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Distribution of cerebellar fiber terminals in the midbrain visuomotor areas: An autoradiographic study in the cat
Brain Research, 238 (1982) 353-370 Elsevier Biomedical Press
353
D I S T R I B U T I O N OF C E R E B E L L A R F I B E R T E R M I N A L S IN T H E MIDBRA1N V I S U O M O T O R AREAS: A N A U T O R A D I O G R A P H I C S T U D Y IN T H E CAT
TETSUO SUGIMOTO, NOBORU MIZUNO and KUNIKO UCH1DA Department of Anatomy (lst Division), Faculty of Medicine, Kyoto University, Kyoto 606 (Japan)
(Accepted October 22nd, 1981) Key words: cerebellar nuclei - - superior colliculus - - pretectum - - oculomotor nucleus - - trochlear
nucleus - - Edinger-Westphal nucleus - - autoradiography - - cat
SUMMARY Cerebellar fibers to the midbrain visuomotor areas were traced in the cat autoradiographically after injections of tritiated amino acids into individual cerebellar nuclei. Fibers from the dentate (DN), anterior interpositus (AIN) and posterior interpositus (PIN) nuclei were distributed contralaterally, while those from the fastigial nucleus (FN) bilaterally. The F N fibers appeared to arise mainly from the caudal half of the FN. In the superior colliculus (SC), the F N or D N fibers were more numerous than the PIN fibers, and the areas of termination of the F N fibers were located more medially than those of the DN and P I N fibers. These cerebellotectal fiber terminals were in the intermediate and deep SC layers; clustering of terminal silver grains was noted in the FN and D N fibers-recipient areas in the intermediate gray layer. In the pretectum, the D N fibers terminated ventrally in the reticular part of the anterior pretectal nucleus and the posterior pretectal nucleus. The AIN fibers terminated ventrally in the compact part of the anterior pretectal nucleus and the posterior pretectal nucleus. The nucleus of the posterior commissure received cerebellar fibers chiefly from the DN, and additionally from the FN. The nucleus of Darkschewitsch and the interstitial nucleus of Cajal received fibers from all cerebellar nuclei. No cerebellar fibers terminated in the extraocular motor nuclei and the Edinger-Westphal and anteromedian nuclei.
INTRODUCTION Cerebellar projections to the superior colliculus, pretectum and other mesencephalic regions have been the subject of studies by anterograde degeneration methods in several mammals and by the autoradiographic tracing technique in the monkey and 0006-8993/82/0000-0000/$02.75 © Elsevier Biomedical Press
354 rat (for reviews, see refs. 5.9. 13.34, 4 3 . 4 4 and 52). Although the general patterns ot termination of cerebellar fibers in the midbrain appear to be fairly well-known, the data about details o f the t o p o g r a p h y o f fiber terminals from each of the.. cerebeltar nuclei are still lacking. In a previous study 46, the precise t o p o g r a p h y of termination of the cerebellothalamic fibers was studied in the cat by the autoradiographic tracing method. In the present study, in turn. an attempt was made to obtain more precise data about distribution o f fiber terminals from each of the cerebellar nuclei to the midbrain regions, especially to the visuomotor areas, such as the superior colliculus. pretectum and o c u l o m o t o r and trochlear nuclei. MATERIALS AND METHODS In 14 adult cats (body weight: 2100-4700 g) anesthetized with intraperitoneal sodium pentobarbital (35 mg/kg), a single unilateral injection o f 0.07-0.4 #l (50-100 /~Ci//A) of a mixture o f u-[3H]leucine and u-[3H]proline (New England Nuclear) was made stereotaxically into the fastigial (FN), dentate (DN), anterior interpositus (AI N~ or posterior interpositus (PIN) nucleus: in an additional 2 cats, injections were made bilaterally into the dentate and interpositus nuclear regions (Table 1). All injections were made gradually over 10-20 rain via a 25-gauge injection needle attached to a stereotaxically m o u n t e d I-/A H a m i l t o n syringe, and the syringe was left in place for an TABLE I Materials used in the present study Cat no.
3* 9 12 t3 R L 21 84* 86* 88* 89* 90* 92* 93* 94* R L 97* 99*
Site of injection
Amount of injected isotope (f~Ci)
Survival periods' (days)
FN DN AIN, PIN AIN DN, AIN, PIN DN, PIN DN PIN, DN DN FN PIN FN DN, PIN, A1N AIN DN, PIN, AIN DN, A1N DN AIN, PIN
30 12 12 24 32 24 8 30 18 30 28 40 40 30 40 40 7 25
13 10 6 12 12 12 9 10 8 23 8 7 20 10 20 20 10 7
In Cats 13 and 94, isotope injections were made bilaterally into the right (R) and left (L) dentate and interpositus nuclear regions (cf. Fig. i). The cats marked With asterisks were also. Used in:ihe previous study4~.
355 A
,,.
1
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I 3
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Fig. 1. The sites of the isotope injection in the cerebellar nuclei (shaded areas) in the cats used ill the present study. In each of the columns of A, B and C, selected sections through the cerebellar nuclei of one animal are represented and arranged in the rostrocaudal direction. The bilateral injections in Cats 13 and 94 are represented on one side (cf. Table I). additional 15 min to reduce the contamination of overlying brain tissue. After a survival period of 6-23 days, the cats were deeply anesthetized and perfused through the ascending aorta with 2 liters of l0 /o °/buffered formalin. After sucrose infiltration, the brains were sectioned serially at 35 # m in the frontal plane on a freezing microtome. The sections were mounted onto gelatin-coated slides, defatted in xylene, coated with photosensitive emulsion (Kodak NTB-2, NTB-3, or Sakura NR-M2), and exposed for 4-8 weeks at 4 °C. The sections were then developed in K o d a k D-19, fixed, washed, stained through the emulsion with cresyl violet or neutral red and examined using both light-field and dark-field illumination. The locations of the injection sites and the radioactive labeling were mapped onto enlarged outline drawings of selected sections with the aid of a projection apparatus. In this communication, the terminology of Kanaseki and Sprague 27, Itoh 25, and Avendafio and Juretschke v is used for the pretectal nuclei and tectal laminae. As described previously 4~, only randomly arranged silver grains with density exceeding background
356
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Fig. 2. Distribution of transported label after injecting isotope into the left fastigial nucleus in Cat 88. Terminal silver grains and labeled fibers of passage are represented with dots and broken lines, respectively, in this and the subsequent figures. The projection drawings of frontal sections are arranged from rostral ( A / t o caudal (H).
357 were considered as terminal grains, and silver deposits on identifiable fiber systems were regarded as labeling of fibers of passage. RESULTS
ln/ections into the fastigial nucleus (FN) In 2 cats (Cats I and 88), the isotope injection was centered on the left FN throughout its rostrocaudal extent (Fig. 1A). Most FN fibers crossed the midline toward the opposite side at the rostral levels of the FN, and left the cerebellum through the uncinate fasciculus which was located dorsomedially to the brachium conjunctivum (BC). The FN fibers ascended through the tegmental regions of the midbrain, and were divided into the major ascending and the minor descending components at the caudal levels of the superior colliculus (SC). Some of the latter components appeared to terminate in the tegmental regions around the BC including the pedunculopontine tegmental nucleus (Fig. 2H); the rest were further traced to the lower pontine levels. The ascending FN fibers terminated in the mesencephalic central gray (CG) and the medial two-thirds of the SC. The terminals in the C G were distributed in the dorsal and dorsolateral portions of the CG as well as in the ventral regions dorsal to the oculomotor nucleus (Fig. 2B-H). In the SC, rather sparse terminal grains were seen in the intermediate and deep gray layers (Fig. 2C H); terminal silver grains in the deep gray layer were distributed diffusely, whereas those in the intermediate gray layer were seen in equivocal patchy clusters (Fig. 2E). Some ascending FN fibers were observed to run dorsally around the C G and to cross the midline to terminate in the SC and the dorsal portions of the C G ipsilateral to the isotope injection (Fig. 2D-H). Some of these
Fig. 3. Dark-field photomicrograph showing terminal silver grains in the medial portions of the intermediate SC layer in Cat 88 injected with the isotope contralaterally in the FN. Arrowheads point to collaterals arising from a labeled fiber, s, superficial layer; p, deep layer, :~: 50.
