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

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Chapter XVIII The Habenula and its Connections

IN ALL vertebrates with fully evaginated cerebral hemispheres the deep transverse stem-hemisphere fissure separates the dorsal parts of the hemisphere from those of the diencephalon. Ventrally of the floor of this fissure there are two great systems of fore-and-aft conduction — the basal forebrain bundles and the stria medullaris thalami. These form a superficial ventrolateral eminence, which is more conspicuous in the frog, where it was termed by Gaupp the "prominentia fascicularis." Attention has been called to the fundamental difference between these two great systems of fibers. The basal bundles are concerned primarily with the patterning of behavior, and, accordingly, their composition and connections vary widely from species to species in conformity with diverse modes of life. The composition of the stria medullaris, on the other hand, is remarkably constant throughout the vertebrate series, and its functional role is obscure. This chapter is devoted to these fibers and their widely dispersed connections, together with a few other systems of fibers which are associated with them.

THE DI-TELENCEPIIALIC JUNCTION

All afferent fibers to the habenula, with the exception of the tectohabenular tract, enter the stria medullaris thalami for longer or shorter parts of their courses. These fibers are assembled from all parts of the cerebral hemisphere and preoptic nucleus and, in smaller number, from the thalamus. They form a massive fasciculus, which ascends vertically in the posterior lip of the stem -hemisphere fissure; and associated with them is a series of bed-nuclei at the di-telencephalic junction, which will next be described. These nuclei have diverse and complicated connections, and all have this in common, that they are in functional relations with the stria medullaris. The following are listed in this series; for their arrangement see figure 2B.

1. Preoptic nucleus. — Among the connections of this nucleus, as described in the preceding chapter, are terminals and collaterals of descending fibers of the nervus terminalis, medial forebrain bundle, precommissural fornix, stria terminalis, and ascending fibers of the medial bundle. Fibers ascend from all parts of this gray to the habenula in the stria medullaris, some externally of the lateral forebrain bundle (tractus olfacto-habenularis lateralis) and some medially of it (tr. olfacto-habenularis medialis) . Among these fibers are strong collaterals from both dorsal and ventral fascicles of the medial forebrain bundle ('396, p. 538).

2. Bed-nuclei of the anterior commissure (figs. 25, 26, 27, 97). — These are cells sparsely scattered in the anterior commissure ridge and massed laterally of it. They are related with tracts of the basal forebrain bundles decussating here, the stria terminalis, and the tr. septo-habenularis .

3. Nucleus of tr. olfacto-habenularis (figs. 27, 28, 29, nuc.tr. ol.h.; '35a, p. 250; '396, p. 538).— This gray is interpolated between the anterior commissure ridge, the anterodorsal part of the nucleus preopticus, the anterior end of the ventral thalamus, and the eminentia thalami. It is penetrated by fibers of the tr. olfacto-habenularis medialis, with which it is related by terminals and collaterals. It is also connected with the amygdala by dispersed thick fibers, some of which are myehnated, termed "tr. amygdalo-thalamicus," though the direction of conduction is unknown (shown but not named on figs. 19 and 30; also shown on fig. 96, where the nucleus of the tr. olfacto-habenularis medialis is marked, p.v.th.). This tract is probably a part of the complicated stria terminalis system. It was described in Necturus ('336, p. 218) as connected with the nucleus of Bellonci, but its main connection is with the nucleus of the olfactohabenular tract, as shown in figure 40 of the paper cited. Impregnated neurons of the posterior part of this nucleus are shown in figure 24 of the paper of 1942. Their unmyelinated axons take widely divergent courses — to the stria medullaris, the amygdala, medial and lateral forebrain bundles, and the ventral thalamus.

In describing the early development of both dipnoan and amphibian brains, Rudebeck ('45) recognizes two parts of the nucleus preopticus: (1) an inferior "nucleus preopticus proper," most of which is developed rostrally of the sulcus intraencephalicus anterior, and (2) a pars superior, developed posteriorly of this sulcus in the ventral part of the di-telencephalic ridge. The superior part he regards as the primordium of the amygdala of the adult amphibian. This part is larger in dipnoan embryos than in amphibians and may be the source of a more extensive area of the adult brain. In Amblys

THE HABENULA AND ITS CONNECTIONS 249

toma the posterior lobe of the inferior or "proper" nucleus preoptions develops posteriorly of the sulcus intraencephalicus anterior; and, more dorsally, Rudebeck's pars superior of this nucleus is clearly the primordium of my nucleus of the olfacto-habenular tract, including, perhaps, also the posterior end of the amygdala. In any case the two nuclei last mentioned are very intimately related.

