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J. Comp. Neurol. 119:77-95 (1962) Some Fiber Projections to the Superior Colliculus in the Cat' JOSEPH ALTMAN Psychophysiological Laboratory, Massachusetts Institfrte of Technology, Cambridge, Massachusetts Our knowledge of fiber projections to the optic tectum or superior colliculus, an important way-station in the visual system of vertebrates including mammals, is still inadequate. Studies of these fiber projections, utilizing different techniques, have been made in various mammals (Tsai, '25; Bodian, '37 in opossum; Johnson, '54, in mole; Cajal, '11, in mouse; Lashley, '34; Tsang, '37; Le Gros Clark, '42; Krieg, '47; Nauta and Bucher, '54, in rat; Castaldi, '23-'26; Hess, '58, in guinea pig; Cajal, '11; Loepp, '12; Minkowski, '20; Brouwer, Zeeman and Houwer, '23; Overbosch, '27, in rabbit; Jefferson, '40, in ferret; Monakow, 1889; Probst, '02; Cajal, '11; Poljak, '26; Barris, Ingram and Ranson, '35; Bucher and Biirgi, '50; Biirgi, '57, in cat; Brouwer and Zeeman, '26; Mettler, '35; Hirasawa, '38; Crosby and Henderson, '48; Whitlock and Nauta, '56; Polyak, '57, in monkey; and Juba, '39, in man). The majority of these investigations has been concerned with retinal projection and with projections from the spinal cord and visual cortex. In the present study, which is a continuation of a previous one (Altman and Carpenter, '61) dealing with the efferent connections of the superior colliculus in the cat, we investigated by means of the Nauta-Gygax ('54) staining technique projections to the superior colliculus in the cat from ( a ) the retina, (b) the lateral geniculate nucleus, (c) the pulvinar, and (d) the visual cortex. In addition, attention was paid to projection from these structures to other mesencephalic and also to the various diencephalic nuclei. MATERIALS AND METHODS Eleven adult cats were used in this experiment. The animals were anesthetized with Nembutal, and surgery was per- formed under aseptic conditions. In two animals the right orbit was unroofed and the optic nerve was cut. Stereotaxic lesions were produced in the right lateral geniculate nucleus in five animals, and in the right pulvinar in one animal. In three animals large portions of the right visual cortex (lateral and postlateral gyri) were removed by suction. Most of the animals were permitted to survive for 11 days; two of them were sacrificed after a shorter period. All animals were sacrificed by cardiac perfusion with 10% neutral formalin. The brains were sectioned in 2-3 mm blocks perpendicular to the axis of the brain stem and further fixed in 10% neutral formalin. Four or five selected blocks of the brain were cut serially at 25 LI on a freezing microtome, and the sections were stained individually according to the Laidlaw modification of the Nauta-Gygax method ('54). In animals with stereotaxic lesions, several frozen sections were stained with cresyl violet to permit more precise evaluation of the location and extent of the lesions produced. OBSERVATIONS Fiber projections from the retina Complete sectioning of the right optic nerve, verified histologically, was accomplished in two animals. All stained fibers in the right optic nerve appeared degenerated, but no degenerated fibers were seen in the left optic nerve. The chiasma 1 This investigation was caxried put at the Department of Anatomy, Colle e of Physicians and Surgeons, Columbia University, w%ile the author was a postdoctoral trainee in neuroanatomy (supported by grant 2B-5242 from the Institute of Neurological Diseases and Blindness). The continuous guidance and help provided by Dr. Malcolm B. Carpenter is gratefully acknowledged. Aid in the reparation of this report was received from the Nazonal Institute of Mental Healfh, upder its program grant M-5673 to the Psychohysiologlcal Laboratory, Massachusetts Institute of echnology. F 77 78 JOSEPH ALTMAN contained degenerated fibers in abundance, while in the optic tract there was a greater preponderance of such fibers in the contralateral optic tract (see fig. 4 ) . A relatively small proportion of the degenerated fibers of the optic tract reached the superior colliculus. These fibers passed mainly through the lateral branch of the brachium of the superior colliculus, after a short course over the dorsolateral edge of the medial geniculate body. Although degenerated fibers reached the superior colliculus on both sides, these were more numerous in the contralateral than ipsilateral brachium. A few degenerated fibers, particularly on the contralateral side, were also seen reaching the dorsomedial surface of the superior colliculus by way of the medial branch of the brachium. The fibers entering the superior colliculus were concentrated mainly in the upper part of the stratum opticum (the third layer from the dorsal surface). Some of these fibers appeared to terminate around cells situated in this layer. A small proportion of the degenerated fibers turned dorsally and ventrally. The dorsally oriented fibers penetrated the stratum griseum superficiale, but did not reach the most superficial layer, the stratum zonale. The ventrally oriented fibers moved toward the deeper layers but did not reach the deepest layer, the stratum album profundum. The number of degenerated fibers in the contralateral colliculus greatly exceeded those in the homolateral colliculus. No degenerated fibers were seen to cross in the commissure of the superior colliculus. At the level of the superior colliculus degenerated fibers were absent from the following structures : the mesencephalic reticular formation, periaqueductal gray, nuclear complex of the third nerve, and the various fibrous and cellular structures of the tegmentum. Outside the superior colliculus degenerated retinal fibers were observed in the mesencephalon only in one area, in a small region situated dorsolateral to the cerebral peduncle. This contralateral degenerated tract, very small in the cat, may represent the posterior accessory optic tract. More anteriorly, at the level of the pretectum, a few degenerated fibers were observed on the contralateral side medial to the cerebral peduncle. This small retinal tract may be identical with the anterior accessory optic tract. Retinal fibers also reach the rostral diencephalic extension of the superior colliculus, the pretectal region. Degenerated fibers were seen to reach this structure laterally by way of the lateral branch of the brachium of superior colliculus, and via the optic tract, in the ventromedial aspects of the lateral geniculate body (the latter fibers were to some extent coursing over the surface of the pulvinar). A considerable proportion of fibers, particularly in the rostral parts of the pretectal region, passed by way of the medial branch of the brachium of the superior colliculus. As in the case of the