358
Fig. 4. Distribution of transported label after injecting isotope bilaterally into the dentate and interpositus nuclear regions in Cat 13. The projection drawings of frontal sections are arranged from rostral (A) to caudal (H). fibers appeared to send collaterals radiating toward the dorsal surface of the SC (Fig. 3). At the caudal SC levels, these terminal silver grains in the SC were more numerous than those in the SC contralateral to the isotope injection, but they became less numerous in the rostral levels of the SC (Fig. 2C-H). At more rostral levels, labeled F N fibers were seen to ascend toward the
359 diencephalic regions through the dorsomedial tegmental regions between the red nucleus and the SC, contralaterally to the isotope injection. These fibers appeared to send axon collaterals and/or terminals to the dorsomedial midbrain tegmental regions, the nucleus of Darkschewitsch, the interstitial nucleus of Cajal, and the dorsomedial portions of the field of Forel, contralateral to the isotope injection (Fig. 2A-C). On the other hand, some labeled fibers in the SC were seen to run through the SC rostrally toward the pretectal regions; some labeled fibers were also observed to run through the posterior commissure from the pretectal regions contralateral to the isotope injection toward the opposite side (Fig. 2B). In the pretectum, the FN fibers were observed to terminate bilaterally in the nucleus of the posterior commissure, and possibly in the reticular part of the anterior pretectal nucleus (Fig. 2B). When the site of the isotope injection was localized in the rostral half of the FN (Cat 90) (Fig. IA), a few possible terminal silver grains were seen in the CG, but no terminals were found in the SC and pretectum. The FN fibers ascending to the mesencephalic regions appeared to arise mostly from the caudal half of the FN. In all cats used in the present study, no FN fibers were found to terminate in the trochlear nucleus, oculomotor nucleus, Edinger-Westphal nucleus, anteromedian nucleus and red nucleus.
Injections into the dentate and interpositus nuclear regions In Cat 13, the isotope injections were made bilaterally into the dentate and interpositus nuclear regions. On the left side, caudolateral portions in the dentate (DN) and posterior interpositus (PIN) nuclei were involved in the site of injection (13L in Fig. 1A). On the right side, the isotope injection was centered more rostromedially and covered the caudal portions of the DN and anterior interpositus nucleus (AIN), and the lateral portions of the PIN (13R in Fig. IA). The pattern of distribution of silver grains indicating the ascending cerebellar fibers from the DN and interpositus nuclear regions in Cat 13 is shown in Fig. 4. In the mesencephalic central gray (CG), terminal silver grains were distributed mainly in the lateral CG regions and the ventral CG regions dorsal or dorsolateral to the oculomotor nucleus (Fig. 4D-H). In the superior colliculus (SC), terminal silver grains were distributed mainly in the lateral two-thirds of the intermediate gray layer and the lateral one-third of the deep gray layer, at the levels ofth~ rostral one-fourth of the SC (Fig. 4E H). The terminal silver grains in the SC were distributed rather sparsely in the deep gray layer, whereas they shgwed a clear tendency of clustering in the deeper portions of the intermediate gray layer. Labeled fibers of passage were often seen in the ventrolateral two-thirds of the SC, and rarely in the media[ portions of the SC, commissure of the SC, and posterior commissure. In the pretectum, terminal silver grains were distributed in the cgmpact and reticular parts of the anterior pretectal nucleus, posterior wctectal nucleus, and nucleus of the posterior commissure on the left side, and in the reticular part of the anterior pretectal nucleus, posterior pretectal nucleus, and nucleus of the posterior commissure on the right side (Fig. 4C-G). On both sides, distribution of terminal silver grains in the anterior and posterior pretectal nuclei was almost confined to the
360 ventral two-thirds of these nuclei. The terminal silver grains in the nucleus of the posterior commissure were seen in the rostrodorsal portions of the nucleus. Terminal silver grains were also seen in the red nucleus: these grains were intermingled with m a n y labeled fibers of passage. On the left side, the terminal silver grains were concentrated on the dorsal and dorsomediat portions of the parvocellular and magnocellular red nuclear regions. On the right side, the terminal labeling was almost confined to the dorsal or dorsolateral portions of the parvocellular red nucleus. Many labeled fibers running through the red nucleus appeared to course toward the SC and/or the pretectum : some of these fibers ended in the mesencephalic tegmental regions ventral to the ventral border of the SC. Additionally, terminal silver grams were seen in the whole areas of the nucleus of Darkschewitsch. In the interstitial nucleus of Cajal. terminal labeling occurred mostly in the dorsal and dorsomedial portions of the nucleus. No labeling was observed in the trochlear nucleus, oculomotor nucleus, Edinger-Westphal nucleus and the anteromedian nucleus. In Cat 94, a large amount of the isotope was injected bilaterally: on the left side. the site of injection covered the dorsal half of the D N and the lateral portions of the AIN, and on the right side. it covered the entire DN, lateral half of the AIN, lateral one-third of the PIN, and the group y of the vestibular nuclear complex, in Cat 92. a large amount of the isotope was injected unilaterally; the site of injection covered the entire DN. caudal half of the A1N. lateral one-third of the PIN, and the group y of the vestibular nuclear complex (Fig. IB, C). In both of these cats, terminal silver grains were observed densely in the reticular and compact parts of the anterior pretectal nucleus as well as in the posterior pretectal nucleus. The pattern of distribution of terminal silver grains in the midbrain regions, however, was almost the same as seen in Cat 13 (Fig. 4); the only difference was the occurrence of terminal silver grains in the trochlear and oculomotor nuclei on the left side in Cat 94 and in those nuclei contralateral to the isotope injection in Cat 92 (Fig. 5). These terminal fibers in the
a
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e
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0 Fig. 5. Distribution of terminal silver grains in the oculomotor (a-e) and trochlear (f) nuclei in Cat 92, The drawings are arranged from rostral (a) to caudal if).
361
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Fig. 6. Distribution of labeled fibers (A-D) in Cat 3 injected with the isotope contralaterally in the DN (a, b), as indicated in Fig. ]. extraocular motor nuclei appeared to arise contralaterally from the group y of the vestibular nuclear complex. The terminal silver grains in the oculomotor nucleus in Cats 94 and 92 were distributed in the whole mediolateral extent of the nucleus at the caudal levels, and in the medial half of the nucleus at the middle levels; no labeling was found, however, in the rostral one-third levels of the nucleus. In the cats injected bilaterally with a rather large amount of the isotope, the general pattern of fiber projections from the cerebellar nuclei was observed easily, but the differences among the patterns of fiber projections from the DN, AIN or PIN were not marked. Therefore, the patterns of fiber projections from each of the DN, AIN and PIN will be described in the cats injected with the isotope unilaterally into each of the DN, AIN and PIN.
Injections into the dentate nucleus (DN) In 4 cats (Cats 3, 21, 86 and 97), the site of isotope injection was confined within
362 the DN (Fig. IA. CI. In these cats. terminal labeling in the midbrain regions was seen contralaterally in the central gray (CG) ~mperior collicutus (SCI. pretectum, red nucleus, tegmental regions, nucleus of Darkschewitsch, interstitial nucleus of Cajal. and field of Forel (Fig. 6). In the SC. terminal silver grains were distributed in the lateral two-thirds of the intermediate and deep gray layers ; they were almost confined to the rostral one-fourth levels of the SC (Fig. 6C. D). In the intermediate gray layer, a patchy pattern of terminations was seen in the deepest tier along the mediolateral axis of the intermediate gray (Fig. 7). No labeling was found in the commissure of the SC. In the pretectum, terminal silver grains were found in the rostrodorsal portions of the nucleus of the posterior commissure as well as in the small ventral regions m the posterior pretectal nucleus and reticular part of the anterior pretectal nucleus: no labeling was seen in the compact part of the anterior pretectal nucleus ~Fig. 6A. B), Terminal labeling in the red nucleus was almost confined to the parvocellular regions (Fig. 6B). Terminal labeling was seen m the nucleus of Darkschewitsch and the interstitial nucleus of Cajal (Fig. 6A. B), but no silver grains were observed in the trochlear nucleus, oculomotor nucleus. Edinger Westphal nucleus and anteromedian nucleus. Injections into the anterior interpositus nucleus / AI N ) In 2 cats (Cats 12 and 93), the site of the isotope injection was confined within the AIN (Fig. 8a). In another 2 cats (Cats 9 and 99~. the isotope injection was centered on the AIN. but the site of the injection extended into small parts of the posterior interpositus nucleus (Fig. lB. C~. In the former 2 cats (Cats 12 and 93), terminal silver
Fig. 7. Dark-field photomicrograph showing terminal silver grains in the lateral portions of the intermediate SC layer in Cat 21 injected with the isotope contralateraliy in the DN. Axrows indicate clusters of terminal sih er grams m the deepest tier of the intermediate gray layer, s, superficial layer; p, deep layer. 50.