4. Eminentia thalami. — This name was given ('10, p. 419) to a prominent ventricular eminence lying behind the interventricular foramen between the anterior commissure ridge and the habenula, which has been variously interpreted by authors. It is appropriately named "nucleus commissurae hippocampi" by Addens ('46). I have regarded it as the anterior end of the ventral thalamus, differentiated as bed-nucleus of several large tracts which converge here. It is well defined in early swimming stages (area 7a) , when the first fibers of the stria medullaris are visible ('38, p. 213 and figs. 18, 19) ; and in early feeding stages, with good development of stria medullaris and hippocampal commissure, it has acquired essentially adult form ('386, p. 401, figs. 1, 2, 6). It is derived from the middle of the di-telencephalic ridge of Rudebeck's ('45) pictures of the embryonic brain.

This eminence receives collaterals from the stria medullaris and in larger numbers from the fibers of the hippocampal commissure (figs. 31, 32, 71, 76; '27, p. 294; '35a, p. 250). As the latter fibers swing downward behind the interventricular foramen toward their crossing in the anterior commissure ridge, they are accompanied by similar fibers which pass from the primordium hippocampi to the ventral thalamus — tr. cortico-thalamicus medialis (figs. 31, 32, 33, 72, 75). Like the fibers of the hippocampal commissure, these are mostly unmyelinated, with a few thick, well-myelinated fibers scattered among them. Many of them end in the eminentia thalami, and others continue into the anterior part of the ventral thalamus. This tract is probably the precursor of the mammalian column of the fornix, though here none of its fibers have been seen to reach the hypothalamus.

Numberless short, thin, unmyelinated axons descend from the small cells of this eminence to spread in the adjoining ventral thalamus ('21a, figs. 26-28; '27, p. 269), and thicker axons enter the complex crossed and uncrossed system of tr. thalamo-tegmentalis ventralis ('39, p. 120 and fig. 2; '396, p. 546; '42, p. 225).

5. Nucleus of Bellonci. — This name is applied to a group of cells which form a low ventricular eminence between the anterior parts of the dorsal and the ventral thalamus. I have regarded it as part of the dorsal thalamus, though its morphological status is uncertain. This nucleus was not recognized by Bellonci ('88), hut he did describe in the frog a peculiar field of very dense neuropil related with it, which I term the "neuropil of Bellonci" in preference to his name, nucleus anterior superior corporis geniculati thalami." This nucleus and associated neuropil I first described in Necturus ('17, p. 243) under the name of "pars optica thalami," but this term also is inappropriate and has been discarded. In Necturus and Ambly stoma this peculiar neuropil receives terminals and collaterals from the optic tract, stria medullaris, tr. cortico-thalamicus medialis, the anterior tectal fasciculus (p. 297), and other sources. Axons of the cells of the nucleus go to the habenula and to the ventral thalamus and peduncle. This neuropil has received much study ('25, p. 454; '27, p. 295; '33&, p. 216; '34, p. 107), but, as recently remarked ('42, p. 279), many details of its structure and connections are still obscure. The probable equivalent of this nucleus has been found in all major groups of vertebrates by Addens ('46 and papers there cited).

6. Habenula. — The general structure and chief connections of the amphibian habenular nuclei are well known and have been summarized by Ariens Kappers, Huber, and Crosby ('36). There are two habenular nuclei on each side, different in position from that of mammals but with similar fibrous connections. They are arranged one above the other at the anterodorsal border of the diencephalon, dorsally of the eminentia thalami. The taenia thalami, or line of attachment of the membranous dorsal sac, extends from the eminentia thalami along the anterior border of both nuclei and backward along the dorsolateral border of the dorsal nucleus as far as the habenular commissure. Posteriorly of this commissure the roof is again membranous as far as the recessus pinealis. The dorsal and ventral nuclei are separated on the ventricular surface by a shallow sulcus intrahabenularis and bounded posteriorly by the sulcus posthabenularis, which is the surviving dorsal end of the sulcus diencephalicus ventralis of Rudebeck ('45). Below the ventral nucleus is the deep sulcus subhabenularis. This is essentially the embryonic arrangement, in contrast with that of adult man, where the great enlargement of the dorsal thalamus and reduction of the membranous dorsal sac and paraphysis result in great changes in the relative positions of parts.

The ventral and dorsal habenular nuclei of Amblystoma are probably the equivalents, respectively, of the lateral and medial nuclei of

THE HABENULA AND ITS CONNECTIONS 251

higher forms, but the details of their connections are not exactly comparable. Both nuclei receive terminals of the stria medullaris thalami (apparently all components of it), and the chief efferent path of both nuclei is the tr. habenulo-interpeduncularis, which is the largest component of the fasciculus retroflexus (of Meynert). The dorsal nucleus is connected with the tectum and pretectal nucleus by fibers running in both directions, and the ventral nucleus is similarly connected with the dorsal thalamus, the ventral border of the tectum, and the dorsal tegmentum.

