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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 XIV Interpeduncular Nucleus

The interpeduncular nucleus, like the habenula with which it is connected, is one of the most conservative structures in the brains of vertebrates, but in urodeles it has some characteristics which have not been reported elsewhere. The general features are outlined on page 46, and the details are described here, together with some speculations about the probable functions. The chief connections are shown very diagrammatically in figures 19 and 20, the spiral endings of the tractus habenulo-interpeduncularis in figure 50, the composition of the glomeruli in figure 84, and some typical connections of its neurons in figure 83.

Comparative Anatomy

This nucleus was discovered by Forel in 1872 and described in the rabbit in 1877, with confirmation by von Gudden in 1881 and Ganser in 1882. It is a constant feature in all vertebrate brains, much larger in some lower groups than in the higher. In urodeles it is a well-defined column of cells, embracing the ventral angle of the ventricle and extending from the fovea isthmi backward to the level of the V nerve roots. It is a ventromedian structure, differentiated in situ in the floor plate and the adjoining borders of the basal plates'. The fovea isthmi marks the anterior end of the embryonic floor plate as defined by Wilhelm His, and this plate is generally regarded as a nonnervous structure characterized by specially differentiated ependyma (Kingsbury, '30, p. 182) ; but Coghill ('24, Paper III) has shown that neuroblasts are differentiated here intrinsically. Some of these persist in the adult medulla oblongata as nucleus raphis, and between the fovea isthmi and the V nerve roofes this differentiation goes much further, producing the interpeduncular nucleus, as pointed out in my description of this nucleus of Necturus ('34c).


The differentiation is primarily isthmic, as was recognized by van Gehuchten ('00, 2, 199). In Amblystoma it extends spinalward into trigeminal territory, and below the level of the V nerve roots it is continuous with the nucleus raphis of the medulla oblongata. In cyclostomes the fasciculus retroflexus extends spinalward as far as the calamus scriptorius (Johnston, '02, p. 31 and figs. 8-16, 30). A mesencephalic sector of the nucleus, rostrally of the fovea isthmi, has been described in some vertebrates, and there is some evidence of this in Necturus ('34c) and Amblystoma. It has been found in some fishes, reptiles, and mammals; but in urodeles there is no group of differentiated cells in the midbrain comparable with this nucleus in the isthmus, and the secondary connections of mesencephalic terminals of fibers from the habenula are radically different from those of the habenulo-interpeduncular tract. In this account, accordingly, the description relates only to those structures spinal ward of the fovea which have habenular connection. This involves a terminological inconsistency, for in my analysis of the brain of Amblystoma the "peduncle" is defined as a strictly mesencephalic structure, and here none of the interpeduncular nucleus lies in the mesencephalon. Since this nucleus, however, is so obviously homologous with the structure so named in mammals, the mammalian name is retained.


The published description of the interpeduncular nucleus of Necturus ('34c) was based on insufficient material and evidently is incomplete. The structure there described is similar to that of Amblystoma but much simpler. Whether this simplicity indicates that Necturus is really more generalized (or more retrograde) or merely that the material available does not adequately show the actual structure cannot be determined. Probably both these suppositions are true. The more abundant Golgi material of Amblystoma reveals a wealth and intricacy of detail that baffle analysis, and much remains obscure. The exceptionally large and elongated nucleus in these animals is favorable for analysis, but the fact that all the connections are unmyelinated and dispersed in very dense neuropil makes accurate description impossible, except where elective silver impregnation isolates particular components. The erratic incidence of these impregnations and the well-recognized hazards of error in their interpretation necessitate great caution and restraint in drawing conclusions. Most of the observations here recorded have been seen in many preparations and can be adequately documented. Some of them, however, rest on slender and ambiguous evidence and require confirmation. The attempt to assemble these fragmentary observations into a coherent unity, such as is shown in figures 19, 83, and 84, is fraught with danger; and it is emphasized that these pictures and the physiological theories expressed are not regarded as final. They present my opinion of the things seen, subject to revision when information is more complete. A few years ago a brief summary of the observations made up to that time was pubhshed ('396, p. 584), and details were later added ('42, figs. 40-43). Here all these data are assembled, some errors in a brief reference in the paper of 1927 (p. 280) are corrected, and further observations and interpretation are recorded.

Histological Structure

In Weigert and cytological preparations the cells of this nucleus are densely crowded under and adjacent to the floor of the ventricle. Between the evels of the III and IV nuclei this gray column is thin. Ventrally of it there are, successively, the ventral median tegmental fascicles of group (1), the decussating fibers of the ventral commissure, and the superficial interpeduncular neuropil (figs. 60, 80-84, 92; '25, figs. 8, 9; '27, fig. 39; '42, figs. 30, 41-43). At the level of the IV nucleus the median fascicles, /.m.^.(jf), turn away from the midplane, and the texture of the ventral medial tissue posteriorly of this level is more open. Some of the cells of the interpeduncular nucleus lie more ventrally among strands of the ventral commissure (fig. 91). This gray is continuous dorsally on each side with that of the isthmic and trigeminal tegmentum, but in cell preparations the boundary is usually evident. Golgi sections show that at this boundary the cells are of transitional form, with some dendrites ramifying in the interpeduncular neuropil and others directed laterally into the alba of the tegmentum (figs. 61, 65, 66).

