. 89) and turn laterally to emerge from the brain, as in Necturus ('30, p. 15). There is no visible boundary between the posterior motor VII and the motor IX and X nuclei.


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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

Reference

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


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