In the ventral habenular nucleus the nerve cells are relatively few in the usual arrangement at the ventricular side. The alba is almost completely filled by the massive stria medullaris, internally of which is neuropil, which invades the gray substance. Most of the cell bodies are widely separated within this dense neuropil. The larger dorsal nucleus has very numerous small cells, densely crowded on all sides except dorsally of the commissure. This layer of cell bodies incloses a central core of dense neuropil, which connects with the stria medullaris below and the habenular commissure above. The thick contorted dendrites ramify in the central neuropil (fig. 73; '42, figs. 77, 79).

Primitively, these nuclei had direct connection with the parietal eye, as is the case in some still living species. It is possible that in some early ancestor of the vertebrates, now extinct, the dorsal parietal eye was better developed than the lateral eyes and that for this reason the primordial olfacto-visual correlation was made in the epithalamus rather than in the tectum of the midbrain.

The habenular system is one of the most conservative parts of the vertebrate brain. Edinger's statement ('11, p. 370) that this is perhaps the only part of the brain the organization and connections of which show no alterations during the whole course of vertebrate phylogeny requires some qualification; yet, as we pass from cyclostomes to man, with revolutionary changes in all surrounding parts, the chief habenular connections show a surprising uniformity.

In urodeles afferent fibers enter the habenula from all parts of the cerebral hemisphere, except perhaps the olfactory bulb (some authorities would not make this exception) and also from the preoptic nucleus, thalamus, and tectum. The largest of these tracts come from areas which are under the strongest olfactory influence, and the habenular complex is generally regarded as primarily concerned with olfactory adjustments. That this is not its only function is evident from the fact that in anosmic animals, like some birds and cetaceans, the habenular system, though reduced in size, retains most of its components. The associational connections of the habenula with the tectum, dorsal thalamus, and adjacent regions justify the conclusion that the complex, viewed as a whole, is adapted to insure the correlation and integration of the activities of all parts of the olfactory field with those of all other exteroceptive systems.

The sense of smell is both interoceptive and exteroceptive. Olfactory nervous impulses of exteroceptive type are somehow sorted out from the entire olfactory field and converged into the epithalamus, and those of interoceptive type are similarly converged into the hypothalamus. In the former of these areas they may be correlated with all relevant somatic sensory experience, and in the latter with the sum total of visceral experience. The habenula discharges into that portion of the motor field known to control the activities of the skeletal musculature and chiefly into the interpeduncular nucleus, which is imbedded within this motor field and articulated with it in very complex patterns (chap. xiv). The olfacto-visceral correlations of the hypothalamus may come to expression in overt action of the skeletal muscles or in less obvious visceral changes. The chief nervous pathways involved in the overt responses can be identified, but those of visceral activities are still obscure. There is a strong connection from the hypothalamus to the interpeduncular nucleus.

Since both the hypothalamic and the epithalamic olfactory systems are large in all vertebrates, it was suggested by Edinger ('11, p. 371) that these regulate the feeding activities, or muzzle reflexes {Oralsinnapparat) — dorsally the exteroceptive components and ventrally the interoceptive. This attractive hypothesis seems to explain the different courses and connections of the medial forebrain bundle and stria medullaris, but it leaves out of account the equally large lateral forebrain system. Moreover, the chief connections of the medial and lateral forebrain bundles are localized in the hemisphere, respectively medially and laterally of the ventricle; but the habenular connections are drawn equally from both sides of the hemisphere. The habenular connections seem to be of a different kind, something added to an existing adequate provision for both visceral and somatic adjustments.

The chief efferent discharge from the habenula is to the interpeduncular nucleus, and there is a large efferent tract from the hypothalamus to this nucleus (figs. 18, 21). It is suggested in chapter xiv that the habenulo-interpeduncular system is the inhibitory com

THE IL\BENULA AND ITS CONNECTIONS 253

ponent of an equilibrated dynamic system, of which the basal forebrain bundles comprise the activator component. On this hypothesis the activation of all olfacto-motor systems goes out through the basal forebrain bundles, and this activation is accompanied by an inhibition of all conflicting activities, the inhibitory component of the reaction being centered in the interpeduncular nucleus. This implies that inhibitory influences derived from exteroceptive fields are transmitted to the interpeduncular nucleus by the f . retroflexus and from interoceptive fields by the mamillo-interpeduncular tract. This hypothesis seems to be consistent with the known structure, but it lacks experimental proof. If there is factual basis for it, the activating and inhibitory systems must not be regarded as independent units of structure; they are everywhere interconnected, and all their activities are balanced one against the other in an integral dynamic system. The literature contains many fragmentary accounts of the habenular connections of Amphibia, with some conflict of observation and confusion of nomenclature. When these descriptions are assembled, together with additional observations here reported, the salient features of the habenular connections may be grouped into three classes. These are:

1. There are two groups of commissural connections between the two cerebral hemispheres. Group 1 comprises the commissura superior telencephali, with fibers from the anterior olfactory nucleus, piriform area, and amygdala (components 3, 4, 5, and 6 of the list given on pp. 257-60). This is the larger part of the habenular commissure. It was seen by van Gehuchten in Salamandra ('97rt), though its true origins were not recognized and his belief that none of these fibers have connection with the habenular nuclei needs confirmation. Group 2 is the com. pallii posterior (component 8 of the list). These fibers come from the primordium hippocampi and are probably comparable with the com. aberrans of some reptiles.