superior colliculus, a larger proportion of degenerated fibers reached the contralateral than the ipsilateral pretectal regions. While numerical estimates are difficult to obtain with the technique employed, the impression was gained that more direct retinal fibers reach the pretectum than the superior colliculus. The majority of retinal fibers in the pretectal region appeared to terminate laterally in the large-celled nucleus of the optic tract, but some also penetrated the whole extent of the pretectum by way of the stratum opticum. Degenerated fibers at this level were absent from the posterior commissure and its nucleus. The lateral geniculate nucleus was surrounded by a dense layer of degenerated fibers; the amount of degeneration was greater on the contralateral than ipsilateral side. The dorsal portion of the nucleus showed a laminar pattern of degeneration essentially similar to that described recently by Hayhow ('58). The amount of degenerated fibers seen in the dorsal nucleus of the lateral geniculate body greatly exceeded that seen in the superior colliculus and pretectum. Also in the ventral nucleus limited areas infiltrated by some degenerated fibers were observed both contra- and ipsilaterally, but there was no evidence of preterminal arborization in this area. Degenerated fibers were observed to pass over the surface of the pulvinar; most of these fibers appeared to terminate in the pretectum. In limited regions of the pulvinar, adjacent to the lateral geniculate body, some indications of preterminal PROJECTIONS TO SUPERIOR COLLICULUS arborization were observed. However, extensive areas of the pulvinar were entirely free of degenerated preterminal fibers. Degenerated fibers were also absent from all other thalamic nuclei, including the posterolateral nucleus. The hypothalamus, likewise, was free of degenerated fibers with the exception of one region, above the chiasma and in its lateral wall immediately adjacent to the optic tract, where a small number of degenerated fibers were observed to pass. These latter appeared to be aberrant fibers of passage which showed no evidence of termination in this region. Fiber projections from the lateral geniculate nucleus In five animals extensive lesions were produced in the right lateral geniculate body. In three of these the lesions affected the ventral aspect of the dorsal nucleus, while in two the destruction was limited mainly to the dorsal aspect of the dorsal nucleus. As these two types of lesions produced somewhat differing patterns of degeneration, they will, in part, be treated separately in the following description. Most of the lesions were restricted to the pars dorsalis of the lateral geniculate body. In one animal the pars ventralis of the lateral geniculate body was to a large extent also destroyed; in another the pulvinar was slightly affected, and in several there was some involvement of the adjacent forebrain structures (see figs. 1, 2). In all animals with lateral geniculate lesions, degenerated fibers were seen to enter the superior colliculus by way of its brachium. Most of the degenerated fibers penetrated by way of the lateral division of the brachium of the superior colliculus (situated dorsally to the medial geniculate body), while fewer fibers passed through the medial branch of the brachium (situated laterodorsally to the commissure of the superior colliculus). In animals with ventrally placed geniculate lesions the number of degenerated fibers that entered the colliculus was considerable, while in animals with dorsally placed geniculate lesions the number of degenerated fibers in the colliculus was much smaller. The involvement, in the former 79 case, of some direct retino-collicular fibers, is possible. Within the superior colliculus degenerated fibers were most numerous in the stratum opticum, where these fibers were mostly oriented horizontally. From the stratum opticum some fibers turned dorsally to terminate in the lower parts of the overlying stratum griseum superficiale, while others turned ventrally and could be followed into the deeper layers, the stratum griseum intermediale and stratum album intermediale. Dorsally, no fibers of the stratum opticum reached the upper part of the stratum griseum superficiale, or the uppermost layer of the colliculus, the stratum zonale. However, in two animals with ventrally placed geniculate lesions a thin band of degenerated fibers was observed in the stratum zonale. This degenerated band was separated from the underlying degenerated layer (the lower part of the stratum griseum superficiale) by a zone devoid of degenerated fibers, and the origin of this band could be traced to the brachium, coursing medially over the dorsal surface of the colliculus. In animals with dorsally placed geniculate lesions no fibers could be traced to the lowest layer of the colliculus, the stratum profundum, though they were present in small numbers in animals with ventral lesions. The large cells in the lower layers of the colliculus were devoid of degenerated preterminal fibers in the dorsal lesion group, while in those with ventral lesions a few degenerated fibers were observed around and in the neighborhood of these cells. Likewise, no degenerated fibers were seen crossing in the commissure of the superior colliculus in the dorsal lesion group, while in the two animals of the ventral lesion group a few degenerated fibers were seen crossing in the commissure and some were present in the contralateral colliculus, mainly in the stratum opticum. No degenerated fibers were found in either group of animals in the following mesencephalic structures : the reticular formation, the oculomotor nucleus, the nucleus of Darkschewitsch, or the interstitial nucleus of Cajal. In animals with lesions involving parts of the cortex some 80 JOSEPH ALTMAN degenerated fibers were observed in the cerebral peduncle. Degenerated fibers were observed in all animals in the pretectum, though the number of degenerated fibers was considerably greater in those animals which had ventrally placed geniculate lesions. These degenerated fibers reached the pretectum by way of the medial aspect of the optic tract and the lateral and medial branches of the brachium of the superior colliculus. As in the superior colliculus, the majority of degenerated fibers in the pretectum were located in the stratum opticum, whence they were distributed both dorsally and ventrally. Arborization of degenerated fibers around cells of the pretectum was observed. In the majority of animals degeneration in the pretectum was restricted to the lesion side; in one animal some degenerated fibers were also present in the posterior commissure and in the contralateral pretectum. In the lateral geniculate body degeneration was conspicuous around the lesion, in the fibrous sheath surrounding the nucleus (fibers