Ependyma

The description of the ependyma of Necturus ('34c, p. 118) applies with little change to Ambly stoma. The ependyma at the fovea isthmi is distinctive (fig. 79) and similar to that bordering the sulcus isthmi (p. 181). Posteriorly of this, the ependymal elements are of two forms. In and near the median raphe they are compact fascicles of thick, thorny fibers (fig. 70). More laterally (figs. 63, 64, 81), each element has a much more widely branched arborization of slender, thorny fibers, many of which end at the pial surface in bulbous enlargements. The external limiting membrane is apparently composed of these expanded ependymal terminal bulbs. Both these types of ependyma are seen in midlarval stages ('396, figs. 89, 94, 95).


The interpeduncular ependyma is an exceptionally dense mat of widely branched and closely interwoven fibers. Many of these branches do not reach the pial surface but arborize throughout the interpeduncular neuropil and especially within the interpeduncular glomeruli (described below), of which they form an integral part. The participation of specially modified ependyma in the formation of these glomeruli raises interesting questions. There is no obvious demand for unusual mechanical support here to account for especially strong ependymal framework, except perhaps in the median raphe, where the ependymal elements are more sturdy. Elsewhere in the interpeduncular field the slender ependymal fibers branch freely, and in the glomeruli they have tufted endings similar to those of dendrites, to be described shortly. This elaboration of the ependymal fabric within specialized synaptic fields suggests that the ependyma has some part to play in metabolism at the synaptic junctions.


Interpeduncular Neuropil

Ventrally of the interpeduncular gray and the commissure there is a sharply circumscribed area of very dense superficial neuropil, oval in cross-section, which in some of my published figures is marked nuc.inp. It is preferable to apply the word "nucleus" to the gray area only. This band of differentiated neuropil is, accordingly, currently called the "specific interpeduncular neuropil" (inp.n. or nucinp.n.), though it should be kept in mind that the entire interpeduncular field is permeated by neuropil, of which this is a specialized part. Its axonic component is a web of interlaced fibers, which is continuous with that of surrounding parts. Imbedded within this fabric are two specialized structures — the spiral terminals of the habenulo-interpeduncular tract and the glomeruli. The whole interpeduncular area is richly vascularized with capillary net and is a synaptic field of great importance. This activity evidently is especially concentrated in the glomeruli and the area of specific superficial neuropil.


The neuropil of the interpeduncular field is continuous dorsally with the deep neuropil of the gray of the isthmic and trigeminal tegmentum and laterally with the intermediate neuropil of the alba of these tegmental areas, as shown very inadequately in figures 60-66. Posteriorly it is continuous with the diffuse neuropil which pervades both the gray and the white substance of the medulla oblongata (figs. 79, 80, 81). In these drawings the structure of the neuropil is shown greatly simplified and schematized, for it is impossible on this scale of magnification to portray the intricacy of its texture. Since all nerve fibers related with the interpeduncular system are unmyelinated and most of the tracts are dispersed in the neuropil, analysis is very difficult and, indeed, impossible except when aided by elective impregnations. The interpretations given in the text and in the diagrams (figs. 19, 83, 84) are based on such evidence. The evidence is incomplete and in many preparations ambiguous, and attention is again called to the fact that the conclusions reached are tentative and subject to revision in detail. It is believed, however, that the main features of the histological analysis are based on adequate evidence and are reliable.

Glomeruli

Glomerulus-like structures have been known in the mammalian interpeduncular nucleus since 1877 (Forel). In Amblystoma these are small and very numerous elongated areas of very dense neuropil. They are distributed throughout the interpeduncular neuropil, in many places densely crowded; most of them are oriented vertically and extend downward into the ventral area of specific neuropil. Histological analysis of their structure is even more difficult than is that of the rest of the interpeduncular neuropil, for each of the constituent elements may present quite different appearances in Golgi sections, depending on the quality of the impregnation.


These glomeruli resemble in some respects those of the olfactory bulb ('246), though of much more complicated structure. In addition to the capillary net, there are three constituent elements: (1) a condensation of the ependymal framework as already described; (2) tufted terminals of dendrites ; and (3) tufted axonic terminals composed of thin contorted fibers interwoven with the dendritic terminals. Any one of these three constituents may be electively impregnated, or two or three of them may be seen in the same section. In some Golgi preparations the three components are so similar that they cannot be distinguished with certainty except where terminals can be followed to their connections outside the glomerulus, though when two of them are impregnated in the same section the difference betw^een them is usually obvious. In the preparation from which figure 66 was drawn, axons and dendrites are intermingled in each glomerulus. Only the dendritic component is drawn on the left side, and only the axonic component on the right. The visible tufted axons are from interpeduncular neurons.


Most of the glomerular dendrites come from cells of the interpeduncular nucleus, though some of them are branches from the transitional neurons at the ventral border of the tegmental gray. The axonic tufts, as far as observed, come from neurons of the interpeduncular nucleus, cells of the overlying tegmentum, and collaterals of fibers of tr. tegmento-bulbaris. No fibers from other sources seem to participate significantly in the formation of glomeruli. Many axons from the three sources mentioned do not enter glomeruli but arborize in the surrounding neuropil. Glomeruli with dendrites and axons derived chiefly from the interpeduncular nucleus tend to be disposed horizontally, the others vertically. The horizontal glomeruli have been illustrated from the larva ('396). Figure 58 of the paper cited shows two of the dendritic tufts, and figure 61 shows the axonic component of several of these horizontal glomeruli. Most of the horizontal glomeruli are imbedded in the general neuropil dorsally of the ventral specific neuropil. The vertical glomeruli generally extend downward into the specific neuropil, where they are penetrated by fibers of the interpeduncular spiral.