363
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Fig. 8. Low-power photomicrographs showing the sites of rejections in the A|N (a) of Cat 93 and the PIN (b) of Cat 89. De, nucleus of Deiters. : 20. grains were seen in the pretectum, midbrain tegmentum, red nucleus and nucleus of Darkschewitsch (Fig. 9). In addition to these regions, terminal labeling was also noted in the mesencephalic central gray and interstitial nucleus of Cajal in the latter 2 cats (Cats 9 and 99). The density of silver grains in the SC was above background levels only in Cat 99; these grains were seen sparsely in the intermediate gray layer at the rostralmost levels of the SC. In the pretectum, terminal silver grains were seen mainly in the ventral half regions in the posterior pretectal nucleus and the cgmpact part of the anterior pretectal nucleus, but no terminal labeling was noted in the reticular part of the anterior pretectal nucleus (Fig. 9A, B). The nucleus of the posterior commissure was labeled only in Cats 9 and 99. Terminal labeling in the red nucleus was seen massively in the ventral and ventrolateral parts of the magnocellular regions (Fig. 9A, B), and that in
364
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Fig. 9. Distribution of labeled fibers (A-C) in Cat 93 injected with the isotope contralaterally in the AIN (a, b), as indicated in Fig. 1.
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Fig. 10. Distribution of labeled fibers (A-C) in Cat 89 injected with the isotope contralateratly in the PIN (a, b), as indicated in Fig. 1.
365 the nucleus of Darkschewitsch was observed most markedly in the rostral regions of the nucleus (Fig. 9A). No terminal labeling was noted in the trochlear, oculomotor, Edinger-Westphal and anteromedian nuclei.
Injections into the posterior interpositus nucleus (PIN) In 2 cats (Cats 84 and 89), isotope injection was centered on the PIN (Fig. 8b); in one of these cats (Cat 84), the isotope deposits also involved small parts of the DN (Fig. 1A). Terminal labeling was seen in the mesencephalic central gray, tegmental regions, SC, red nucleus, nucleus of Darkschewitsch, nucleus of the posterior commissure and interstitial nucleus of Cajal (Fig. 10). Terminal silver grains in the SC were distributed mainly in the ventrolateral portions of the intermediate and deep gray layers at the rostral one-fourth levels of the SC (Fig. 10B). In the pretectum, terminal labeling was found sparsely in the nucleus of the posterior commissure (Fig. 10A). Many terminal silver grains were seen in the medial and dorsomedial parts of the magnocellular parts of the red nucleus (Fig. 10B, C), but no terminal labeling was found in the trochlear, oculomotor, Edinger-Westphal and anteromedian nuclei. DISCUSSION
Cerebellar fibers to the superior colliculus ( SC) Although the existence of cerebellotectal fibers to the SC appears to be established in the cat 3,5,6A4,as,5°,52, rat 1~,19, monkey T M and opossum 32,53 by the anterograde degeneration and the autoradiographiO, 13 methods, some discrepancies and uncertainties are still pending concerning the origins and terminations of these fibers. The crossed and uncrossed cerebellotectal fibers from the fastigial nucleus (FN) were reported in the monkey 9 and cat 3,6, and the crossed tectal fibers from the dentate nucleus (DN) were shown to exist in the opossum 32 and raO 3. On the other hand, Angaut 5 and Chan-Palay 13 could not obtain conclusive evidences for the existence of the dentatotectal fibers in the cat and monkey, respectively. The present data, however, showed that the cerebellotectal fibers to the SC in the the cat arose mainly from the DN and FN, and additionally from the posterior interpositus nucleus (PIN). Although Angaut4, 5 reported that the cerebellotectal fibers from the interpositus nuclei arose from the anterior interpositus nucleus (AIN) rather than the PIN, the present study provided no confirmative evidence indicating the existence of the cerebellotectal fibers from the AIN. In the previous studies performed by the degeneration methods, the cerebellotectal fibers were reported to end in the deep layers of the SC in the rat I0, cat~,5, 6 and monkey 9. According to the other degeneration study in the opossum 32 and the autoradiographic study in the rat 13, however, the cerebellotectal fibers from the DN ended in the intermediate gray layer of the SC. The present data showed that the cerebellotecta[ fibers were distributed mainly to the intermediate gray layer, and sparsely to the deep gray layer of the SC. In the monkey, some neurons in the intermediate gray layer of the SC were found to discharge before saccadic eye movements ~5,4°-4'~,~4. The neurons sending their axons around the extraocular motor
366 nuclei were also found in the intermediate gray layer of the SC in the catlL Therefore the cerebellar fibers to the intermediate gray layer of the SC might be considered to exert some regulatory influences upon such so-called eye movement cells The FN- and DN-tectal fiber terminals showed the tendency of clustering in the intermediate gray layer of the SC, especially in the deepest tier of the intermediate gray layer. Similar findings were reported in the recent autoradiographic studies concerning the trigeminotectal'~4, 49 and nigrotecta123, 26 fibers, which also ended in the intermediate gray layer of the SC. The functional meanings of these data sugg~ting the discontinuity of afferent fiber terminations in the intermediate gray layer of the SC still remain to be elucidated. Cerebellar fibers to the pretectum Cerebellopretectal fibers have been described, but rather anecdotally, in the opossum 32, rat 13,19, monkey 9.12,33,34,43 and cat 14,50. Although most of the previous investigators agreed that the cerebellopreteetal fibers ended in the nucleus of the posterior commissure, the termination of the cerebellopretectal fibers in the anterior pretectal nucleus was also reported in the rat ~9 and opossum ~2. In these previous studies, the cerebellopretectal fibers to the nucleus of the posterior c~mmissure were reported to arise from the DN and interpositus nuclei14, 33,43, from the DN12,13. or from the FN 9,5°. On the other hand, the present data showed that the nucleus of the posterior commissure received fibers from the DN and FN. and possibly from the AIN and PIN, and that the anterior and posterior pretectal nuclei received fibers from the DN and A1N; in the anterior pretectal nucleus, the D N and AIN fibers ended in the reticular and compact parts, respectively. The termination of the DN fibers in the ventrolateral part of the anterior pretectal nucleus was also reported in the opossum~L In the ventral regions of the anterior and posterior pretectal nuclei, where the cerebellar fibers were seen to terminate in the present study, no retinal fibers seem to end in the catll,z7, 3°. On the other hand, the area of distribution of fibers from the ventral lateral geniculate nucleus 18,2s,4v and the sensorimotor and visual cortical areasl0,Z0,'~9,,~1 appears to include the ventral regions of the anterior and posterior pretectal nuclei. In these pretectal regions, convergence of direct inputs from the cerebellar nuclei, cerebral cortical areas and the ventral lateral geniculate nucleus might occur. Cerebellar.fibers to the oculornotor and trochlear nuclei In a cat (Cat 92) injected with the isotope around the DN, terminal labeling occurred contralaterally in the oculomotor and trochlear nuclei. In other cats which were injected with the isotope similarly around the D N (Cats 3, 13, 21, 86 and 97), however, no terminal silver grains were found in these cranial nerve nuclei, In the neuronal structures involved in the injection site in Cat 92, the group y of the vestibular nuclear complex was found to be the only nucleus that was not involved in the injection sites of the other cats. Similar terminal labeling in the oculomotor and trochlear nuclei was also seen in another cat (Cat 94) which was injected with the isotope bilaterally around the DN. In this cat the group y of the vestibular nuclear
367 complex was involved in the injection site on the right side, and the terminal labeling in the oculomotor and trochlear nuclei was observed only on the left side. The fiber terminals seen in the oculomotor and trochlear nuclei in Cats 92 and 94 were thus assumed to derive contralaterally from the group y of the vestibular nuclear complex. In accordance with the present results, afferent fibers from the group y to the oculomotor and trochlear nuclei have been reported in the monkey 44. In the rat, the fibers arising from the group y were traced contralaterally only to the dorsomedial part of the oculomotor nucleus 19. The medial regions of the oculomotor nucleus, where the terminals of fibers arising from the group y were observed in the present study, appeared to contain the motoneurons supplying the superior rectus eye muscle1,92, a6,4s. Thus, the group y of the vestibular nuclear complex appears to give rise to afferent fibers to the motoneurons innervating the superior rectus and superior oblique eye muscles, and to be possibly involved in the control mechanisms of vertical eye movements.