of the optic tract and optic radiation), and in selected parts of the lateral geniculate nucleus some distance away from the lesion. In animals with dorsally placed lesions, in which the pars ventralis of the lateral geniculate body was spared, numerous degenerated fibers could be observed in the latter structure. This evidence suggests that fibers from the dorsal or principal nucleus of the lateral geniculate body project to the ventral or pregeniculate nucleus. No degenerated fibers were observed in the contralateral lateral geniculate body in any of these animals. In all animals degenerated fibers from the lateral geniculate body could be followed laterally in the optic radiation to the striate cortex, and medially in the optic tract to various thalamic nuclei. The latter included the pulvinar, the posterior nucleus, the suprageniculate nucleus, the posterolateral nucleus and the dorsolateral nucleus. All of these contained degenerated fibers in large numbers on the lesion side, with indications of terminal arborization around cells. No degenerated fibers were present in the intralaminar nuclei, except in one animal. This lesion in- volving the pars ventralis, produced degeneration in the centromedian nucleus. In another animal a few degenerated fibers were observed in the habenular nuclei. Ventral to the lateral geniculate body, and in its immediate vicinity, the optic tract was full of black granules; these appeared to be debiis from the lateral geniculate nucleus. These granules, which could be differentiated from degenerated fibers, were present in decreasing numbers at increasing distances from the lateral geniculate body and were not present at the level of the chiasma or in the optic nerves. In two animals with ventral lesions some degenerated fibers were present in the optic tract. These fibers could be traced around the lateral wall of the medial geniculate body to the reticular nucleus of the thalamus, where apparently some of them terminated, and from there to Forel's field HI and the zona incerta. This ventral band was particularly conspicuous in the animal in which the pars ventralis of the lateral geniculate body was destroyed. In none of the animals were degenerated fibers observed in the hypothalamus. Fiber projections from the pulvinar In a single animal a large lesion was produced in the right pulvinar. The lesion destroyed a large part of the dorsal and rostra1 portions of the pulvinar; its more caudal and ventral parts were less affected. The lateral geniculate body and other adjacent diencephalic structures were spared (see fig. 3). In this animal degenerated fibers, many of them of large diameter, were present in the ipsilateral superior colliculus. These fibers appeared to be concentrated mainly in two separate bands, the stratum opticum and stratum griseum intermediale - with a relatively greater concentration in the latter layer. From the stratum opticum some fibers could be followed dorsally into the stratum griseum superficiale; a very few horizontally oriented degenerated fibers were also present in the stratum zonale. From the stratum griseum intermediale degenerated fibers (mostly coarse ones) could be followed ventrally as far down as the upper edge of the stratum profundum. In general, the number of degenerated fibers PROJECTIONS TO SUPERIOR COLLICULUS in the colliculus following the lesion in the pulvinar was smaller than following severance of the optic nerve, lesion of the lateral geniculate nucleus or ablation of the striate cortex. Outside the superior colliculus degenerated fibers were not present in any portion of the mesencephalon, including the reticular formation and the oculomotor nuclear complex. Degenerated preterminal fibers were also present in the homolateral pretectum, mostly in its medial parts. The number of degenerated fibers in the pretectum appeared to be much smaller than in the superior colliculus. A few degenerated fibers were also present in the homolateral posterior and suprageniculate nuclei, and also in some parts oE the posterolateral nucleus. No degenerated fibers were present in the lateral geniculate nucleus, either in the pars dorsalis or pars ventralis. Some degenerated fibers could be observed in the outer fibrous sheath of the lateral geniculate body; presumably these fibers were destined to the superior colliculus, pretectum and the few diencephalic structures previously mentioned. Degenerated fibers were not present in the optic tract below the level of the lateral geniculate body. Degenerated fibers were also present in the neighborhood of the pulvinar in the internal capsule, and a few degenerated fibers could be seen in the striate cortex. Fiber projections from the visual cortex The right lateral and postlateral gyri (visual cortex) were removed by suction in three animals. In two animals the removal was extensive, involving the greater part of the primary visual area (see fig. 5), while in the third, only a portion of the visual cortex was ablated (see fig. 6). In all three animals numerous degenerated fibers were observed to leave the cortex by way of the internal capsule, but the degeneration was less extensive in the animal with small striate cortex lesion. In animals with unilateral removal of the striate cortex (lateral and postlateral gyri), degenerated fibers were observed to reach the superior colliculus in large number on the lesion side. These fibers reach the superior colliculus mainly by way of the lateral division of the brachium of 81 superior colliculus and, to a lesser extent (observed only in two animals), by way of the medial branch of the brachium. These corticofugal fibers were mostly concentrated in the stratum griseum intermediale, but were also numerous in the stratum opticum. A few degenerated fibers were also observed to pass on the dorsal surface of the colliculus in the stratum zonale. In these three layers the corticofugal fibers moved mainly in a horizontal direction, with some fibers moving dorsally and ventrally. The dorsally turning fibers of the stratum opticum reached the lower part of the stratum griseum superficiale but did not appear to fuse with the degenerated fibers of the stratum zonale, from which they remained separated by a thin band containing no degenerated fibers. The ventrally turning fibers leaving the stratum opticum were found intermingled with fibers that moved dorsally from the underlying stratum griseum intermediale. In all these layers degenerated fibers were seen surrounding cells. In particular, the large cells situated laterally in the region of the brachium and in the stratum album intermediale (nucleus of the optic tract) were richly supplied with degenerated fibers. N o degenerated fibers were seen to cross the commissure of the superior colliculus (except for a n occasional fiber noted in all animals), and