Neurons

In transverse Golgi sections the dendrites of the interpeduncular neurons are directed ventrally, passing through the ventral commissure. Within the interpeduncular neuropil they branch widely, and many of the branches have tufted endings in the glomeruli (figs. 19, 65, 66, 83, 84). Longitudinal sections show that the spread of these dendrites is much greater fore and aft than it is transversely (figs. 80, 81, 82; '396, figs. 57, 58), and the tufted terminals may be oriented either vertically or horizontally. Some of the cells of the isthmic tegmentum at the border of the interpeduncular nucleus may send dendrites into the interpeduncular neuropil, and these, too, may have tufted endings ('396, figs. 78, 95). Sagittal sections in which both interpeduncular dendrites and ependyma are fully impregnated give spectacular demonstration that the interpeduncular formation ends anteriorly at the fovea isthmi and isthmic sulcus. These interwoven elements directed anteroventrally form a dense mat, which ends abruptly at the locus of the sulcus isthmi. Posteriorly, the interpeduncular formation merges insensibly with the trigeminal tegmentum.


The slender axons of the interpeduncular neurons arise from the cell body or the base of the dendrite (figs. 65, 66, 70, 84; '396, figs. 61, 66) and immediately branch profusely. These fibers take tortuous courses within the interpeduncular neuropil and can be followed only when electively impregnated. In such preparations the longer branches are seen to be directed spinalward and to form the dorsal and ventral interpedunculo-bulbar tracts, as in Necturus ('30, p. 80; '34c, p 120).


Other branches spread widely in the general interpeduncular neuropil, of which they form an important component. Most of these fibers are dispersed, but some of them form compact longitudinal tufts within the glomeruli (fig. 84: 396, figs. 41, 61).

Afferent Connections

Fibers from remarkably diversified sources terminate in the interpeduncular neuropil. The widely branched terminals of some of these fibers spread diffusely ; the endings of others are specialized in diverse ways. The dominant member of this complex evidently is tr. habenulo-interpeduncularis, which is the chief component of the f. retroflexus as described in chapter xviii. The interpeduncular connections of this tract are similar in Amblystoma and Necturus ('34c).


Tractu.s habenulo-interpediaicularis. — The two bundles of unmyelinated fibers converge immediately below the fovea isthmi, and here most of their fibers decussate close to the ventral surface. Their f urthei- course is shown in figure 50. Immediately after crossing, each fiber reverses its course, and this is repeated so that a compact spiral is formed, which extends the entire length of the interpeduncular neuropil, diminishing spinalward. This spiral is coextensive with the specific interpeduncular neuropil and is its most characteristic feature. There are many series of sections cut in various planes in which this is clearly shown. In some of these, only one of the habenulo-interpeduncular tracts is impregnated (figs. 51, 52, 56, 57,. 58).


Figures 53 and 54 are drawn from a specimen in which tr. habenulo-interpeduncularis is impregnated on both sides at the origin in the habenula. The impregnation fails on the left side from the level of the dorsal thalamus downward. On the right side it is well stained as far as the decussation, below which only a few fibers are blackened, thus revealing clearly the courses of individual fibers, one of which is drawn in figure 54 through several turns of the spiral (cf. fig. 55). These fibers are slightly varicose and thorny. No specialized endings of any sort have been seen, and they have not been observed to branch except for occasional short forked terminals. The spiral penetrates the glomeruli, and its fibers are in synaptic connection with the glomerular dendrites.


Transverse sections show that the spiral is flattened dorsoventrally ('42, figs. 40-43). In the specimen from which these figures were drawn the spiral is fully impregnated, and few other fibers of the interpeduncular neuropil are stained so that the structure of the spiral is clear. No fibers leave the spiral to pass beyond the specialized interpeduncular neuropil. There is a small fascicle of uncrossed fibers at each lateral border of the sjjiral, and these a})parently enter the spiral at successive levels. Another series of transverse sections (no. 'i'iB'i) from the same lot of young adult s])ecimens shows almost identically the same structure.


Not all the habenulo-intcrpeduncular fibers enter the initial decussation. As mentioned above, a considerable fraction of them, including some of thicker caliber, descend uncrossed along the lateral borders of the interpeduncular neuroi)ih which they enter farther spinalward. In some preparations both crossed antl uncrossed fibers are imi)regnated, in some only the spiral fibers (fig. 50), and in one sagittal series only the uncrossed fibers are blackened (fig. S'i) . In the latter case the f. retroflexus is partially impregnated on each side for its entire length from the habenula to the interpeduncular nucleus. At the decussation none of the crossing fibers or the spiral fibers below it are darkened, but there is a large fascicle of uncrossed fibers, which descends laterally of the decussation and the spiral for almost the entire length of the interpeduncular nucleus. These fibers terminate within the interpeduncular neuropil among those of the unimpregnated spiral.


In 1894 van (iehuchten described thef. retroflexus of the trout. The origin in the habenula is similar to that of Amblystoma, and the course is the same. These fibers decussate in the interpeduncular nucleus and recross with much branching, but they do not form a compact spiral. They are varicose and have no specialized terminals. Simpler spiral terminals of mammals have been many times described (rabbit, von Gudden, '81; mole, Ganser, '82, p. 682; mouse, Ramon y Cajal, '11,2, 27-1; Calderon, '28; and many others).