2. The habenula is an important way-station for through traflSc from all parts of the cerebral hemisphere and preoptic nucleus to the brain stem below this level, particularly to the peduncle and interpeduncular nucleus. All these conduction pathways except the commissural fibers are interrupted by synaptic junctions in the habenula, and the habenular synaptic field is connected with neighboring regions by fibers passing in both directions.

3. The through traffic is influenced by these local connections with areas of the sensory zone concerned primarily with exteroceptive functions. The habenula, accordingly, may be regarded as a bednucleus interpolated in one of the main pathways from higher centers of correlation, where olfaction as an exteroceptive function is integrated with other functions of this type and transmitted to lower centers in the motor zone, where patterns of response are organized. The hypothalamus is a similar way-station for through traffic from the same higher centers to lower motor fields, with olfacto- visceral functions dominant.

Most of the afferent connections of the habenula are in the stria medullaris, and most of the efferent connections in the f. retroflexus. Before describing this chief thoroughfare of through traffic, mention should be made of two systems of fibers which are in intimate functional relation with the stria medullaris, though not component parts of it. These are the fornix and stria terminalis.

In mammals this name is given to a complicated system of fibers which descends medially from the hippocampal formation to the underlying brain stem in two groups separated by the anterior commissure. Both groups descend within or adjacent to the lamina terminalis dorsally and rostrally of the interventricular foramen. The postcommissural fornix, commonly called columna fornicis, passes downward between the foramen and the anterior commissure and thence across the thalamus to end chiefly in the mamillary body. The precommissural fornix is a complex system of more loosely arranged fibers descending in front of the anterior commissure to the gray of the septal nuclei and neighboring parts and continuing spinalward in the medial forebrain bundles to preoptic nucleus, hypothalamus, and (according to some descriptions) as far as the cerebral peduncle.

Primordia of the two main divisions of the mammalian fornix are obviously present in the amphibian brain, but the topography of the region of the lamina terminalis is here so different that these tracts take peculiar courses. The anterior and hippocampal commissures cross, not in the lamina terminahs, but in a commissural ridge behind the interventricular foramen (fig. 2; '27, p. 235; '35, p. 299). To reach this crossing, the fibers of the massive hippocampal commissure swing downward behind the foramen (figs. 72, 76), and here they are accompanied by the fibers of tr. cortico-habenularis medialis and tr. cortico-thalamicus mediahs (fig. 20, nos. 8 and 9), which, as pointed

THE HABENULA AND ITS CONNECTIONS ^55

out in the preceding description of the eminentia thalami, marks the beginning of the differentiation of the mammahan columna fornicis. Some of these fil)ers are collaterals of those of the com. hippocampi and tr. cortico-habenularis medial is. In Ambly stoma none of these fibers have been followed as far as the dorsal (mamillary) part of the hypothalamus, so that the homology with the mammalian postcommissural fornix is incomplete. In other urodeles it has been described as reaching the hypothalamus (Rothig, '24, pp. 10, 15; Salamandra, Kreht, '30, p. 252). The precommissural fornix is an ancient system, being well developed in many fishes. In Ambly stoma it is large and of typical pattern. These fibers descend from the hippocampal formation rostrally of the foramen to the medial forebrain bundle (figs. 98, 99), within which they descend for an undetermined distance.

' The transverse sections described in 1927 revealed clearly the relations of the precommissural fornix ('27, p. 311), but the postcommissural connections were obscure. In Necturus these connections are perfectly clear, and the morphological relations of precommissural and postcommissural fornix fibers have been discussed ('336, p. 188). Amblystoma resembles Necturus. Accompanying the unmyelinated fibers of the hippocampal commissure there are similar fibers of tr. cortico-habenularis medialis and tr. cortico-thalamicus medialis, and among these are a few myelinated fibers. In the horizontal Cajal sections (figs. 28-32) the very numerous thin, fibers of this complex are not impregnated, but the thick axons are deeply stained. Few of the thick fibers decussate in the hippocampal commissure (figs. 28, 29, 30). Many of them ascend in the stria medullaris (figs. 32, 33, 34, tr.c.h.m.), and most of the others pass backward and downward through the eminentia thalami into the ventral thalamus and (probably) the preoptic nucleus (figs. 31, 32, tr.c.th.ni., 72, 75). These thick fibers and the much more numerous thin fibers by which they are accompanied I have termed "tr. cortico-thalamicus medialis." An extension of this tract into the hypothalamus would give the connection described by Kreht ('30) in Salamandra and by Loo ('31, p. 84) as tr. cortico-hypothalamicus in the opossum. The mammalian tr. cortico-mamillaris is a further addition to this system.