Cerebellar fibers to other midbrain regions In the present study, the nucleus of Darkschewitsch, interstitial nucleus of Cajal and the mesencephalic central gray regions were found to receive cerebellar fibers from all cerebellar nuclei; bilaterally from the FN and contralaterally from the DN, AIN and PIN. Of these cerebellar fibers, the DN fibers terminating chiefly in the rostral portions of the nucleus of Darkschewitsch were most numerous. in agreement with the previous studies in the cat z,4,5,15,16,37,a9,52 and monkey TM 43, the parvocellular and magnocellular red nuclei were observed to receive cerebellar fibers contralaterally from the DN and the interpositus nuclei, respectively. No FN fibers, however, were found to end in the red nucleus, as reported in the cat 6,5°,~2 and opossum 3'~. The Edinger Westphal and/or anteromedian nuclei were reported to receive cerebellar fibers in the eat14, ~0 and rat 13. No such terminals, however, were observed in the present study, supporting the other reports in the cat 4 ~,38 and monkey 13,34. The ventral regions of the mesencephalic central gray close to the Edinger-Westphal and anteromedian nuclei, however, were found to receive the cerebellar fibers bilaterally from the FN and contralaterally from the DN and/or the interpositus nuclei. These regions of the central gray have been known to contain preganglionic neurons sending their axons ipsilaterally to the ciliary ganglion31, 4~. The cerebellar nuclei, thus, might exert direct regulatory influences on the reflex system of the intrinsic eye muscles through the projections to the mesencephalic central gray 8. ACKNOWLEDGEMENTS The photographic work of Mr. Akira Uesugi and the support of the Niwa Medical Research Foundation are gratefully acknowledged.
368 LIST OF ABBREVIATIONS AIN AM BC CG CP CM CSC De DN EW FF FN Hb HI i lp LGd LGv MG ML ND N1C NOT
anterior interpositus nucleus anteromedian nucleus brachium conjunctivum central gray cerebral peduncle centre median nucleus commissure of the superior colliculus nucleus of Deiters dentate nucleus Edinger-Westphal nucleus field of Forel fastigial nucleus habenular nucleus habenulo-interpeduncular tract intermediate gray layer of the superior colliculus interpeduncular nucleus dorsallateral geniculate nucleus ventral lateral geniculate nucleus medial geniculate nucleus medial lemniscus nucleus of Darkschewitsch interstitial nucleus of Cajal nucleus of optic tract
NPC NRT OT p Pac Par PC Pf PIN Pm PN Pp RN s SC SN V 3 4
nucleus of the posterior commissure nucleus reticularis tegmenti pontis optic tract deep gray layer of the superior colliculus compact part of the anterior pretectal nucleus reticular part of the anterior pretectal nucleus posterior commissure parafascicular nucleus posterior interpositus nucleus medial pretectal nucleus pontme nuclei posterior pretectal nucleus red nucleus superficial gray layer of the superior colliculus superior colliculus substantia nigra third ventricle oculomotor nucleus trochlear nucleus
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369 14 Cohen, D., Chambers, W. W. and Sprague, J. M., Experimental study of the efferent projections from the cerebellar nuclei to the brainstem of the cat, J. comp. Neurol., 109 (1958) 233-259. 15 Courville, J,, Somatotopical organization of the projection from the nucleus interpositus anterior of the cerebellum to the red nucleus. An experimental study in the cat with silver impregnation methods, E.~p. Braitt Res., 2 (1966) 191 215. 16 Courville, J., Connections of the red nucleus with the cerebellum and certain caudal brain stem structures. A review with functional considerations, Rev. Canad, Biol., 27 (1968) 127-144. 17 Edwards, S. B. and Henkel, C. K., Superior colliculus connections with the extraocular motor nuclei in the cat, J. comp. NeuroL, 197 (1978) 451-468. 18 Edwards, S. B., Rosenquist, A. C. and Palmer, I,. A., An autoradiographic study of ventral lateral geniculate projections in the cat, Brain Research, 72 (1974) 282-287. 19 Faull, R. L. M. and Carman, J. B., The cerebellofugal projections in the brachmm conjunctivum of the rat. 1. The contralateral ascending pathway, J. comp. Neurol., 178 (1978) 495-518. 20 Flindt-Egebak, P., An autoradiographical study of the projections from the feline sensorimotor cortex to the brain stem, J. Hirnforsch., 20 (1979) 375-390. 21 Flumerfelt, B. A., Otabe, S. and Courville, J., Distinct projections to the red nucleus from the dentate and interposed nuclei in the monkey, Brain Research, 50 (1973) 408414. 22 Gacek, R. R., Localization of neurons supplying the extraocular muscles in the kitten using horseradish peroxidase, Exp. Neurol., 44 (1974) 381-403. 23 Graybiel, A. M., Organization of the nigrotectal connection: an experimental tracer study in the cat, Brain Research, 143 (1978) 339-348. 24 Huerta, M. F., Frankfurter, A. J. and Harting, J. K., The trigeminocollicular projection in the cat: patch-like endings within the intermediate gray, Brain Research, 211 (1981) 1-13. 25 Itoh, K., Efferent projections of the pretectum in the cat, Exp. Brain Res., 30 (1977) 89-105. 26 Jayaraman, A., Batton, R. R. III and Carpenter, M. B., Nigrotectal projections in the monkey: an autoradiographic study, Brain Research, 135 (1977) 147-152. 27 Kanaseki, T. and Sprague, J. M., Anatomical organization of pretectal nuclei and tectal laminae in the cat, J. comp. Neurol., 158 (1974) 319-338. 28 Kawamura, S., Fukushima, N., Hattori, S. and Tashiro, T., A ventral lateral geniculate nucleus projection to the dorsal thalamus and the midbrain in the cat, Exp. Brain Res., 31 (1978) 95-106. 29 Kawamura, S., Sprague, J. M. and Niimi, K., Corticofugal projections from the visual cortices to the thalamus, pretectum and superior colliculus in the cat, J. comp. Neurol., 158 (1974) 339-362. 30 Laties, A. M. and Sprague, J. M., The projection of optic fibers to the visual centers in the cat, J comp. Neurol., 127 (1966) 35-70. 31 Loewy, A. D., Saper, C. B. and Yamodis, N. D., Re-evaluation of the efferent projections of the Edinger Westphal nucleus in the cat, Brain Research, 141 (1978) 153-159. 32 Martin, G. F., King, J. S. and Dora, R., The projections of the deep cerebellar nuclei of the opossum, Didelphis marsapialis virginiana, J. Hirnforsch., 15 (1974) 545-573. 33 Mehler, W. R., Vernier, V. G. and Nauta, W. J. H., Efferent projections from dentate and interpositus nuclei in primates, Anat. Rec., 130 (1958) 430-431. 34 Miller, R. A. and Strominger, N. L., An experimental study of the efferent connections of the superior cerebellar peduncle in the rhesus monkey, Brain Research, 133 (1977) 237-250. 35 Mohler, C. W. and Wurtz, R. H., Organization of monkey superior colliculus : intermediate layer cells discharging before eye movements, J. Neurophysiol., 39 (1976) 722-744. 36 Naito, H., Tanimura, K., Taga, N. and Hosoya, Y., Microelectrode study of the subnuclei of the oculomotor nucleus in the cat, Brain Research, 81 (1974) 215-231. 37 Nakamura, Y., Mizuno, N. and Konishi, A., A quantitative electron microscope study of cerebellar axon terminals on the magnocellular red nucleus neurons in the cat, Brain Research, 147 (1978) 17-27. 38 Nlimi, K., Fujiwara, N., Takimoto, T. and Matsugi, S., The course and termination of the ascending fibers of the brachium conjunctivum in the cat as studied by the Nauta method, Tokushima J. exp. Med., 8 (1962) 269-284. 39 Oka, H. and Jinnai, K., Electrophysiological study of parvocellular red nucleus neurons, Brain Research, 149 (1978) 239 246. 40 Schiller, P. H. and Koerner, F., Discharge characteristics of single units in superior colliculus of the alert rhesus monkey, J. Neurophysiol., 34 (1971) 920-936. 41 Schiller, P. H. and Stryker, M., Single-unit recording and stimulation in superior colliculus of tbe alert rhesus monkey, J. Neurophysiol., 35 (1972) 915-924.