Tractuff mamillo-i)ifi'rpeduncuIaris. — These fibers comprise group (2) of the tegmental fascicles ('3G, pp. 303, 338, figs, 3, 8). They arise in the dorsal part of the hypothalamus in company with similar fibers for the peduncle and tegmentum (figs. 19, 71, 79). The mixed bundle decussates partially in the retroinfundibular commissure, which is component 1 of the commissure of the tuberculum posterior (p. 302). The interpeduncular fibers, crossed and uncrossed, pass the fovea isthmi at the ventral surface close to the mid-plane and then descend along the lateral border of the specific interpeduncular neuropil (figs. 27-30, 60; '396, figs. 22, 41, 42, 57-61; '42, fig. 3), within which they end in open arborizations. They do not join the spiral or participate notably in the formation of glomeruli. Most of them end in the rostral half of the interpeduncular neuropil.


Tradus olfacto-pedujicularis. — This important component of the basal forebrain bundles (fig. 101; 'SOb, p. 534, figs. 1, 57), after contributing fibers to the hypothalamus and peduncle, continues spinalward along the lateral border of the specific interpeduncular neuropil. The endings of these fibers are similar to those of tr. mamillointerpeduncularis (figs. 18, 19, 21, 25-30, 53, 54, 59, 72, 82). This tract in the interpeduncular region lies laterally and dorsally of tr. mamillo-interpeduncularis, extending spinalward beyond the posterior end of the interpeduncular nucleus. There are some terminals of both this and the preceding tract in the dispersed interpeduncular neuropil.


Nervus terminalis. — In Necturus the longest fascicles of this nerve root probably reach the interpeduncular neuropil ('34c, p. 124). In Ambly stoma a small fascicle was observed by McKibben ('11, p. 270) to reach the "dorsolateral part of the hypothalamus and the interpeduncular region." Some of these fibers may connect with the interpeduncular nucleus, but this has not been demonstrated.


Tradus tegmento-ititerpedimcularis. — This is a very extensive connection, which takes two forms. There is, first, a system of short axons dispersed in the neuropil of the gray and the deep neuropil of the alba which arise from small cells of the dorsal, isthmic, and trigeminal tegmentum and descend directly to the interpeduncular neuropil. Some may come from the tectum. They are especially concentrated in the f. tegmentalis profundus (p. 286). A second type of connection is made by collaterals of the thicker axons of tr. tegmentobulbaris at their decussation in the ventral commissure.


1. The short tegmento-interpeduncular fibers of the first grouj) are unmyelinated. Their general arrangement is well shown in the sagittal sections, figures 79 and 80. They arborize in the neuropil of the gray of the interpeduncular nucleus and at all depths of the neuroj^il of the alba, forming an important component of the diffuse neuropil. Transverse sections show that, in addition to the diffuse spread of these fibers in the neuropil, there are also tufted endings which form part of the axonic component of the glomeruli (figs. 61, 62, 63, 66, 84).


2. The tr. tegmento-bulbaris cruciatus as described in the larva ('396, p. 590) is a series of thick axons of large cells of the isthmic and trigeminal tegmentum, which decussate dispersed in the ventral commissure and then descend in the ventral and ventrolateral fascicles of the medulla oblongata. Horizontal sections of one of these larvae show slender collaterals of these decussating fibers, which are directed posteroventrally into the interpeduncular neuropil and here have tufted endings in the interpeduncular glomeruli ('396, p. 600 and figs. 46 and 59). Figures 67 and 68 of the present work show similar collaterals, as seen in transverse sections from the same lot of larvae. Each compact glomerulus-like tuft contains terminals of several of these collaterals. Figure 69 shows similar collaterals in an adult brain. In this preparation only a few of these decussating fibers are impregnated, and these can be followed from section to section. Nothing else is stained here, so there is no opportunity for confusion. Figure 60 is from another adult specimen which shows some of these features more clearly, though the impregnation is less selective. This section is from the series illustrated in 1927 and is a few sections rostrally of figures 39 and 40 of that article. The tufted axonic terminals shown there are similar to the one seen in the present figure 60, and they are now known not to be derived from the mamillo-peduncular tract as there suggested ('27, p. 280).


Tertiary visceral-gustatory tract. — These fibers, as elsewhere described (p. 169), pass from the secondary visceral nucleus in the isthmus to the area ventrolateralis pedunculi. They lie close to the gray in the posterior lip of the sulcus isthmi and form one component of the complex f. tegmentalis profundus. Some fibers of this fasciculus decussate in the ventral commissure dorsally and spinalward of the decussation of the f. retroflexus, and here in some preparations there is evidence that fibers of the tertiary visceral tract turn spinalward to enter the interpeduncular neuropil. Several other systems of similar fibers are mingled here, and, in the absence of elective impregnation of this connection, its presence remains doubtful. Whether or not this direct connection exists, the visceral-gustatory system is related less directly with the interpeduncular nucleus by way of the hypothalamus. The secondary visceral nucleus is connected with the dorsal (mamillary) part of the hypothalamus and from here the large tr. mamillo-interpeduncularis may transmit visceral sensory and gustatory influences to this nucleus.


Other afferent fibers to the interpeduncular nucleus have been described in various animals. Gillilan ('41) reports that in bats and rodents the basal optic tract sends some fibers directly to this nucleus.


This connection may be present in Amblystoma also, though we have no demonstration of it.