degenerated fibers were absent from the contralateral superior colliculus. No degenerated fibers were seen in the mesencephalic reticular formation or in any of the other mesencephalic nuclei implicated in visual functions, e. g., the oculomotor nucleus, the nucleus of Darkschewitsch and the interstitial nucleus of Cajal. Some degenerated fibers were present in the lateroventral part of the cerebral peduncle. Degenerated fibers reached the pretectum on the lesion side in large numbers by way of the brachium of the superior colliculus. These fibers were concentrated mainly on the lateral aspect of the pretectum. While lamination in the pretectum is less distinct than in the superior colliculus, the impression was gained that the corticofugal fibers terminated here largely in a layer ventral to the region of termination of the optic tract fibers 82 JOSEPH ALTMAN (stratum opticum). Degenerated fibers were seen arborizing around large cells situated in the lateral part of the pretectum (nucleus of optic tract). No degenerated fibers were seen crossing in the posterior commissure, and the opposite pretectal region was free of degeneration. Numerous degenerated fibers were present in the fibrous sheath of the lateral geniculate body. However, in the dorsal nucleus of the lateral geniculate body degenerated fibers were present only in small number in limited regions, and they were altogether absent in others. In general, degenerated fibers were more abundant in the rostral and dorsal parts of the dorsal nucleus than in its more caudally and ventrally situated parts. A limited number of fine degenerated fibers were also seen in some parts of the ventral nucleus of the lateral geniculate body. There was no degeneration in the contralateral lateral geniculate body. In contrast to the scarcity of degenerated corticofugal fibers in the lateral geniculate nuclei, numerous degenerated fibers were present on the lesion side in the posterior nucleus and the pulvinar, and, to a lesser extent, in the suprageniculate nucleus and the posterolateral nucleus. In all these structures degenerated fibers were seen arborizing around cells, in particular around the larger cells of the posterior nucleus and pulvinar. In addition to these thalamic nuclei, degenerated fibers were also present in the dorsal parts of the reticular nucleus in the neighborhood of the pulvinar and lateral geniculate body. Other parts of the thalamus, including the intralaminar nuclei, were devoid of degenerated fibers. No degenerated fibers were seen in the optic tract below the level of the lateral geniculate body or in any part of the hypothalamus. DISCUSSION Fiber projection to the superior colliculus ( a ) Retinal projection. Our observation that direct retinal fibers reach the superior colliculus in the cat is in agreement with the findings of earlier investigators (Probst, ’02; Barris, Ingram and Ranson, ’ 3 5 ) . The description by Barris, et d. that the crossed retinal fibers in the col- liculus of the cat greatly exceed in number the uncrossed ones was also confirmed. This asymmetry of projection is supported by an electrophysiological investigation made earlier (Altman, ’59) which showed that, of the simultaneously recorded photically evoked potentials, those obtained from the contralateral colliculus were consistently of larger amplitude than those obtained from the ipsilateral colliculus. The present investigation also confirms the claim (Polyak, ’57) that the number of retinocollicular fibers in the cat is quite small in comparison with the retinogeniculate fibers. This would reflect a greater “corticalization” in the feline visual system, as compared with lower mammalian forms (marsupials and rodents) in which the proportion of retinocollicular fibers is much higher (cf. LeGros Clark, ’42; Polyak, ’57). The observation (Altman, ’59) that, on simultaneous recording, evoked potentials to photic or optic nerve stimulation are generally of greater amplitude in the cat’s visual cortex than in its superior colliculus may reflect the same phenomenon. There is general agreement in the literature that the optic fibers reach the superior colliculus through its brachium, and that within the colliculus they are concentrated in the stratum opticum. There is, on the other hand, a controversey of long standing with regard to the termination of these fibers. The problem was first investigated intensively by Cajal (‘1 1) with the Golgi technique. He described two kinds of fiber endings, “arborisations infkrieures,” which, entering the stratum opticum, turn ventrally and end in the same layer, and “arborisations supkrieures,” which turn dorsally and end in the stratum griseum superficiale. Some investigators employing the Weigert and Marchi techniques (e.g., Brouwer, Zeeman and Houwer, ’ 2 3 ) similarly failed to observe terminal fibers reaching the uppermost collicular layer, the stratum zonale. Other histologists, however, such as Loepp (’12) and Bodian ( ’ 3 7 ) ,claimed that some fibers also reach the stratum zonale. In re-investigating this problem in the ferret, Jefferson (’40) found that with the Marchi technique osmic acid granulation is limited to the stratum opticum and stratum griseum superficiale, with no signs of degen- PROJECTIONS T O SUPERIOR COLLICULUS eration in the stratum zonale, whereas a silver impregnation technique yielded evidence for the termination of unmyelinated fiber branches or collaterals in the stratum zonale. The results of the present study do not lend support to the claim that preterminal optic tract fibers reach the stratum zonale. ( b ) Geniczilate projection. While the existence of direct retinotectal projection is well established, the present investigation suggests that the colliculus also receives indirect or relayed optic fibers by way of the lateral geniculate nucleus. This conclusion is supported by the observation that lesions of the dorsal nucleus of the lateral geniculate body, including those located rostrally and dorsally (and thus presumably sparing the retinotectal fiber system) produced preterminal degeneration in the colliculus. It should also be noted that degeneration in the colliculus following lesions in caudal and ventral parts of the lateral geniculate nucleus greatly exceeded that found after severance of the optic nerve. Such a lesion apparently affects both the direct retinotectal fiber system situated in this region and the indirect retino-geniculotectal projection. While the technique employed here is not suitable for exact determination of fiber diameters, the impression was gained that the fibers of the retinotectal system are generally of smaller diameter than the fibers of the retinogeniculate system. This has been claimed by several investigators using histological material (e.g., Gudden, 1886, in rabbit; Bishop and Clare, ’55, in