370 42 Sparks, D. L., Functional properties of neurons in the monkey superior colliculus: coupling of neuronal activity and saccade onset, Brain Research, 156 (1978) 1-16. 43 Stanton, G. B., Topographical organization of ascending cerebellar projections from the dentate and interposed nuclei in Macaca mulatta: an anterograde degeneration study, J. eomp. Neurol.. 190 (1980) 699-731. 44 Stanton, G. B., Afferents to oculomotor nuclei from area 'y' in Macaca mulatta: an anterograde degeneration study, J. comp. Neurol., 192 (1980) 377-385. 45 Sugimoto, T., Itoh, K. and Mizuno, N., Localization of neurons giving rise to the oculomotor parasympathetic outflow: an H R P study in cat, Neurosci. Lett., 7 (1978) 301-305. 46 Sugimoto, T., Mizuno, N. and Itoh, K., An autoradiographic study on the terminal distribution of cerebellothalamic fibers in the cat, Brain Research, 215 (1981) 29-47. 47 Swanson, L. W., Cowan, W. M. and Jones, E. G., An autoradiographic study of the efferent connections of the ventral lateral geniculate nucleus in the albino rat and the cat, J. eomp. Neurol.. 156 (1974) 143-164. 48 Tarlov, E. and Tarlov, S. R., The representation of extraocular muscles in the ocutomotor nuclei : experimental studies in the cat, Brain Research, 34 (1971) 37-52. 49 Tashiro, T., Kudo, M. and Kawamura, S.. Discontinuous spatial distribution of the tectal afferents from the trigeminal nucleus in the cat, Neurosci. Lett., 20 (1980) 249-252. 50 Thomas, D. M., Kaufman, R. P., Sprague, J. M. and Chambers, W. W., Experimental studies of the vermal cerebellar projections in the brain stem of the cat (fastigiobulbar tract), J. Anat. rLond, j. 90 (1956) 371--385. 51 Updyke, B. V., Topographic organization of the projections from cortical areas 17, 18 and 19 onto the thalamus, pretectum and superior colliculus in the cat, J. eomp. Neurol.. 173 (1977) 81-122. 52 Voogd, J., The Cerebellum o f the Cat. Structure and Fibre Connexions, Van Gorcum. Assen. 1964. 215 pp. 53 Walsh, T. M. and Ebner, F. F.. Distribution of cerebellar and somatic lemniscal projections in the ventral nuclear complex of the virginia opossum, J. comp. Neurol., 147 (1973) 427-446. 54 Wurtz, R. H. and Goldberg, M. E., Activity of superior colliculus in behaving monkey, lII. Cells discharging before eye movements. J. Neurophysiol.. 35 (1972) 575-586.
353
D I S T R I B U T I O N OF C E R E B E L L A R F I B E R T E R M I N A L S IN T H E MIDBRA1N V I S U O M O T O R AREAS: A N A U T O R A D I O G R A P H I C S T U D Y IN T H E CAT
TETSUO SUGIMOTO, NOBORU MIZUNO and KUNIKO UCH1DA Department of Anatomy (lst Division), Faculty of Medicine, Kyoto University, Kyoto 606 (Japan)
(Accepted October 22nd, 1981) Key words: cerebellar nuclei - - superior colliculus - - pretectum - - oculomotor nucleus - - trochlear
nucleus - - Edinger-Westphal nucleus - - autoradiography - - cat
SUMMARY Cerebellar fibers to the midbrain visuomotor areas were traced in the cat autoradiographically after injections of tritiated amino acids into individual cerebellar nuclei. Fibers from the dentate (DN), anterior interpositus (AIN) and posterior interpositus (PIN) nuclei were distributed contralaterally, while those from the fastigial nucleus (FN) bilaterally. The F N fibers appeared to arise mainly from the caudal half of the FN. In the superior colliculus (SC), the F N or D N fibers were more numerous than the PIN fibers, and the areas of termination of the F N fibers were located more medially than those of the DN and P I N fibers. These cerebellotectal fiber terminals were in the intermediate and deep SC layers; clustering of terminal silver grains was noted in the FN and D N fibers-recipient areas in the intermediate gray layer. In the pretectum, the D N fibers terminated ventrally in the reticular part of the anterior pretectal nucleus and the posterior pretectal nucleus. The AIN fibers terminated ventrally in the compact part of the anterior pretectal nucleus and the posterior pretectal nucleus. The nucleus of the posterior commissure received cerebellar fibers chiefly from the DN, and additionally from the FN. The nucleus of Darkschewitsch and the interstitial nucleus of Cajal received fibers from all cerebellar nuclei. No cerebellar fibers terminated in the extraocular motor nuclei and the Edinger-Westphal and anteromedian nuclei.
INTRODUCTION Cerebellar projections to the superior colliculus, pretectum and other mesencephalic regions have been the subject of studies by anterograde degeneration methods in several mammals and by the autoradiographic tracing technique in the monkey and 0006-8993/82/0000-0000/$02.75 © Elsevier Biomedical Press
354 rat (for reviews, see refs. 5.9. 13.34, 4 3 . 4 4 and 52). Although the general patterns ot termination of cerebellar fibers in the midbrain appear to be fairly well-known, the data about details o f the t o p o g r a p h y o f fiber terminals from each of the.. cerebeltar nuclei are still lacking. In a previous study 46, the precise t o p o g r a p h y of termination of the cerebellothalamic fibers was studied in the cat by the autoradiographic tracing method. In the present study, in turn. an attempt was made to obtain more precise data about distribution o f fiber terminals from each of the cerebellar nuclei to the midbrain regions, especially to the visuomotor areas, such as the superior colliculus. pretectum and o c u l o m o t o r and trochlear nuclei. MATERIALS AND METHODS In 14 adult cats (body weight: 2100-4700 g) anesthetized with intraperitoneal sodium pentobarbital (35 mg/kg), a single unilateral injection o f 0.07-0.4 #l (50-100 /~Ci//A) of a mixture o f u-[3H]leucine and u-[3H]proline (New England Nuclear) was made stereotaxically into the fastigial (FN), dentate (DN), anterior interpositus (AI N~ or posterior interpositus (PIN) nucleus: in an additional 2 cats, injections were made bilaterally into the dentate and interpositus nuclear regions (Table 1). All injections were made gradually over 10-20 rain via a 25-gauge injection needle attached to a stereotaxically m o u n t e d I-/A H a m i l t o n syringe, and the syringe was left in place for an TABLE I Materials used in the present study Cat no.
3* 9 12 t3 R L 21 84* 86* 88* 89* 90* 92* 93* 94* R L 97* 99*
Site of injection
Amount of injected isotope (f~Ci)
Survival periods' (days)
FN DN AIN, PIN AIN DN, AIN, PIN DN, PIN DN PIN, DN DN FN PIN FN DN, PIN, A1N AIN DN, PIN, AIN DN, A1N DN AIN, PIN
30 12 12 24 32 24 8 30 18 30 28 40 40 30 40 40 7 25
13 10 6 12 12 12 9 10 8 23 8 7 20 10 20 20 10 7
In Cats 13 and 94, isotope injections were made bilaterally into the right (R) and left (L) dentate and interpositus nuclear regions (cf. Fig. i). The cats marked With asterisks were also. Used in:ihe previous study4~.