Efferent Connections

The widely branched axons of the interpeduncular neurons apparently ramify throughout the entire interpeduncular field, and some of them pass beyond this field. The latter go out in three directions and are designated as three tracts named after their terminal connections — tr. interpedunculo-bulbaris dorsalis and ventralis and tr. interpedunculo-tegmentalis (figs. 19, 83, 84). All these efferent fibers go out in a web of mixed neuropil, within which the two bulbar groups are more or less clearly fasciculated in elective impregnations. The tegmental group of efferents are nowhere fasciculated, and we have no Golgi preparations in which they are electively impregnated.


Sagittal and transverse sections show that the interpeduncular neuropil extends dorsally into the isthmic and trigeminal tegmentum. Most of these fibers trend dorsoventrally, these comprising part of the mixed system, termed "fasciculus tegmentalis profundus." These fibers are marked f .teg. p. in the following figures: 29, 30, 31, 79; '42, figs. 30, 41, 42, 43. Elective impregnations have revealed some of the components of this fasciculus, including the brachium conjunctivum, tertiary visceral tract, and tr. tegmento-interpeduncularis. The latter is shown in figures 61, 62, 63, 65, and 66. These sections show also (though not clearly drawn in the figures) that from the interpeduncular neuropil a large number of fibers swing dorsolaterally into the alba of the tegmentum, where they engage dendrites of tegmental neurons. These fibers are interpreted as an interpedunculo-tegmental connection. In the light of the mammalian connections of the chief efi^erent tract from the interpeduncular nucleus to the dorsal tegmental nucleus discussed below, it seems probable that in Amblystoma the small-celled central nucleus of the isthmic tegmentum contains the precursor of the dorsal tegmental nucleus, though this evidently is only one of its relationships.


The interpedunculo-bulbar connections are clearly seen in our material. These fibers emerge from the diffuse interpeduncular neuropil in dorsal and ventral strands, which are connected with each other and with the surrounding neuropil, as shown in figures 79 and 81. The tr. interpedunculo-bulbaris ventralis descends for an undetermined distance at the lateral border of the interpeduncular neuropil and farther spinalward in the lip of the ventral fissure. The dorsal tract descends dorsally of the f. longitudinalis medialis (fig. 92). As pointed out below, this position of the dorsal tract agrees with that of the dorsal longitudinal fasciculus of Schiitz, and its fibers take a similar course, turning laterally to spread in the trigemino-facial tegmentum and as far back as the level of the motor nucleus of the IX nerve. In fact, the dorsal bulbar tract is really an extension posteriorly of the tegmental tract, for these comprise a continuous series of efferents to the tegmentum. The dorsal longitudinal fasciculus of Amblystoma is not a well-formed tract as in mammals, but comparable fibers can be recognized in the deep neuropil of the brain stem. In both lower and higher animals this complex seems to be concerned with general central excitatory state and disposition of the individual rather than with specific sensori-motor responses (pp. 208, 217). The inteipedunculo-tegmental and dorsal interpedunculo-bulbar system of fibers is evidently the primordium of an important component of the "caudal division of the dorsal longitudinal fasciculus" as described in the opossum by Thompson ('42), This morphological conclusion rests, I think, on sufficient evidence, whether or not the following physiological speculations can be confirmed experimentally.

Interpretation

Though much remains obscure, the main features of the histological structure and connections of the urodele interpeduncular nucleus are now clear, and these are assembled schematically in figures 19, 83, and 84. The most striking feature is the ventral plaque of specific neuropil containing spiral terminals of the habenulo-interpeduncular tract and glomeruli. Other afferent fibers enter both the specific and the diffuse interpeduncular neuropil and are so arranged as to permit their activation from almost all parts of the cerebrum. All these fibers come from areas of intermediate-zone type, not from primary sensory centers.


These afferents are of four general classes, depending on the source of their activation: (1) olfactory from the hemisphere, ending in the diffuse neuropil ; (2) olf acto-somatic from the habenula, ending in the specific (spiral) neuropil; (3) olf acto-visceral from the hypothalamus, ending in diffuse neuropil; and (4) tegmento-interpeduncular from the overlying tegmentum and ending in both diffuse neuropil and glomeruli. Those of the last class come from somatic sensory fields of correlation with no appreciable olfactory component. The glomeruli provide apparatus for nonspecific summation and reinforcement.


Each one of the other classes of afferents may have its own specific type of trans-synaptic transmission, depending on the histological and chemical structure and the strength and timing of volleys delivered.


Provision is thus made for discriminative responses to a considerable range of different kinds of activity that may be in process elsewhere in the brain — olfactory, visceral, somesthetic, and so on. The number of interpeduncular neurons activated and the temporal rhythm of their discharge may be determined not only by the algebraic sum of afferent impulses received but also by their timing. It is believed that this sort of analysis is characteristic of the nervous adjusters.


The outflow from the interpeduncular nucleus is distributed in part to remote regions and in part within the interpeduncular field, the latter providing apparatus for summation and intensification of the discharge. The remote effects of this outflow will depend on the location, structure, and connections of the motor pools entered by the efferent fibers.