cat; Polyak, ’57, in monkey) and is also in agreement with the electrophysiological evidence that the conduction velocity of impulses is much lower in the retinotectal than the retinogeniculo-striate projection system, (e.g., Bishop and Clare, ’55; Altman, ’59). ( c ) Projection from the pulvinar. The superior colliculus also receives fibers from the pulvinar. As the pulvinar itself receives but few fibers from the optic tract, this connection may not serve a function similar to that of the retino-geniculo-tectal fiber system. Of the structures investigated in this study, the pulvinar alone appears to have reciprocal connections with the superior 83 colliculus; the lateral geniculate and striate cortex send fibers to the colliculus but do not receive any from it. ( d ) Cortical projection. In addition to fibers from optic tract, lateral geniculate nucleus and pulvinar, the superior colliculus also receives a large number of fibers from the ipsilateral striate cortex. Evidence for corticotectal projection in the cat was first obtained by Monakow (1889), and was later confirmed by Probst (’02); Beevor and Horsley (’02); Cajal (’11);Poljak (’26,’28) and Barns, Ingram and Ranson (’35) in the cat, and by several investigators in other mammalian species (Johnson, ’54, in mole; Krieg, ’47; Nauta and Bucher, ’54, in rat; Leblanc, ’28, in rabbit; Probst, ’02, in dog; Jefferson, ’40; in ferret; Ferrier and Turner, 1897; Mettler, ’35; Crosby and Henderson, ’48; in monkey). With regard to the laminar distribution of corticofugal fibers in the colliculus there is considerable disagreement. Some investigators localized the penetrating corticotectal fibers in a single layer, either in the stratum opticum (e.g., Probst, ’02 [described as “lower zonal layer”], Barris, Ingram and Ranson, ’35; Jefferson, ’40), or ventral to the stratum opticum (Cajal, ’ l l ) , with arborizations in the layers situated dorsally and ventrally. Others described two zones of distribution (e.g., Poljak, ’26, ’28 [“upper” and “middle” layers], Krieg, ’47 [“superficial fibrous lamina” and ‘“deep lamina”] ) . The present investigation suggests that the corticotectal fibers are distributed in the cat through three separate zones in the colliculus. First, a very small but distinct band of fibers terminates in the stratum zonale. These small fibers do not come by way of the stratum opticum, as some in vestigators suggested (e.g., Barris, Ingram and Ranson, ’35), but may be followed directly from the brachium as a thin band of horizontal fibers moving over the dorsal surface of the colliculus. Second, some fibers are present in the stratum opticum, forming a dark band in this region. Some of these penetrate dorsally into the stratum griseum superficiale, but do not reach the stratum zonale, while others turn ventrally and end in the stratum griseum intermediale. The largest share of corticofugal fibers is concentrated in this latter 84 JOSEPH ALTMAN layer, and the majority of them appears to come directly from the brachium rather than via the stratum opticum. Thus, the bulk of corticotectal fibers is concentrated in a layer ventral to the stratum opticum (the layer of termination of the direct retinal and indirect retinogeniculate fibers); an observation that was made first by Cajal ('11) and was noted later by other investigators (e.g., Crosby and Henderson, '48). The corticotectal fibers from the striate cortex and adjacent regions are strictly homolateral in distribution, and no fibers of this system cross in the commissure of the superior colliculus. This observation is in agreement with the reports of the majority of investigators considered, with the exception of Probst ('02),who claimed that in the cat some corticotectal fibers go to the contralateral colliculus by way of the commissure. The observation made by Mettler ('35) and Crosby and Henderson ('48) that, in the monkey, the occipital cortex projects to the aculomotor nucleus, the nucleus of Darkschewitsch, and interstitial nucleus of Cajal could not be substantiated in the cat. Apart from the superficial and middle layers of the superior colliculus, which receive a massive projection from the visual cortex, no other mesencephalic structure receives fibers from this region. This applies also to the mesencephalic reticular formation which was found to be devoid of degenerated fibers. With regard to the reticular formation, the present investigation suggests that this "activating" or "arousal" mechanism does not receive direct input from the optic tract, the lateral geniculate nucleus, the pulvinar or striate cortex. On the other hand, evidence was obtained in a previous study (Altman and Carpenter, '61) that a major efferent outflow of the superior colliculus is into the mesencephalic and bulbar reticular formation. Thus, it is conceivable that the EEG activation and behavioral arousal effects of peripheral (retinal) and central (cortical) visual stimulation are, at least partially, mediated by way of the superior colliculus. For the superior colliculus receives input from all the visual structures considered and discharges into the reticular forma- tion. That electrical stimulation of the superior colliculus produces EEG activation and behavioral arousal was observed by Pearce (cf., Jefferson, '58), and there is an unconfirmed report (Takebayashi, '57) that after bilateral ablation of the colliculus in rabbits EEG activation by light flash (blocking of alpha activity) is abolished. Fiber projections to and within the diencephalon ( a ) Retinal projection to the diencephalon. Some investigators (e.g., Polyak, '57) reported that in the cat, as in primates, the number of crossed and uncrossed fibers in the optic tract are approximately equal. The observation made in the present investigation was that the crossed optic fibers greatly exceed in number the uncrossed fibers in this species. Similarly, the amount of degeneration i n the contralateral lateral geniculate nucleus greatly exceeded the degeneration found on the homolateral side. No detailed investigation was made here of the pattern of termination of the crossed and uncrossed components in the laminae of the lateral geniculate nucleus, but the essential features of a recent description by Hayhow ('58) could be confirmed. There is considerable controversy in the literature with regard to the problem of retinal projection to the ventral nucleus of the lateral geniculate body. Some investigators have claimed that a few retinal fibers terminate in this structure (eg., Castaldi, '23, in guinea pig; Pavlow, '00; Cajal, '11; Loepp, '12; Brouwer, Zeeman and Houwer, '23, in rabbit; Minkowski, '20; O'Leary, '40; Polyak, '57; Hayhow, '58, in cat; Polyak, '57, in monkey). Others maintained that, while retinal fibers do pass through the ventral nucleus, none terminate in it (Tsai, '25, in