355 A
,,.
1
B
I 3
AIN
13L
86 liil
~
9
94L ~
C
12
,3
g
88
ii
....
94L
.......
!:; 92
"
12 9
I
94L
~.:.
AIN
94R ~:i~i~.
9
92 ....
Fig. 1. The sites of the isotope injection in the cerebellar nuclei (shaded areas) in the cats used ill the present study. In each of the columns of A, B and C, selected sections through the cerebellar nuclei of one animal are represented and arranged in the rostrocaudal direction. The bilateral injections in Cats 13 and 94 are represented on one side (cf. Table I). additional 15 min to reduce the contamination of overlying brain tissue. After a survival period of 6-23 days, the cats were deeply anesthetized and perfused through the ascending aorta with 2 liters of l0 /o °/buffered formalin. After sucrose infiltration, the brains were sectioned serially at 35 # m in the frontal plane on a freezing microtome. The sections were mounted onto gelatin-coated slides, defatted in xylene, coated with photosensitive emulsion (Kodak NTB-2, NTB-3, or Sakura NR-M2), and exposed for 4-8 weeks at 4 °C. The sections were then developed in K o d a k D-19, fixed, washed, stained through the emulsion with cresyl violet or neutral red and examined using both light-field and dark-field illumination. The locations of the injection sites and the radioactive labeling were mapped onto enlarged outline drawings of selected sections with the aid of a projection apparatus. In this communication, the terminology of Kanaseki and Sprague 27, Itoh 25, and Avendafio and Juretschke v is used for the pretectal nuclei and tectal laminae. As described previously 4~, only randomly arranged silver grains with density exceeding background
356
\
/
Fig. 2. Distribution of transported label after injecting isotope into the left fastigial nucleus in Cat 88. Terminal silver grains and labeled fibers of passage are represented with dots and broken lines, respectively, in this and the subsequent figures. The projection drawings of frontal sections are arranged from rostral ( A / t o caudal (H).
357 were considered as terminal grains, and silver deposits on identifiable fiber systems were regarded as labeling of fibers of passage. RESULTS
ln/ections into the fastigial nucleus (FN) In 2 cats (Cats I and 88), the isotope injection was centered on the left FN throughout its rostrocaudal extent (Fig. 1A). Most FN fibers crossed the midline toward the opposite side at the rostral levels of the FN, and left the cerebellum through the uncinate fasciculus which was located dorsomedially to the brachium conjunctivum (BC). The FN fibers ascended through the tegmental regions of the midbrain, and were divided into the major ascending and the minor descending components at the caudal levels of the superior colliculus (SC). Some of the latter components appeared to terminate in the tegmental regions around the BC including the pedunculopontine tegmental nucleus (Fig. 2H); the rest were further traced to the lower pontine levels. The ascending FN fibers terminated in the mesencephalic central gray (CG) and the medial two-thirds of the SC. The terminals in the C G were distributed in the dorsal and dorsolateral portions of the CG as well as in the ventral regions dorsal to the oculomotor nucleus (Fig. 2B-H). In the SC, rather sparse terminal grains were seen in the intermediate and deep gray layers (Fig. 2C H); terminal silver grains in the deep gray layer were distributed diffusely, whereas those in the intermediate gray layer were seen in equivocal patchy clusters (Fig. 2E). Some ascending FN fibers were observed to run dorsally around the C G and to cross the midline to terminate in the SC and the dorsal portions of the C G ipsilateral to the isotope injection (Fig. 2D-H). Some of these
Fig. 3. Dark-field photomicrograph showing terminal silver grains in the medial portions of the intermediate SC layer in Cat 88 injected with the isotope contralaterally in the FN. Arrowheads point to collaterals arising from a labeled fiber, s, superficial layer; p, deep layer, :~: 50.
358
Fig. 4. Distribution of transported label after injecting isotope bilaterally into the dentate and interpositus nuclear regions in Cat 13. The projection drawings of frontal sections are arranged from rostral (A) to caudal (H). fibers appeared to send collaterals radiating toward the dorsal surface of the SC (Fig. 3). At the caudal SC levels, these terminal silver grains in the SC were more numerous than those in the SC contralateral to the isotope injection, but they became less numerous in the rostral levels of the SC (Fig. 2C-H). At more rostral levels, labeled F N fibers were seen to ascend toward the
359 diencephalic regions through the dorsomedial tegmental regions between the red nucleus and the SC, contralaterally to the isotope injection. These fibers appeared to send axon collaterals and/or terminals to the dorsomedial midbrain tegmental regions, the nucleus of Darkschewitsch, the interstitial nucleus of Cajal, and the dorsomedial portions of the field of Forel, contralateral to the isotope injection (Fig. 2A-C). On the other hand, some labeled fibers in the SC were seen to run through the SC rostrally toward the pretectal regions; some labeled fibers were also observed to run through the posterior commissure from the pretectal regions contralateral to the isotope injection toward the opposite side (Fig. 2B). In the pretectum, the FN fibers were observed to terminate bilaterally in the nucleus of the posterior commissure, and possibly in the reticular part of the anterior pretectal nucleus (Fig. 2B). When the site of the isotope injection was localized in the rostral half of the FN (Cat 90) (Fig. IA), a few possible terminal silver grains were seen in the CG, but no terminals were found in the SC and pretectum. The FN fibers ascending to the mesencephalic regions appeared to arise mostly from the caudal half of the FN. In all cats used in the present study, no FN fibers were found to terminate in the trochlear nucleus, oculomotor nucleus, Edinger-Westphal nucleus, anteromedian nucleus and red nucleus.
Injections into the dentate and interpositus nuclear regions In Cat 13, the isotope injections were made bilaterally into the dentate and interpositus nuclear regions. On the left side, caudolateral portions in the dentate (DN) and posterior interpositus (PIN) nuclei were involved in the site of injection (13L in Fig. 1A). On the right side, the isotope injection was centered more rostromedially and covered the caudal portions of the DN and anterior interpositus nucleus (AIN), and the lateral portions of the PIN (13R in Fig. IA). The pattern of distribution of silver grains indicating the ascending cerebellar fibers from the DN and interpositus nuclear regions in Cat 13 is shown in Fig. 4. In the mesencephalic central gray (CG), terminal silver grains were distributed mainly in the lateral CG regions and the ventral CG regions dorsal or dorsolateral to the oculomotor nucleus (Fig. 4D-H). In the superior colliculus (SC), terminal silver grains were distributed mainly in the lateral two-thirds of the intermediate gray layer and the lateral one-third of the deep gray layer, at the levels ofth~ rostral one-fourth of the SC (Fig. 4E H). The terminal silver grains in the SC were distributed rather sparsely in the deep gray layer, whereas they shgwed a clear tendency of clustering in the deeper portions of the intermediate gray layer. Labeled fibers of passage were often seen in the ventrolateral two-thirds of the SC, and rarely in the media[ portions of the SC, commissure of the SC, and posterior commissure. In the pretectum, terminal silver grains were distributed in the cgmpact and reticular parts of the anterior pretectal nucleus, posterior wctectal nucleus, and nucleus of the posterior commissure on the left side, and in the reticular part of the anterior pretectal nucleus, posterior pretectal nucleus, and nucleus of the posterior commissure on the right side (Fig. 4C-G). On both sides, distribution of terminal silver grains in the anterior and posterior pretectal nuclei was almost confined to the
360 ventral two-thirds of these nuclei. The terminal silver grains in the nucleus of the posterior commissure were seen in the rostrodorsal portions of the nucleus. Terminal silver grains were also seen in the red nucleus: these grains were intermingled with m a n y labeled fibers of passage. On the left side, the terminal silver grains were concentrated on the dorsal and dorsomediat portions of the parvocellular and magnocellular red nuclear regions. On the right side, the terminal labeling was almost confined to the dorsal or dorsolateral portions of the parvocellular red nucleus. Many labeled fibers running through the red nucleus appeared to course toward the SC and/or the pretectum : some of these fibers ended in the mesencephalic tegmental regions ventral to the ventral border of the SC. Additionally, terminal silver grams were seen in the whole areas of the nucleus of Darkschewitsch. In the interstitial nucleus of Cajal. terminal labeling occurred mostly in the dorsal and dorsomedial portions of the nucleus. No labeling was observed in the trochlear nucleus, oculomotor nucleus, Edinger-Westphal nucleus and the anteromedian nucleus. In Cat 94, a large amount of the isotope was injected bilaterally: on the left side. the site of injection covered the dorsal half of the D N and the lateral portions of the AIN, and on the right side. it covered the entire DN, lateral half of the AIN, lateral one-third of the PIN, and the group y of the vestibular nuclear complex, in Cat 92. a large amount of the isotope was injected unilaterally; the site of injection covered the entire DN. caudal half of the A1N. lateral one-third of the PIN, and the group y of the vestibular nuclear complex (Fig. IB, C). In both of these cats, terminal silver grains were observed densely in the reticular and compact parts of the anterior pretectal nucleus as well as in the posterior pretectal nucleus. The pattern of distribution of terminal silver grains in the midbrain regions, however, was almost the same as seen in Cat 13 (Fig. 4); the only difference was the occurrence of terminal silver grains in the trochlear and oculomotor nuclei on the left side in Cat 94 and in those nuclei contralateral to the isotope injection in Cat 92 (Fig. 5). These terminal fibers in the
a
c
e
@
oo
EW
0 Fig. 5. Distribution of terminal silver grains in the oculomotor (a-e) and trochlear (f) nuclei in Cat 92, The drawings are arranged from rostral (a) to caudal if).