STRIA TERMINALIS

In mammals the ventromedial septal field is connected with the ventrolateral amygdala by fibers, passing probably in both directions, some ventrallv of the basal forebrain bundles (diagonal band of Broca) and some dorsally of them (stria terminalis, stria semicircularis, or stria cornea). Here the enormous enlargement of the basal forebrain bundles, particularly the internal capsule system of fibers, displaces the dorsal stria so that its course between medial and lateral ends is a wide arc, in some species almost a complete circle. At both of these terminal areas the stria makes complicated connections with the preoptic nucleus and hypothalamus, some of which were termed by Cajal the "olfactory projection tract." In Amblystoma, with smaller basal forebrain bundles, these fibers take more direct courses, and they are more dispersed so that there is no compact stria terminalis as in mammals. For description and illustrations of these tracts the reader is referred to my paper of 1927 (p. 302). The following connections have been described:

1. The com. amygdalarum, crossing in the anterior commissure

(fig. 97). '

2. The stria terminalis sensu strido (fig. 96), a massive connection passing downward from the amygdala medially of the basal forebrain bundles. Some of its fibers are directed rostrad toward the septal area, but most of them turn posteriorly in the dorsal fascicles of the medial forebrain bundle to reach the preoptic nucleus and dorsal part of the hypothalamus. The rostrally directed fibers of this group and the commissural fibers are comparable with the fascicles of the stria which in mammals follow the taenia semicircularis and tail of the caudate nucleus, arching over the internal capsule and connecting the amygdala with the septal field. None of the fibers of this tract are drawn in the figures of horizontal sections. At the levels of figures 27-30 the descending fibers accompany the tr. olfacto-habenularis medialis and then turn spinalward in the dorsal fascicles of the medial forebrain bundle. Accompanying these are shorter myelinated fibers which pass between the amygdala and the nucleus of the olfactohabenular tract— the tr. amygdalo-thalamicus (p.- 248).

3. The ventral olfactory projection tract, descending from the amygdala externally of the basal forebrain bundles. These fibers are shown but not named in figure 16 of 1927.

4. The dorsal olfactory projection tract (p. 242, figs. 19, 25, 26, 27, ol.p.tr.) .

STRIA MEDULLARIS TIIALAMI

In cyclostomes, with incomplete evagination of the cerebral hemisphere, the connections between the dorsal parts of the telencephalon

THE HABENULA AND ITS CONNECTIONS 257

and of the diencephalon are massive and direct ('22«, fig. 8), and the habenular tracts are not fasciculated to form a stria medullaris. With further evagination of the hemisphere in amphibians and the appearance of a deep stem-hemisphere fissure, the habenuhir connections of the palHal parts of the hemisphere must turn downward to pass under the floor of this fissure. Here they are joined by other habenular tracts to form the stria medullaris thalami. These tracts of Amblystoma were described in 1910 (and further details, '27, p. 284 and figs. 15-18; '396, p. 538), and now some corrections and additions can be contributed. Compare also my description of the habenular connections of Necturus ('336, pp. 204-14).

The components of the stria which have been identified in Amblystoma are shown in figure 20, where they are projected upon the median plane. The courses of four of the more lateral components are shown as projected upon the lateral aspect of the brain in figure 85. Their arrangement as seen in horizontal sections is shown in figures 25-36 and in sagittal sections in figures 74-78. Some components are electively impregnated in our Golgi preparations, and these specimens have been especially useful in demonstration of the truly commissural connections of several of the tracts listed below. Components 3, 4, 5, and 6 are known to decussate in com. superior telencephali and component 8 in com. pallii posterior. On the figures the components of the stria are numbered as in the following list:

1. Tractus olfacto-habenularis medialis.

2. Tractus olfacto-habenularis lateralis.

Most of the fibers of these two tracts are axons of cells of the preoptic nucleus, ascending, respectively, medially and laterally of the basal forebrain bundles (figs. 25-30, 74-77; '27, fig. 16; '42, figs. 18, 24), but some of them are collateral branches of axons of the medial forebrain bundle ('396, p. 538). This is doubtless true in Necturus also, though I was not able to demonstrate it ('336, p. 208). In the passage last cited, references are given to descriptions of this connection in other urodeles. The fibers of these tracts are assembled from all parts of the preoptic nucleus, ascending on both sides of the sulcus preopticus. The fibers of the medial tract pass through the gray of the nucleus of this tract, with many terminals and collaterals, and here the tract receives accessions from the nucleus. More dorsally both tracts have collateral connections with the eminentia thalami and neuropil of Bellonci. They form the most posterior component of the stria medullaris, and within the habenular nuclei they spread out in the neuropil. Wliether any of them cross in the habenular commissure has not been determined. A few of these fibers are myehnated.