opossum; Lashley, '34; Tsang, '37, in rat; Jefferson, '40, in ferret; Barris, Ingram and Ranson, '35; Glees, '41, in cat). The present investigation does not presume to resolve this controversy. It should be pointed out, however, that while retinal fibers were observed to pass through the ventral nucleus in our material, arborization around cells was not observed. PROJECTIONS T O SUPERIOR COLLICULUS Apart from the pretectum and the dorsal nucleus of the lateral geniculate body, no other diencephalic structures were observed to receive direct optic fibers in any great number. This applies to the suprageniculate, posterior and posterolateral nuclei of the thalamus, which receive fibers from various central visual structures but do not receive any direct fibers from the retina. Some optic fibers were observed to pass over the dorsolateral surface of the pulvinar, but only a few of these appeared to terminate there. This agrees with observations by a majority of investigators (Monakow, 1889, Probst, '02; Minkowski, '13, '20; Polyak, '57, in various mammalian species), although others denied that the pulvinar receives any direct optic fibers (Brouwer, Zeeman and Houwer, '23; Rioch, '29; Barris, Ingram and Ranson, '35). Fibers of retinal origin were also observed to course through the hypothalamus, above the optic chiasma, but no evidence was obtained that these fibers actually terminated in this region. Finally, we may mention the two small fiber bundles of retinal origin, the so-called anterior and posterior accessory optic tracts, both of which contain only crossed fibers. The first of these terminates medial to the cerebral peduncle at the level of the pretectum, while the latter terminates in a nuclear region dorsolateral to the cerebral peduncle at the level of the superior colliculus. The recent description by Hayhow ('59) of the origin and course of these fiber tracts in the cat could not be adequately evaluated in the material available. (b) Projections t o and from the lateral geniculate nucleus. The main fiber projection of the dorsal nucleus of the lateral geniculate nucleus is to the striate cortex. In addition, the lateral geniculate nucleus sends fibers (in part possibly collaterals) to the superior colliculus, to the pretectum, to the pulvinar and to the posterior, posterolateral and suprageniculate nuclei of the thalamus. In contrast to this extensive projection from the lateral geniculate body, the projection to it is very sparse from the striate cortex and nonexistent from the pulvinar and, as a previous study has shown (Altman and Carpenter, '61), from the superior colliculus. 85 The pathway through the lateral geniculate is, accordingly, essentially unidirectional, with an input from the retina and an output to the structures mentioned. If the lateral geniculate nucleus receives any reciprocal fibers at all from the structures to which it projects, such a connection must be by way of a central nervous region that was not investigated here (such as, perhaps, the pre- and parastriate regions of the cortex). Of some importance also is the finding that the pars dorsalis of the lateral geniculate body projects to the pars ventralis. Accordingly, the pars ventralis of the lateral geniculate body, which does not appear to receive direct retinal fibers, receives input from at least two structures implicated in vision, the dorsal nucleus and, as was previously shown (Altman and Carpenter, '61), the superior colliculus. The possibility that the ventral nucleus of the lateral geniculate body represents a motor outflow in the visual system via the subthalamus (cf. Polyak, '57), deserves consideration. ( c ) Projections to and from the pulvinar. The pulvinar, which receives few direct retinal fibers, receives indirect optical input from the lateral geniculate nucleus, the striate cortex, and also from the superior colliculus (Altman and Carpenter, '61). It sends reciprocal fibers to the superior colliculus and the striate cortex. In the single animal investigated in this study, no evidence could be obtained that it projects to the lateral geniculate nucleus. The possibility, of course, cannot be excluded that with a larger and more favorably placed lesion in the pulvinar such a connection could be demonstrated. The present evidence is compatible with the view that the pulvinar is an important secondary link in the visual system, comparable to the neighboring structures of the posterior, suprageniculate and posterolateral nuclei of the thalamus. ( d ) Cortical projection to the diencephd o n . In contrast to the extensive projection from the dorsal nucleus of the lateral geniculate body to the striate cortex, corticofugal projection from the striate cortex to this structure is suprisingly small. The fibrous sheath of the lateral geniculate body was full of degenerated fibers following ablation of the striate cortex; the dor- 86 JOSEPH ALTMAN alon were also investigated. The following conclusions were drawn from this study: 1. The superior colliculus receives afferent fibers directly from the retina. These afferents, which are more numerous on the contralateral than on the ipsilateral side, are distributed through the stratum opticum and reach dorsally the stratum griseum superficiale and ventrally the stratum griseum intermediale. Fibers of retinal origin do not cross in the commissure of the superior colliculus. 2. The superior colliculus also receives indirect optic afferents from the ipsilateral lateral geniculate nucleus. The intracollicular distribution of these fibers is similar to that of the direct optic fibers. 3. The superior colliculus receives ipsilaterally a few coarse fibers from the pulvinar and a bulky projection from the striate cortex. The corticofugal fibers are distributed separately through three layers, the stratum zonale, stratum opticum and the stratum griseum intermediale. 4. Fiber projection could not be demonstrated from the retina, lateral geniculate, pulvinar or striate cortex to the third nerve nuclear complex or the mesencephalic reticular formation, Projection from these structures to the pretectum is essentially similar to that of the superior colliculus. 5. The number of retinal fibers reaching the lateral geniculate nucleus in the cat greatly exceeds the number of fibers reaching the superior colliculus and pretectum. The lateral geniculate nucleus projects, not only to the striate cortex, but also to the superior colliculus, pretectum, pulvinar and several other thalarnic nuclei. It receives only a few reciprocal fibers from the striate cortex and none from SUMMARY AND CONCLUSIONS the superior colliculus or pulvinar. 