The entire interpeduncular field is a well-circumscribed motor pool, in Sherrington's sense, in which every intrinsic nervous element is subject to activation by a wide variety of nervous impulses coming from diverse sources, each of which has a specific form of synaptic junction. The different structural patterns of these synapses presumably involve physiological differences in the type of activation. The dominant member of this complex of afferents evidently is the spiral of habenulo-interpeduncular fibers; every fiber of this tract may activate (or inhibit) every neuron of the nucleus, and, indeed, in successive turns of the spiral it may act upon several dendrites of the same neuron. There is no provision for separate localization of specific function here. The nucleus inevitably acts as a whole. But there is provision for summation of the effect in a large way. The diffuse neuropil also may act upon these neurons. Volleys may be discharged into it from many sources, each of which may reinforce (or inhibit) the activity instigated by the spiral.


Though temporal summation at an individual synapse is regarded as practically inoperative (Fulton, '43, p. 58), there is ample provision in this pool for spatial summation. The glomeruli present a series of difficult problems. Each of these small nodes of denser neuropil contains tufted dendritic terminals and tufted axonal terminals, and the latter come from two sources, intrinsic and extrinsic. The horizontal glomeruli seem to be especially adapted for summation of the discharge from the nucleus. If one of these neurons is experiencing sul)liminal activation, a collateral discharge from an active neuron may impinge upon it in a horizontal glomerulus, and the sum of the two excitations may be sufficient to fire the element. In a similar way, terminals of intrinsic fibers in the vertical glomeruli may reinforce the action of the extrinsic fibers. The glomerular activities may reinforce (or inhibit) those of the spiral, or conceivably they may act independently if the habenular component is inactive.


The observed structure seems to favor the supposition that, whatever may be the functions performed by this complex, they are of generalized type. The apparatus which patterns the specific reflexes, both somatic and visceral, is located elsewhere in the brain stem. The intrinsic structure of the interpeduncular field seems to preclude any well-defined local representation of different functions within it. The nucleus apparently acts as a unit, and any functional specificity that may exist would be in terms of differential excitation at the various forms of synaptic junction or of the functions of the motor fields into which its efterent fibers discharge. The ventral bulbar tract descends in the primary motor column of Coghill, and this suggests that it is in some way concerned with mass movements of the musculature of the trunk and limbs. The tegmental and dorsal bulbar efferent tracts form an aftatomical unit, and they probably are similarly related physiologically. These fibers discharge into a motor field within which the reflexes of the head are organized, notably those concerned with feeding. The interpeduncular complex seems to be so organized as to act as a whole without intrinsic localization of function. What part, then, does this complex play in patterned behavior?


In the first place, it is a noteworthy feature of the interpeduncular system that it is connected "in parallel," as the electrician would say, with the major systems of fore-and-aft conduction of the brain stem. The olfactory, optic, and lemniscus systems on the afferent side and the strio-pedunculo-bulbar systems on the efferent side, with their related centers of adjustment, seem to provide the apparatus which patterns overt behavior. The interpedunculo-habenular system is in addition to this apparatus and in some way ancillary to it.


In noncorticated vertebrates the activators of the motor zone receive their nervous excitations mainly from three regions which are physiologically distinctive: (1) the somatic sensory field of the tectum and dorsal thalamus, (2) the visceral field of the hypothalamus, and (3) the olfactory field of the cerebral hemispheres. The parts of this primary activator system of the cerebrum are interconnected, and all are represented in the higher adjusters of the hemispheres.


The interpeduncular complex is separate from this great system of activators except at its upper and lower ends. It is activated from the same three physiologically distinctive regions, and its efferent impulses are discharged into the same lower motor fields. These relationships are in some respects similar to those of the cerebellum with the activators of the skeletal musculature. The cerebellum does not pattern behavior, but it acts upon the motor systems as going concerns, facilitating the activity in process by reinforcement and inhibition, appropriately placed and timed. The structure and connections of the interpeduncular nucleus suggest that it is similarly related with the great descending (extra-pyramidal) systems of the cerebrum, and specifically with those concerned in the feeding reactions.


In the light of Coghill's definition of the amphibian reflex "as a total behavior pattern which consists of two components, one overt or excitatory, the other covert or inhibitory," and making application to a specific problem of the general discussion of reflex and inhibition in chapter vi, an attractive hypothesis might be framed along the following lines:


The brain stem may be conceived as a labile, equilibrated, dynamic system, within which the excitatory and inhibitory components are balanced against each other in reciprocal interaction at every successive phase of motor activity. The efferent activating systems of patterned behavior discharge through the basal forebrain bundles and the tegmental fascicles (fig. 6). Above and below this central core of activating fibers and parallel with them, there are inhibitory systems of fibers which have the same origins and terminations as do the activating systems but which pursue different courses with different connections. Dorsally there is an olfactosomatic inhibitory system centered in the habenula, and ventrally there is an olfacto-visceral inhibitory system centered in the mamillary region of the hypothalamus. Both these inhibitory systems converge into the interpeduncular nucleus (figs. 19 and 112). Here the inhibitory influences are integrated and distributed to lower motor centers as going concerns, in accordance with momentarily changing physiological requirements. Presumably not all components of the action system are under this sort of regulatory control by the interpeduncular complex, for, as pointed out below, there are other local fields with inhibitory functions.


The unusually large size of the interpeduncular nucleus of urodeles may be correlated with the fact that in the normal behavior of these animals total inhibition is a conspicuous feature (p. 77). Adopting Sherrington's terms, there is usually a long period of inhibition between the anticipatory and the consummatory phases of the reaction, notably in the feeding reflexes.