361
EW ~ -
/
B
C
NIC ('
\ ///
a
D
b
Fig. 6. Distribution of labeled fibers (A-D) in Cat 3 injected with the isotope contralaterally in the DN (a, b), as indicated in Fig. ]. extraocular motor nuclei appeared to arise contralaterally from the group y of the vestibular nuclear complex. The terminal silver grains in the oculomotor nucleus in Cats 94 and 92 were distributed in the whole mediolateral extent of the nucleus at the caudal levels, and in the medial half of the nucleus at the middle levels; no labeling was found, however, in the rostral one-third levels of the nucleus. In the cats injected bilaterally with a rather large amount of the isotope, the general pattern of fiber projections from the cerebellar nuclei was observed easily, but the differences among the patterns of fiber projections from the DN, AIN or PIN were not marked. Therefore, the patterns of fiber projections from each of the DN, AIN and PIN will be described in the cats injected with the isotope unilaterally into each of the DN, AIN and PIN.
Injections into the dentate nucleus (DN) In 4 cats (Cats 3, 21, 86 and 97), the site of isotope injection was confined within
362 the DN (Fig. IA. CI. In these cats. terminal labeling in the midbrain regions was seen contralaterally in the central gray (CG) ~mperior collicutus (SCI. pretectum, red nucleus, tegmental regions, nucleus of Darkschewitsch, interstitial nucleus of Cajal. and field of Forel (Fig. 6). In the SC. terminal silver grains were distributed in the lateral two-thirds of the intermediate and deep gray layers ; they were almost confined to the rostral one-fourth levels of the SC (Fig. 6C. D). In the intermediate gray layer, a patchy pattern of terminations was seen in the deepest tier along the mediolateral axis of the intermediate gray (Fig. 7). No labeling was found in the commissure of the SC. In the pretectum, terminal silver grains were found in the rostrodorsal portions of the nucleus of the posterior commissure as well as in the small ventral regions m the posterior pretectal nucleus and reticular part of the anterior pretectal nucleus: no labeling was seen in the compact part of the anterior pretectal nucleus ~Fig. 6A. B), Terminal labeling in the red nucleus was almost confined to the parvocellular regions (Fig. 6B). Terminal labeling was seen m the nucleus of Darkschewitsch and the interstitial nucleus of Cajal (Fig. 6A. B), but no silver grains were observed in the trochlear nucleus, oculomotor nucleus. Edinger Westphal nucleus and anteromedian nucleus. Injections into the anterior interpositus nucleus / AI N ) In 2 cats (Cats 12 and 93), the site of the isotope injection was confined within the AIN (Fig. 8a). In another 2 cats (Cats 9 and 99~. the isotope injection was centered on the AIN. but the site of the injection extended into small parts of the posterior interpositus nucleus (Fig. lB. C~. In the former 2 cats (Cats 12 and 93), terminal silver
Fig. 7. Dark-field photomicrograph showing terminal silver grains in the lateral portions of the intermediate SC layer in Cat 21 injected with the isotope contralateraliy in the DN. Axrows indicate clusters of terminal sih er grams m the deepest tier of the intermediate gray layer, s, superficial layer; p, deep layer. 50.
363
(FN',
:"
-. •
b
Fig. 8. Low-power photomicrographs showing the sites of rejections in the A|N (a) of Cat 93 and the PIN (b) of Cat 89. De, nucleus of Deiters. : 20. grains were seen in the pretectum, midbrain tegmentum, red nucleus and nucleus of Darkschewitsch (Fig. 9). In addition to these regions, terminal labeling was also noted in the mesencephalic central gray and interstitial nucleus of Cajal in the latter 2 cats (Cats 9 and 99). The density of silver grains in the SC was above background levels only in Cat 99; these grains were seen sparsely in the intermediate gray layer at the rostralmost levels of the SC. In the pretectum, terminal silver grains were seen mainly in the ventral half regions in the posterior pretectal nucleus and the cgmpact part of the anterior pretectal nucleus, but no terminal labeling was noted in the reticular part of the anterior pretectal nucleus (Fig. 9A, B). The nucleus of the posterior commissure was labeled only in Cats 9 and 99. Terminal labeling in the red nucleus was seen massively in the ventral and ventrolateral parts of the magnocellular regions (Fig. 9A, B), and that in
364
,6,
\
B
C a
Fig. 9. Distribution of labeled fibers (A-C) in Cat 93 injected with the isotope contralaterally in the AIN (a, b), as indicated in Fig. 1.
A
•
/j
C
Fig. 10. Distribution of labeled fibers (A-C) in Cat 89 injected with the isotope contralateratly in the PIN (a, b), as indicated in Fig. 1.
365 the nucleus of Darkschewitsch was observed most markedly in the rostral regions of the nucleus (Fig. 9A). No terminal labeling was noted in the trochlear, oculomotor, Edinger-Westphal and anteromedian nuclei.