6. Extensive projection from the striate Afferent projection to the superior colliculus was investigated by means of the cortex was observed to the following thalNauta-Gygax staining technique in 11cats. amic nuclei: pulvinar, the posterior, supraIn two animals the right optic nerve was geniculate and posterolateral nuclei. These cut; in five animals stereotaxic lesions structures also receive fibers from the were produced in the right lateral geni- superior collicuIus and the lateral genicuculate body; in a single animal, a re- late. LITERATURE CITED stricted stereotaxic lesion was produced in the pulvinar; and in three animals the Altman, J. 1959 A neurophysiological study of the superior colliculus. Ph.D. thesis, New York right striate cortex (lateral and postlatUniversity. era1 gyri) was removed by suction. Fiber Altman, J., and M. B. Carpenter 1961 Fiber projections from these structures to other projections of the superior colliculus in the mesencephalic nuclei and to the diencephcat. J. Comp. New., 116: 157-178. sal nucleus itself, however, showed no degenerated fibers over large areas and only a few degenerated preterminal fibers over limited regions, in particular, its rostra1 and dorsal portions. A few fine degenerated fibers, with suggestions of termination around cells, were seen in parts of the ventral nucleus of the lateral geniculate body. While the lateral geniculate nucleus, whose main outflow is into the striate cortex, receives but a few reciprocal fibers from this region, numerous degenerated preterminal fibers were observed after ablation of the striate cortex on the lesion side in several other thalamic nuclei - the posterior nucleus, the pulvinar, the suprageniculate and posterolateral nu. clei, and also in the pretectal region. Especially striking was the rich corticofugal projection to the posterior nucleus and the pulvinar. It is possible that the postulated reciprocal cortico-thalamic connection within the visual system (cf., Bartley, '59, p. 718) is mediated, at least partly, by way of these nuclei. In the same way, reciprocal cortical connections of the superior colliculus (which receives many corticofugal fibers but does not send fibers either to the cortex directly or to the lateral geniculate nucleus) may be by way of these thalamic nuclei, since all of them receive fibers from the colliculus (Altman and Carpenter, '61 ). Our present findings contradict, incidentally, the claim of Barris, Ingram and Ranson ('35) that the striate cortex sends no fibers to the pretectum, the pulvinar, the posterior and posterolateral nuclei, or the dorsal and ventral nuclei of the lateral geniculate body. PROJECTIONS TO SUPERIOR COLLICULUS 87 Hess, A. 1958 Optic centers and pathways Barris, R. W., W. R. Ingram and S. W. Ranson after eye removal i n fetal guinea pigs. Ibid., 1935 Optic connections of the diencephalon 109: 91-116. and midbrain of the cat. Ibid., 62: 117-153. Hirasawa, K., S. Okano and S. Kamio 1938 Bartley, S. H. 1959 Central mechanisms of Beitrag zur Kenntnis uber die corticalen extravision. In: Handbook of Physiology, section pyramidalen Fasern aus der Area temporalis 1, vol. 1, Neurophysiology. American Physiosuperior (Area 2 2 ) beim Affen. Z. mikr. anat. logical Society, Washington, chap. 30, pp. 713Forsch., 44: 74-84. 740. Beevor, C. E., and V. Horsley 1902 On the pal- Jefferson, G. 1958 Discussion. I n : Henry Ford Hospital International Symposium, Reticular lio-tectal or corticomeseocephalic system of Formation of the Brain. Little, Brown, Boston, fibers. Brain, 25: 436-443. pp. 65-68. Bishop, G. H., and M. H. Clare 1955 Organization and distribution of fibers in the optic Jefferson, J. M. 1940 A study of the subcortical connexions of the optic tract system of tract of the cat. J. Comp. Neur., 103: 269-304. the ferret with special reference to gonadal Bodian, D. 1937 An experimental study of the activation by retinal stimulation. J. Anat., optic tracts and retinal projection of the London, 75: 106-134. Virginia opossum. Ibid., 66: 113-144. Johnson, T. N. 1954 The superior and inferior Brouwer, B., and W. P. C. Zeeman 1926 The colliculi of the mole (Scalopus aquaticus projection of the retina i n the primary optic machrinus). J. Comp. Neur., 101: 765-799. neuron i n monkeys. Brain, 49: 1-35. Juba, A. 1939 Die optischen Verbindungen der Brouwer, B., W. P. C. Zeeman and A. W. M. oberen Vierhiigelgegegnd. 2. ges. Neurol. Houwer 1923 Experimentell-anatomischeUnPsychiat., 164: 273-285. tersuchungen uber die Projektion der Retina auf die primaren Opticuszentren. Schweiz. Krieg, W. J. S. 1947 Connections of the cerebral cortex. I. The albino rat. C. Extrinsic Arch. Neurol. Psychiat., 23: 118-137. connections. J. Comp. Neur., 86: 267-394. Bucher, V. M., and S. M. Biirgi 1950 Some observations on the fiber connections of the di- Lashley, K. S. 1934 The mechanism of vision. VII. The projection of the retina upon the and mesencephalon i n the cat. I. Fiber conprimary optic centers in the rat. Ibid., 59: nections of the optic tectum. J. Comp. Neur., 341-3 73, 93: 139-172. Burgi, S. 1957 Das Tectum opticum. Seine Leblanc, L. 1928 Recherches sur la systematisation des voies corticotectales. La Cellule, Verbindungen bei der Katze und seine Bedeut38: 353-384. ung beim Menschen. Dtsch. Z. Nervenheilk., Loepp, W. H. 1912 Ueber die zentralen Opti176: 701-729. cusendigung beim Kaninchen. Anat. Anz., 40: Cajal, S. Ram6n Y. 1952-1955 (1909-1911) 309-323. Histologie du systBme nerveux de l'homme et des vertkbrks, 2 vols. Consejo de Investiga- Mettler, F. A. 1935 Corticifugal fiber connections of the cortex of Macaca mulatta. A. The ciones Cientificas, Madrid, vol. 2, chap. 9, pp. occipital region. J. Comp. Neur., 61: 221-256. 175-193. Castaldi, L. 1923, 1924, 1926 Studi sulla strut- Minkowski, M. 1913 Experimentelle Untersuchungen iiber die Beziehungen der Grosshirntura e sullo sviluppo del mesencefalo. Ricerche rinde und der Netzhaut zu den primaren in Cavia Cobaya. Parte 1, 2, 3. Arch. ital. anat. optischen Zentren, besonders zum Corpus genembryol., 20: 23-225; 21: 172-263; 23: 481iculatum externum. Arb. hirnanat. Inst., 609. Ziirich, 7: 259-362. Clark, W. E. Le Gros 1942 Visual centers of 1920 Ueber den Verlauf, die Endigung the brain and their connections. Physiol. Rev., und die zentrale Reprasentation von gekreuzten 22: 205-232. und ungekreuzten Sehnervenfasern bei einiCrosby, E. C., J. W. Henderson 1948 The mammalian midbrain and isthmus regions. 