This hypothesis can have only academic interest unless and until it is confirmed by physiological experiment or clinical evidence, but it may have heuristic value as an indication of profitable points of attack in further exploration. From such scanty evidence as is now available, it seems to the writer to rest on an insecure foundation because it probably is an oversimplification of the problem. Our knowledge of the mechanism of central inhibition is so inadequate that inferences about physiological action from anatomical evidence alone are unsafe in this field, though such inferences are justifiable in many other fields where adequate physiological controls are available and have been made. Keeping these admonitions in mind, let us inquire further into the possible role that inhibition may play in the interpeduncular complex.


Though we do not know exactly how inhibition is effected in the central nervous system, we do know that in some parts of the brain the dominant function is activation, and in other parts it is inhibition. Current analysis of the primate cerebral cortex has revealed specific activating fields in the motor cortex and also specific inhibitory fields, the so-called "suppressor bands" (p. 79). In the stem the head of the caudate nucleus and the reticular formation of the upper medulla oblongata are also known to have inhibitory functions. That the interpeduncular nucleus is a similar field in which inhibition is dominant is a legitimate working hypothesis that can be tested experimentally. This, of course, does not imply that inhibition is the only function here localized, for inhibitory action is balanced against excitatory action in normal behavior. It follows that experimental disturbance of this normal balance may come to expression in so great a variety of ways depending on so great a variety of factors that it is difficult to devise crucial experiments.


This difficulty is illustrated by the published report of experiments by Aronson and Noble ('45) designed to localize in the brain the mechanisms which mediate specific components of the mating behavior of male frogs. In hundreds of experiments involving local ablations or transections, there were a few which gave clear-cut evidence of precise localization of function. In this connection Dr. Aronson writes me: "I believe that, while some activities, e.g., warning croak, ejaculatory response, and release of the female by the male at the termination of oviposition, are quite definitely localized, the mechanism controlling other phases of mating behavior are rather diffuse. In the latter cases more precise experiments w^ould, I think, demonstrate diffuseness rather than localization."

The authors' very conservative analysis of their protocols does reveal a few areas with local specificity of function. Among these is the clasp reflex, which is one of the most characteristic features of this mating behavior. Normally, the mating clasp is relaxed or inhibited immediately after oviposition, and this presumably involves inhibitory action. There is evidence that the primary center of this reflex is in the spinal cord and that the inhibitory phase is under some measure of cerebral control. Relaxation or inhibition of the clasp is quite consistently abolished by destruction of the preoptic nucleus or dorsal part of the hypothalamus, but this result does not consistently follow injury to the habenulae or interpeduncular nucleus. Though the clasp involves the use of skeletal muscles, the reflex as a whole is a visceral reaction related with oviposition and ejaculation of sperm. Cerebral control of the release of the clasp in the hypothalamus may be transmitted to the upper levels of the spinal cord by a direct pathway via tr. mamillo-tegmentalis and ventral tegmental fascicles of group (3), as described on page 278, without involvement of the interpeduncular complex. But Dr. Aronson would not limit the inhibitory influence resulting in release to this pathway. Again in personal correspondence he says: "While the spinal clasp center might be quite limited, the mechanism inhibiting or modifying the spinal clasp reflex is very diffuse, especially in the midbrain and diencephalon The interpeduncular nucleus might well be involved here."


An interesting series of experiments on the Japanese toad reported by Kato ('34) reveals an inhibitory center for the muscles of the contralateral limbs in a region described as "on the anterior end of the lamina terminalis," but not accurately defined. The diagrammatic figures seem to place it in the region of the anterior commissure between the septum and the preoptic nucleus. The efferent pathway from this center decussates in the vicinity of the interpeduncular nucleus. Further information about the connections and physiological significance of this center is desirable.


These experiments yield no crucial evidence of participation of the interpeduncular nucleus in the components of mating behavior under investigation or of movements of the limbs in general. This nucleus may play a more specific part in some other types of behavior; and some experiments indicate that this is true.


The only direct experimental evidence about the functions of the interpeduncular nucleus of mammals known to me is a recent note by Bailey and Davis ('42a) in which they describe a "syndrome of obstinate progression" in cats following destruction of this nucleus. This is a locomotor impulsion, which continues without remission until the death of the animal. Mettler and Mettler ('41) have produced similar symptoms by lesions involving the head of the caudate nucleus, and more recently Mettler ('45, p. 180) describes in primates a direct connection from the globus pallidus to the interpeduncular nucleus. The caudate is supposed to be one link in a chain of conductors with inhibitory functions (Fulton, '43, p. 456) and the syndrome following the destruction of the interpeduncular nucleus suggests to me that this nucleus also may be an inhibitor. The "obstinate progression" may then be interpreted as a release phenomenon.


In mammals efferent fibers from the interpeduncular nucleus have been described with distribution to neighboring parts of the brain stem, of which by far the most important is the large pedunculotegmental tract to the dorsal tegmental nucleus and the related dorsal longitudinal fasciculus of Schiitz. In the recent study of this fasciculus of the opossum by Thompson ('42), she describes this interpeduncular connection as an important component of it. In this marsupial the dorsal longitudinal fasciculus is a complicated system of fibers, chiefly descending, connecting the deeper areas of gray between the diencephalon and the spinal cord.