Injections into the posterior interpositus nucleus (PIN) In 2 cats (Cats 84 and 89), isotope injection was centered on the PIN (Fig. 8b); in one of these cats (Cat 84), the isotope deposits also involved small parts of the DN (Fig. 1A). Terminal labeling was seen in the mesencephalic central gray, tegmental regions, SC, red nucleus, nucleus of Darkschewitsch, nucleus of the posterior commissure and interstitial nucleus of Cajal (Fig. 10). Terminal silver grains in the SC were distributed mainly in the ventrolateral portions of the intermediate and deep gray layers at the rostral one-fourth levels of the SC (Fig. 10B). In the pretectum, terminal labeling was found sparsely in the nucleus of the posterior commissure (Fig. 10A). Many terminal silver grains were seen in the medial and dorsomedial parts of the magnocellular parts of the red nucleus (Fig. 10B, C), but no terminal labeling was found in the trochlear, oculomotor, Edinger-Westphal and anteromedian nuclei. DISCUSSION
Cerebellar fibers to the superior colliculus ( SC) Although the existence of cerebellotectal fibers to the SC appears to be established in the cat 3,5,6A4,as,5°,52, rat 1~,19, monkey T M and opossum 32,53 by the anterograde degeneration and the autoradiographiO, 13 methods, some discrepancies and uncertainties are still pending concerning the origins and terminations of these fibers. The crossed and uncrossed cerebellotectal fibers from the fastigial nucleus (FN) were reported in the monkey 9 and cat 3,6, and the crossed tectal fibers from the dentate nucleus (DN) were shown to exist in the opossum 32 and raO 3. On the other hand, Angaut 5 and Chan-Palay 13 could not obtain conclusive evidences for the existence of the dentatotectal fibers in the cat and monkey, respectively. The present data, however, showed that the cerebellotectal fibers to the SC in the the cat arose mainly from the DN and FN, and additionally from the posterior interpositus nucleus (PIN). Although Angaut4, 5 reported that the cerebellotectal fibers from the interpositus nuclei arose from the anterior interpositus nucleus (AIN) rather than the PIN, the present study provided no confirmative evidence indicating the existence of the cerebellotectal fibers from the AIN. In the previous studies performed by the degeneration methods, the cerebellotectal fibers were reported to end in the deep layers of the SC in the rat I0, cat~,5, 6 and monkey 9. According to the other degeneration study in the opossum 32 and the autoradiographic study in the rat 13, however, the cerebellotectal fibers from the DN ended in the intermediate gray layer of the SC. The present data showed that the cerebellotecta[ fibers were distributed mainly to the intermediate gray layer, and sparsely to the deep gray layer of the SC. In the monkey, some neurons in the intermediate gray layer of the SC were found to discharge before saccadic eye movements ~5,4°-4'~,~4. The neurons sending their axons around the extraocular motor
366 nuclei were also found in the intermediate gray layer of the SC in the catlL Therefore the cerebellar fibers to the intermediate gray layer of the SC might be considered to exert some regulatory influences upon such so-called eye movement cells The FN- and DN-tectal fiber terminals showed the tendency of clustering in the intermediate gray layer of the SC, especially in the deepest tier of the intermediate gray layer. Similar findings were reported in the recent autoradiographic studies concerning the trigeminotectal'~4, 49 and nigrotecta123, 26 fibers, which also ended in the intermediate gray layer of the SC. The functional meanings of these data sugg~ting the discontinuity of afferent fiber terminations in the intermediate gray layer of the SC still remain to be elucidated. Cerebellar fibers to the pretectum Cerebellopretectal fibers have been described, but rather anecdotally, in the opossum 32, rat 13,19, monkey 9.12,33,34,43 and cat 14,50. Although most of the previous investigators agreed that the cerebellopreteetal fibers ended in the nucleus of the posterior commissure, the termination of the cerebellopretectal fibers in the anterior pretectal nucleus was also reported in the rat ~9 and opossum ~2. In these previous studies, the cerebellopretectal fibers to the nucleus of the posterior c~mmissure were reported to arise from the DN and interpositus nuclei14, 33,43, from the DN12,13. or from the FN 9,5°. On the other hand, the present data showed that the nucleus of the posterior commissure received fibers from the DN and FN. and possibly from the AIN and PIN, and that the anterior and posterior pretectal nuclei received fibers from the DN and A1N; in the anterior pretectal nucleus, the D N and AIN fibers ended in the reticular and compact parts, respectively. The termination of the DN fibers in the ventrolateral part of the anterior pretectal nucleus was also reported in the opossum~L In the ventral regions of the anterior and posterior pretectal nuclei, where the cerebellar fibers were seen to terminate in the present study, no retinal fibers seem to end in the catll,z7, 3°. On the other hand, the area of distribution of fibers from the ventral lateral geniculate nucleus 18,2s,4v and the sensorimotor and visual cortical areasl0,Z0,'~9,,~1 appears to include the ventral regions of the anterior and posterior pretectal nuclei. In these pretectal regions, convergence of direct inputs from the cerebellar nuclei, cerebral cortical areas and the ventral lateral geniculate nucleus might occur. Cerebellar.fibers to the oculornotor and trochlear nuclei In a cat (Cat 92) injected with the isotope around the DN, terminal labeling occurred contralaterally in the oculomotor and trochlear nuclei. In other cats which were injected with the isotope similarly around the D N (Cats 3, 13, 21, 86 and 97), however, no terminal silver grains were found in these cranial nerve nuclei, In the neuronal structures involved in the injection site in Cat 92, the group y of the vestibular nuclear complex was found to be the only nucleus that was not involved in the injection sites of the other cats. Similar terminal labeling in the oculomotor and trochlear nuclei was also seen in another cat (Cat 94) which was injected with the isotope bilaterally around the DN. In this cat the group y of the vestibular nuclear
367 complex was involved in the injection site on the right side, and the terminal labeling in the oculomotor and trochlear nuclei was observed only on the left side. The fiber terminals seen in the oculomotor and trochlear nuclei in Cats 92 and 94 were thus assumed to derive contralaterally from the group y of the vestibular nuclear complex. In accordance with the present results, afferent fibers from the group y to the oculomotor and trochlear nuclei have been reported in the monkey 44. In the rat, the fibers arising from the group y were traced contralaterally only to the dorsomedial part of the oculomotor nucleus 19. The medial regions of the oculomotor nucleus, where the terminals of fibers arising from the group y were observed in the present study, appeared to contain the motoneurons supplying the superior rectus eye muscle1,92, a6,4s. Thus, the group y of the vestibular nuclear complex appears to give rise to afferent fibers to the motoneurons innervating the superior rectus and superior oblique eye muscles, and to be possibly involved in the control mechanisms of vertical eye movements.
Cerebellar fibers to other midbrain regions In the present study, the nucleus of Darkschewitsch, interstitial nucleus of Cajal and the mesencephalic central gray regions were found to receive cerebellar fibers from all cerebellar nuclei; bilaterally from the FN and contralaterally from the DN, AIN and PIN. Of these cerebellar fibers, the DN fibers terminating chiefly in the rostral portions of the nucleus of Darkschewitsch were most numerous. in agreement with the previous studies in the cat z,4,5,15,16,37,a9,52 and monkey TM 43, the parvocellular and magnocellular red nuclei were observed to receive cerebellar fibers contralaterally from the DN and the interpositus nuclei, respectively. No FN fibers, however, were found to end in the red nucleus, as reported in the cat 6,5°,~2 and opossum 3'~. The Edinger Westphal and/or anteromedian nuclei were reported to receive cerebellar fibers in the eat14, ~0 and rat 13. No such terminals, however, were observed in the present study, supporting the other reports in the cat 4 ~,38 and monkey 13,34. The ventral regions of the mesencephalic central gray close to the Edinger-Westphal and anteromedian nuclei, however, were found to receive the cerebellar fibers bilaterally from the FN and contralaterally from the DN and/or the interpositus nuclei. These regions of the central gray have been known to contain preganglionic neurons sending their axons ipsilaterally to the ciliary ganglion31, 4~. The cerebellar nuclei, thus, might exert direct regulatory influences on the reflex system of the intrinsic eye muscles through the projections to the mesencephalic central gray 8. ACKNOWLEDGEMENTS The photographic work of Mr. Akira Uesugi and the support of the Niwa Medical Research Foundation are gratefully acknowledged.
368 LIST OF ABBREVIATIONS AIN AM BC CG CP CM CSC De DN EW FF FN Hb HI i lp LGd LGv MG ML ND N1C NOT
anterior interpositus nucleus anteromedian nucleus brachium conjunctivum central gray cerebral peduncle centre median nucleus commissure of the superior colliculus nucleus of Deiters dentate nucleus Edinger-Westphal nucleus field of Forel fastigial nucleus habenular nucleus habenulo-interpeduncular tract intermediate gray layer of the superior colliculus interpeduncular nucleus dorsallateral geniculate nucleus ventral lateral geniculate nucleus medial geniculate nucleus medial lemniscus nucleus of Darkschewitsch interstitial nucleus of Cajal nucleus of optic tract
NPC NRT OT p Pac Par PC Pf PIN Pm PN Pp RN s SC SN V 3 4
nucleus of the posterior commissure nucleus reticularis tegmenti pontis optic tract deep gray layer of the superior colliculus compact part of the anterior pretectal nucleus reticular part of the anterior pretectal nucleus posterior commissure parafascicular nucleus posterior interpositus nucleus medial pretectal nucleus pontme nuclei posterior pretectal nucleus red nucleus superficial gray layer of the superior colliculus superior colliculus substantia nigra third ventricle oculomotor nucleus trochlear nucleus
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