11. Figen Saugetieren und beim Menschen. Schweiz. Arch. Neurol. Psychiat., 6: 201-252; 7: 268ber conections of the superior colliculus. B. 303. Pathways concerned in automatic eye moveMonakow, C. von 1889 Experimentelle unct ments. J. Comp. Neur., 88: 53-91. pathologisch-anatomische Untersuchungen iiber Ferrier, D., and W. A. Turner 1897 An experidie optischen Centren und Bahnen. Arch. Psymental research upon cerebrocortical afferent chiat., 20: 714-787. and efferent tracts. Proc. Roy. SOC., London, Nauta, W. J. H., and V. N. Bucher 1954 Effer62: 1-3. ent connections of the striate cortex in the Glees, P. 1941 The termination of optic fibres albino rat. J. Comp. Neur., 100: 257-286. i n the lateral geniculate body of the cat. J. Nauta, W. J. H., and P. A. Gygax 1954 Silver Anat., London, 76: 65-92. impregnation of degenerating axons in central Gudden, B . von 1886 Demonstration der Sehfanervous system. A modified technique. Stain sern und Pupillarfasern des Nervus opticus. Tech., 29: 91-93. Sitzungsb. Gesellsch. Morphol. Physiol., I : 169. O'Leary, J. L. 1940 A structural analysis of Hayhow, W. R. 1958 The cytoarchitecture of the lateral geniculate body in the cat in relathe lateral geniculate nucleus of the cat. J. Comp. Neur., 73: 405-430. tion to the distribution of crossed and unOverbosch, J. F. A. 1927 Experimenteel-anatcrossed optic fibers. J. Comp. Neur., 110: 1-63. omische onderzoekingen over de projecfie der 1959 An experimental study of the accessory optic fiber system in the cat. Ibid., retina in het centrale zenuwstelsel. Academisch proefschrift, Amsterdam. 113: 281-313. 88 JOSEPH ALTMAN Pavlow, M. 1900 Les voies descendantes des tubercules quadrijunleaux supCrieurs, 1-11, Le Nevraxe, I : 57-75, 129-136. Poljak, S. 1926 Die Verbindungen der Area striata (intrahemisphaerale, kommissurale, palliodienzephalische, palliotektale Fasern) bei der Katze und deren funktionelle Bedeutung. 2.ges. Neurol. Psychiat., 100: 545-563. 1928 An experimental study of the association, callosal and projection fibers of the cerebral cortex of the cat. J. Comp. Neur., 44: 197-258. Polyak, S. 1957 The vertebrate visual system. H. Kliiver, ed. Univ. of Chicago Press, Chicago, chap. 6, pp. 288-389. Probst, M. 1902 Ueber den Verlauf der centralen Sehfasern (Rinde-Sehhiigelfasern) und deren Endigung im Zwischen- und Mittelhirne und uber die Associations- und Commissuren- fasern der Sehsphare. Arch. Psychiat. Nervenkr., 35: 22-43. Rioch, D.M. 1929 Studies on the diencephalon of carnivora. I. Nuclear configuration of the thalamus, epithalamus and hypothalamus of dog and cat. J. Comp. Neur., 49: 1-120. Takebayashi, H. 1957 Superior colliculus, playing roles in the optokinetic and neurovegetative mechanism. Wakayama Med. Rep., 4 : 1-12. Tsai, C. 1925 The descending tracts of the thalamus and midbrain of the opossum, Didelp h i s virginiana. J. Comp. Neur., 39: 317-348. Tsang, Y.-(2. 1937 Visual centers in blinded rats. Ibid., 66: 211-261. Whitlock, D. G.,and W. J. H.Nauta 1956 Subcortical projections from the temporal neocortex i n Macaca mulatta. Ibid., 106: 183-212. PLATE 1 EXPLANATION OF FIGURES Low power microphotographs and drawings illustrating some of the lesions produced. Cat C-439. Lesion in the right lateral geniculate nucleus, pars dorsalis. Frozen section; Nissl. x 5. Cat C-434. Less extensive lesion in right lateral geniculate nucleus, pars dorsalis. Frozen section; Nissl. X 5. Cat C-438. Lesion in right pulvinar. Frozen section; Nissl. X 5. Cat C-429. Degenerated fibers in the left (severe) and right (milder) optic tract, following severance of the right optic nerve. Nauta-Gygax. x 10. Cat C-426. Schematic drawing, illustrating extensive removal of the striate cortex in this animal. Cat C-411. Schematic drawing, illustrating partial removal of the striate cortex in this animal. PROJECTIONS TO SUPERIOR COLLICULUS PLATE 1 Joseph Altman 89 PLATE 2 EXPLANATION OF FIGURES Low and high power microphotographs illustrating axonal and preterminal degcncration in mesencephalic and dicncephalic regions following severance of the right optic nerve. 7 Cat C-429. Degcneratcd fibers in and surrounding the contralateral lateral geniculate nucleus. Nauta-Gvgax. X 73. 8 Cat C-429. Degencrated fibers surrounding the contralateral lateral geniculate nucleus (upper part) and i n the brachiurn of the superior colliculus at the level of the pretectal region (lower part). NautaGygax. X 73. 9 Cat C-428. Degenerated fibers in the contralateral brachium of the superior colliculus and in the lateral parts of the superior colllculus. Nauta-Gygax. X 73. 10 Cat C-429. Degenerated fibcrs i n the stratum opticum i n the contralateral superior colliculus. Nauta-Gygax. X 73. 90 11 Cat C-428. Deqenerated fibers in the contralateral superior colliculus at higher magnification. Nauta-Gygax. X 360. 12 Cat C-429. Degenerated fibers in the contralateral prctcctal region at higher magnification. Nauta-Gygax. X 360. PROJECTIONS TO SUPERIOR COLLICULUS Joseph Altman PLATE 2 91 PLATE 3 EXPLANATION OF FIGURES High power microphotographs illustrating axonal and preterminal degeneration. Figures 13-14: degeneration iollowing severance of the right optic nerve. Figures 15-18 : degeneration following coagulation of the lateral geniculate nucleus, pars dorsalis. 13 Cat C-429. Degenerated “aberrant” optic fibers above the chiasma i n the hypothalamus. Nauta-Gygax. x 360. 14 Cat C-429. Degenerated optic fibers i n the contralateral medial accessory tract. Nauta-Gygax. X 360. 15 Cat C-439. Degenerated fibers in the ipsilateral superior colliculus following lesion in the lateral geniculate nucleus, pars dorsalis. Nauta-Gygax. x 360. 16 Cat (2-439. Degenerated fibers in the ipsilateral pretectal area following lesion i n the lateral geniculate nucleus, pars dorsalis. NautaGygax. x 360. 17 Cat C-439. Degenerated fibers in the pars ventralis of the lateral geniculate nucleus following lesion in the pars dorsalis. Nauta-Gygax. x 360. 18 Cat C-439. Degenerated fibers in the ipsilateral pulvinar following lesion in the lateral geniculate nucleus, pars dorsalis. Nauta-Gygax. X 360. 92 PROJECTIONS TO SUPERIOR COLLICIJLUS Joseph Altman PLATE 3 93 PLATE 4 EXPLANATION OF FIGURES Low and high power microphotographs illustrating axonal and preterminal degeneration. Figures 19-22: Degeneration following partial removal of the right striate cortex (lateral and postlateral gyri). Figures 23-24 : Degeneration following lesion in the right pulvinar. 19 Cat C-427. Degenerated fibers in ipsilateral superior colliculus (particularly abundant in stratum griseuin intermediale; lower half of picture) following striate cortex lesion. Nauta-Gygax. x 73. 20 Cat C-426. Degenerated fibers in ipsilateral superior colliculus following striate cortex lesion, at higher magnification. Nauta-Gygax. X 360. 21 Cat C-427. Degenerated fibers in ipsilateral lateral geniculate nucleus, pars dorsalis, following striate cortex lesion. Nauta-Gygax. X 360. 94 22 Cat C-437. Degenerated fibers in ipsilateral posterior nucleus of the thalamus following striate cortex lesion. Nauta-Gygax. x 360. 23 Cat C-438. Degenerated fibers in ipsilateral superior colliculus following lesion in pulvinar. Nauta-Gygax. X 360. 24 Cat C438. Degenerated fibers in the stratum griseum intermediale of the ipsilateral superior colliculus following lesion in pulvinar. Nauta-Gygax. x 360. PROJECTIONS TO SUPERIOR COLLICULUS Joseph Altman PLATE 4 95