The structure and connections of the dorsal longitudinal fasciculus suggest general functions of some sort rather than control of local reflexes. Another series of experiments by Bailey and Davis ('42) shows that this fasciculus has some activating function which is essential for maintenance of normal motor behavior. They succeeded in destroying by electrocautery the periaqueductal gray of cats without injury to surrounding parts. This lesion must have involved the dorsal longitudinal fasciculus and the dorsal tegmental nucleus. If the injury is slight, the cats on awakening from the anesthetic are very wild and active but after a few days recover normal behavior. This seems to be an irritative excitation. If the lesion is extensive, the cats "lie inert, silent and flaccid as a wet rag." They never again show any spontaneous activity, though after a few days placing reactions are elicited normally and, if stimulated, they may walk slowly.


If now it is assumed that the dorsal longitudinal fasciculus contains fibers which normally transmit some sort of continuous nonspecific activating or facilitating influence upon the entire motor field of the lower brain stem — an influence which is essential for effective co-ordination and integration of these local systems of synergic muscular activity — then the destruction of this pathway would leave the animal helpless. This is not a flaccid paralysis, because the animal ultimately regains control of righting and placing reactions and even co-ordinated locomotor movements. All initiative and spontaneous activity are permanently lost because the animal is deprived of some essential component of the integrating apparatus. The "obstinate progression" that follows destruction of the interpeduncular nucleus may result from loss of an essential inhibitory influence normally acting upon the dorsal tegmental nucleus and the f. longitudinalis dorsalis. Loss of this influence allows the remaining apparatus of facilitation in the f. longitudinalis dorsalis to "race" like a steam engine deprived of its governor, and in this particular setup of conditions the result is uncontrolled progression.


In Rabat's ('36) study of alterations in respiration resulting from electrical stimulation of cats, it was reported that stimulation of the periaqueductal gray and of diencephalic regions known to contribute fibers to the dorsal longitudinal fasciculus was followed by increase in rate and amplitude of respiration. Shallower and unusually slower breathing followed stimulation of the habenula and habenulointerpeduncular tract.


Detwiler has shown (p. 6'2) that in Amblystoma a nonspecific mesencephalic influence is essential for the maintenance of motor efficiency. This is in addition to the action of the apparatus which activates patterned behavior, the latter maturing earlier and quite independently of cerebral influence. This mesencephalic influence in the amphibian brain seems to be comparable, in a general way, with the activating function of the dorsal longitudinal fasciculus of mammals.


These fragmentary observations cannot justify any final conclusions, but they support the working hypothesis that the habenulointerpeduncular complex is balanced against the strio-pedunculobulbar and f. longitudinalis dorsalis systems, the latter being the activating members and the former the inhibiting member of a dynamic system adapted to insure co-ordinated action of specific synergic systems of muscles.


It is evident that in macrosmatic animals the olfactory system is dominant in the interpeduncular complex. It is the chief functional component of the stria medullaris thalami, habenula, and f. retroflexus and probably also of the f. longitudinalis dorsalis, though all these structures survive its absence in anosmic animals. In Ichthyopsida the olfactory system is dominant in the hypothalamus. Attention has been called (p. 99) to the double role played by the olfactory system in the cortical activities of macrosmatic mammals; that is, in addition to the specific olfactory functions, there is a nonspecific facilitation by activation or inhibition of other cortical activities. This conception of the nonspecific facilitating action of the olfactory cortex may be extended into the subcortical field also, and in the interpeduncular complex the dominant part played by olfaction is probably of this nonspecific nature.

Conclusion

The hypothesis here tentatively suggested divides the adjusting apparatus of the brain into two reciprocally interacting components, the one a system of activators, the other a system of inhibitors. In the normal patterning of behavior these systems are balanced one against the other. In the brains of primitive vertebrates the dominant highest center of correlation of the exteroceptive sensory systems lies in the tecto-thalamic sector and of the interoceptive systems in the hypothalamus. From both these regions the activating fibers converge into the ventral thalamus and motor zone of the jnidbrain and isthmus, where they are joined by olfactory fibers and others from the supra-sensory centers of the hemispheres. Above and below this central core of activating fibers are two systems of inhib


INTERPEDUNCULAR NUCLEUS 211

itors — the olfacto-somatic system in the habenula and the olfactovisceral system in the hypothahimus — both of which discharge into the interpeduncular nucleus. The efferents from this nucleus reach the same lower motor centers as do the efferents of the activating systems.


In all macrosmatic species, and especially in those of more primitive groups, the olfactory system is dominant in the forebrain, and in all groups it plays an important part in nonspecific activation and inhibition. In lower groups the deep neuropil of the gray substance is a diffuse activator, and this sytem survives in mammals as the dispersed periventricular fibers which converge to descend in the f. longitudinalis dorsalis of Schiitz. Associated with this fasciculus is the dorsal tegmental nucleus, which receives inhibitory fibers from the interpeduncular nucleus. This complex discharges nonspecific activating and inhibiting impulses into the bulbar tegmentum, and these play an essential part in the maintenance of the appropriate balance between activation and inhibition in all muscular activity. The destruction of any major component of this equilibrated dynamic system may result in pathological behavior which has no counterpart in the normal animal but which may furnish clues pointing the way toward successful analysis.


Though, as suggested above, this schematic outline is doubtless oversimplified, the hypothesis or some variant of it may suggest profitable lines of experiment. For this purpose the urodeles, with great enlargement and elongation of the interpeduncular nucleus, are favorable subjects. The larger species, like Necturus and Cryptobranchus, can be operated upon more conveniently than can the salamanders and frogs, though their more sluggish behavior may make interpretation more difficult.


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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

Reference

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


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