3. Tractus olfacto-habenularis anterior, ventral division.

4. Tractus olfacto-habenularis anterior, dorsal division.

As shown in figure 85, these fibers arise chiefly in the medial sector of the nucleus olfactorius anterior, from which they diverge ventrally and dorsally in a medial fascicle of fibers, which I have called the "f. postolfactorius" (fig. 100; '27, p. 283, figs. 2-4). The fibers of this system which are directed ventrally (no. 3) arise also in the ventral sector of the anterior nucleus and the septum. They take a posterolateral course along the ventral surface of the hemisphere, turning dorsally at the level of the anterior commissure to enter the stria medullaris under the posterior pole of the hemisphere ('27, p. 284 and figs. 5-17, tr.ol.hah.ant.). In the stria they lie anteriorly of the tr. olfacto-habenularis (1 and 2) and posteriorly of the tr. corticohabenularis lateralis (5), as shown in sagittal sections (figs. 75, 76, 77, tr.ol.h.a.v.). In the horizontal sections (figs. 25-34) this tract is marked ir.ol.h.a. Some of these fibers terminate in the habenular neuropil, and some cross at the posterior end of the habenular commissure in the com. superior telencephali.

The dorsal fibers of this system (no. 4) cross from the medial to the lateral side of the hemisphere in the f. postolfactorius between the olfactory bulb and the anterior olfactory nucleus (fig. 5) and then turn posteroventrally across the lateral aspect of the hemisphere in company with the large tr. olfactorius dorsolateralis ('27, p. 284). Over the piriform area these fibers are joined by those of tr. corticohabenularis lateralis (no. 5), and the mixed fascicle enters the stria medullaris under the posterior pole of the hemisphere. In the stria the mixed fascicle 4 + 5 ascends anteriorly of no. 3, and at the boundary between ventral and dorsal habenular nuclei it splits into lateral and medial bundles. The lateral fibers are dispersed in the habenular neuropil, and the medial fibers decussate in the com. superior telencephali (figs. 74-77, tr.c.h.l.). This component is shown in horizontal sections in figures 30-34, and its entire course is seen in transverse sections in figures 6-17 of 1927 {tr.c.hah.L).

The anterior olfacto-habenular tract is the first component of the stria medullaris to mature in ontogeny, its fibers appearing in early swimming stages ('38, pp. 222, 238, figs. 10, 19); and its relations in cyclostomes indicate that it is very ancient phylogenetically ('336,

THE HABENULA AND ITS CONNECTIONS 259

p. 212). In Necturus the arrangement of these tracts is somewhat different ('336, pp. 210-13).

5. Tractus cortico-habenularis lateralis. These unmyelinated fibers, as just described, pass from the piriform and dorsal pallial areas in company with those of no. 4 (fig. 20) to the habenula, where the majority of them decussate in the com. superior telencephali. Although there is no differentiated cortex in the amphibian brain, this tract is so evidently homologous with the one so named in mammals that this name is preferable to Ariens Kappers' term, "tr. olfacto-habenularis lateralis," because the latter term is commonly applied to a different tract, no. 2 of the present list. In my paper of 1910 (p. 428) the tr. olfacto-habenularis anterior was not recognized as a separate entity but was regarded as a forward extension of the tr. olfacto-habenularis from the preoptic nucleus. This usage has some justification in cyclostomes and other most primitive vertebrates and is still employed by some authors, but the distinction between the fibers which arise from the preoptic nucleus and those from the hemisphere is significant and should be recognized in the nomenclature. In most species tr. cortico-habenularis lateralis is well defined. To avoid confusion, the terms "tr. olfacto-habenularis lateralis et medialis" should be restricted to fibers which enter the stria medullaris between the anterior commissure and the optic chiasma, arising either in the preoptic nucleus or as collaterals from the medial forebrain bundle.

6. Tractus amygdalo-habenularis. These are thick fibers, some of which are myelinated, passing from the gray of the amygdala to the habenula. Some of them may connect farther forward with the primordial corpus striatum — tr. strio-habenularis. These fibers ascend in the stria between nos. 5 and 8, and many of them end in the habenular neuropil (figs. 31-34, 74-78; '27, p. 302 and figs. 13, 14). As they approach the habenular commissure, these thick fibers mingle with those of the medial cortico-habenular tract, and these components can be separated only in electively impregnated specimens. In one such preparation of adult Amblystoma (no. 2257) the sections are inclined about 45° to the sagittal plane and the tr. amygdalo-habenularis is heavily and electively impregnated on both sides. The only other component of the stria stained is a small number of fibers of tr. cortico-habenularis medialis on one side only. The large tract from the amygdala is clearly followed through the commissure to the amygdala of the opposite side.

7. Tractus septo-habenularis. These fibers arise from the septal area and the bed-nuclei of the anterior commissure and ascend to the stria medullaris between this commissure and the interventricular foramen (fig. 75) . They spread in the ventral habenular neuropil and have not been followed farther. In some preparations there is evidence that these fibers are accompanied by others from the anteroventral part of the corpus striatum complex (primordial nucleus caudatus) — a strio-habenular connection.

8. Tractus cortico-habenularis medialis (figs. 32, 33, 34, 71, 76; '27, figs. 11-17, here marked, str.med.). This is a large component of unmyelinated fibers and a few thick fibers with myelin sheaths. They arise from all parts of the primordium hippocampi, leaving its posteroventral border in company with similar fibers of the hippocampal commissure and tr. cortico-thalamicus medialis. Under the stemhemisphere fissure they turn sharply dorsad, to ascend as the most anterior component of the stria medullaris. They spread widely in the habenular neuropil, and some of them decussate at the anterior end of the habenular commissure, thus forming the com. pallii posterior.

9. Tractus cortico-thalamicus medialis (figs. 31, 32, 72, 75). These fibers are regarded as primordia of the columna fornicis. They accompany the tr. cortico-habenularis medialis, and some of their fibers are collaterals from that tract and the hippocampal commissure. They cross the stria medullaris obliquely and are not integral parts of it except for the collateral connection mentioned.

10. Tractus olfacto-thalamicus. This name was given to a collateral connection from the stria medullaris to the neuropil of Bellonci in Necturus ('336, p. 205). It is present also in Amblystoma.

11. Tractus thalamo-habenularis. These fibers arising from the dorsal thalamus and regions posteriorly of it enter the stria medullaris within the ventral habenular nucleus (fig. 76).. They are accompanied by fibers passing in the reverse direction, the tr. habenulothalamicus ('396, p. 539; '42, p. 261 and fig. 77). This connection has been described in mammals by several authors, recently by Marburg ('44, p. 220) in man, where its fibers arise from the anterior nucleus and pulvinar.

The tr. strio-habenularis is probably present in Amblystoma but has not been clearly seen. If so, its fibers may accompany those of the tr. amygdalo-habenularis and tr. septo-habenularis, as mentioned above. The former of these probable striatal connections is compa

THE HABENULA AND ITS CONNECTIONS 261

rable with the pallido-habenular connection described in man by Marburg ('44).

Number 12 of figure 20 is an afferent tract to the habenula from the tectum and nucleus pretectaHs, which has no connection with the stria medullaris — tr. tecto-habenularis. These fibers are accompanied by others which pass in the reverse direction — tr. habenulo-tectaUs.

FASCICULUS RETROFLEXUS

Efferent fibers leave the habenula, so far as is known, in three tracts: (1) from the dorsal nucleus to the tectum by the tr. habenulotectalis, (2) from the ventral nucleus to the dorsal thalamus by the tr. habenulo-thalamicus accompanying the tr. thalamo-habenularis, and (3) between these from both nuclei in the much larger f. retroflexus of Meynert. There may be other efferent fibers, e.g., to the cerebral hemispheres accompanying those of com. superior telencephah and com. pallii posterior, but these have not been observed. One habenula of the newborn rabbit was destroyed by von Gudden ('81), and subsequently Meynert's bundle of the same side was found to be atrophied.

The chief component of the f. retroflexus is the habenulo-interpeduncular tract, the fibers of which arise from both dorsal and ventral habenular nuclei (figs. 20, 71, 73, 77, 103). This tract is composed chiefly of thin unmyelinated fibers, which form the central core of Meynert's bundle. Surrounding this core, other thicker fibers are loosely arranged, some of these being myelinated. Weigert sections show that a few myelinated fibers arise from both dorsal and ventral habenular nuclei and that these are joined by a few others from the dorsal thalamus, pretectal nucleus, and eminence of the posterior commissure. This fasciculus is also accompanied for part of its course by the few myelinated fibers of the parietal nerve (p. 235). No fibers have been seen to enter it from the tectum. The myelinated fibers leave the fasciculus and scatter in the alba of the nucleus of the tuberculum posterius; none of them enter the interpeduncular nucleus. In addition to these myelinated and other thick axons which terminate in the alba of the peduncle, there are many fine fibers from the axial core which take similar courses ; some of these are probably of habenular origin.

The fasciculus descends across the thalamus at the outer border of the gray and is partly imbedded within it. Its course as seen in horizontal sections is shown in figures 30-35 (for the course in transverse sections see '"io, ^gs. -2-7. and 'il , figs. '■28-oo, tr.hab.pcd.). As it enters the peduncle, it turns outward, passing ventrolaterally thriiugh tlie alba to reach the surface near the superficial origin of the III nerve root. Passing ventrally of these emerging root fibers, it turns medially at the fovea isthmi, immediately spinahvard of which it enters its decussation in the ventral commissure (figs. 50, 51, 53). The spiral endings of these fibers are described in chapter xiv. In the alba of the peduncle it passes internally of the area ventrolateralis pedunculi and well separated from this superficial neuropil {fig. 94). Here many thin axons separate from the fasciculus to enter the superficial neuropil. A little farther spinalward. at the level of the III nerve root, a larger number of fine fibers leave the fasciculus and turn forwartl into the posterior end of the neuropil, as shown in a favorable (lolgi section ('4^, fig. 40, fibers from, f.retr. to a.I.t.).

This is the usual arrangement. That the connection of the f. retroflexus with the area ventrolateralis pedunculi is important physiologically is evident from atypical courses of the fasciculus which have been observed in a number of specimens, always on one side only. One such anomaly is well illustrated in figures 56. 57. and 58. In this specimen (horizontal Golgi sections) the right f. retroflexus is unstained but can be seen to take the usual course; the left is abundantly impregnated from the habenula to its decussation. As it enters the alba of the peduncle it divides into two bundles. The medial bundle, containing about one-third of the fibers, takes the typical course: the larger lateral bundle passes along the inner border of the area ventrolateralis pedunculi with numberless terminals or collaterals entering this neuropil and spreading in the surrounding alba. Both bundles pass spinalward under the emerging III root fibers and converge to the decussation below the fovea isthmi. Many of these fibers spread in the alba rostrally and caudally of the fovea without decussation.

Another adult specimen (^no. "2'-217) from the same. lot and similarly prepared is like that just described except that the lateral bundle is smaller than the medial. This smaller bundle enters the area ventrolateralis and here breaks up into several slender fasciculi. Posteriorly of this area of neuropil, these fasciculi, somewhat diminished in volume, i-ejoin the medial bundle at the level of the III nerve root and both bundles then enter the decussation. This arrangement is found. on one side only, in the series of sagittal Golgi sections from which figures 7'2 and 73 were drawn. A somewhat different atypical feature

THE HABENULA AND ITS COXNECTIOXS 263

is seen in the series of sagittal Cajal sections from which figures 74-78 were drawn. The fasciculus is well impregnated on both sides, and on one side it takes the typical course. At the decussation the thinnest fibers cross in the usual way, and some fibers of thicker caliber descend uncrossed at the lateral border of the interpeduncular neuropil. Whether they ultimately decussate and enter the interpeduncular spiral is unknown, because the impregnation fails below the decussation. On the opposite side the f . retroflexus divides as it enters the peduncle. The larger medial bundle takes the txT^ical course. A small compact fascicle separates from it and passes more laterally to reach the area ventrolateralis pedunculi, where its fibers spread in the neuropil and disappear. Modifications of the arrangements just described have been seen in several other series of Golgi sections of late larv^ae and adults. The lateral bundle may be larger or smaller than the medial bundle, and in the latter instances it may end in the peduncle or rejoin the medial bundle at the decussation.

From these observations it is concluded that in Amblystoma the f. retroflexus is a mixture of fibers of different physiological characteristics. The main axial bundle of fine unmyelinated fibers is the habenulo-interpeduncular tract. Most of these fibers decussate below the fovea isthmi and enter a peculiar elongated spiral in the interpeduncular neuropil within which they end. A smaller number, including some thicker axons, descend uncrossed along the lateral border of the interpeduncular neuropil. These endings are in isthmic territory. Rostrally of the fovea many thin unmyelinated fibers, evidently of habenular origin, end uncrossed in the posteroventral border of the cerebral peduncle near the level of the nucleus of the III nerve. This area may be regarded as a mesencephalic sector of the interpeduncular nucleus, though there is no cellular differentiation here, like that of this nucleus below the fovea. Other similar fibers, doubtless also from the habenula, leave the f. retroflexus farther forward and terminate in the superficial neuropil termed "area ventrolateralis pedunculi." In some specimens these are very numerous. The few myelinated fibers of f . retroflexus derived from the habenula end in the cerebral peduncle. This fasciculus receives accessions of fibers, a few of which are myelinated, from the dorsal thalamus, pretectal nucleus, and eminence of the posterior commissure. All these fibers probably end in the cerebral peduncle; there is no evidence that any of them reach the interpeduncular nucleus. In a series of sagittal Golgi sections (no. 2215), in which the tr. habenulointerpeduncularis is impregnated, a few thick axons are seen to arise in the gray of the dorsal thalamus and join the f . retroflexus, which they accompany almost to the ventral surface. Here some of them end by wide arborization in the area ventrolateralis pedunculi. This area of neuropil, accordingly, receives fibers by way of the f . retroflexus from both the habenula and the dorsal thalamus.

The connections just described are a simplified version of the complicated structure of the f. retroflexus of Ceratodus described by Holmgren and van der Horst ('25, p. 105). The fact that the atypical arrangements occur on only one side in Amblystoma probably is explained by the asymmetry of the habenular system in Ceratodus and other primitive species.