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Brain Research, 106 (1976) 152-158 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Net~herlands

Laterality and topography of cerebellar cortical efferents in the opossum

(Didelphis marsupialis virginiana) D. E. H A I N E S , J. L. C U L B E R S O N

AND G. F. M A R T I N

Department of Anatomy, West Virginia University School of Medicine, Morgantown, W. Va. 26506 and (G.F.M.), Department of Anatomy, Ohio State University School of Medicine, Columbus, Ohio 43210 (U.S.A.)

(Accepted January 5th, 1976)

In one of the first detailed studies, Clarke and Horsley 4 concluded that cerebellar corticonuclear and corticovestibular fibers were ipsilateral. Although most subsequent investigators have substantiated the ipsilateral nature of such fibers 1,3, 5-9,xs-19,z2-2~ a few have reported bilateral projections from the vermis 2,14,~1 or from vermis plus more lateral cortex 10. In a study on the opossum 2° extensive bilateral corticonuclear and corticovestibular fibers have been reported from vermal, paravermal and hemisphere cortices. Recent evidenceS-7,15-17. 22 also suggests that each cerebellar lobule projects to a particular area of the ipsilateral cerebellar nuclei revealing a specificity of topographic relationships not suspected in earlier studies. In the opossum 2°, however, it has been suggested that specific cortical lobules project essentially throughout their respective nuclei. Since many investigators agree that the opossum is a generalized mammal, verification of this extensive and diffuse pattern of cerebellar cortical efferents would significantly alter certain concepts of cerebellar function. F o r this reason, and in light of the consensus, it was deemed appropriate to reconsider these projections in the opossum. Two general questions are addressed: (1) are cerebellar corticonuclear and corticovestibular fibers of the opossum bilateral and, if so, to what degree, and (2) is there evidence suggestive of a specific topographic organization of these fiber systems? Eight North American opossums (Didelphis marsupialis virginiana) were used for this study. Lesions were placed in the posterior lobe vermis and/or paravermis by applying the heated tip of a metal teasing needle to the exposed unopened dura. The brain stems were sectioned at 40/~m and impregnated by the F i n k - H e i m e r 13 method. Alternate sections were either stained with the F i n k - H e i m e r method, decolored in 1 ~ potassium ferricyanide and then counterstained with cresyl violet acetate or stained with only cresyl violet acetate. Lesions confined to one side of an arbitrary midline produce only ipsilateral degeneration in either the cerebellar nuclei or vestibular complex. The results from a case with an ipsilateral lesion of lobules VIII and dorsal IX (Figs. 1D and 2A) serve to illustrate this point. Degenerated fibers are traced from the lesion to the caudo-

153

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den

,1.0 mm,

VIII

IX

J

Fig. 1. Tracings in cross-section from rostral (A) to caudal (C) of the cerebellar and vestibular nuclei of an opossum with an ipsilateral lesion (D) of lobules VIII and dorsal IX. Large dots represent fibers of passage and small dots indicate areas containing preterminal degeneration. Note the location of degeneration in the NM. Abbreviations for this and other figures: dcn, dorsal cochlear nucleus; jrb, juxtarestiform body; lvn, lateral vestibular nucleus; m, approximate vermal midline; mvn, medial vestibular nucleus; nia, anterior interposed nucleus; nip, posterior interposed nucleus; nl, lateral cerebeIlar nucleus; nm, medial cerebellar nucleus; p-v, approximate paravermal-vcrmis junction; rb, restiform body; spvn, spinal vestibular nucleus; vcn, ventral cochlear nucleus; VIII, vermis lobule VIII, pyramidal lobule; IX, vermis lobule IX, uvula.

lateral pole o f the medial cerebellar nucleus ( N M ) . A t t h a t level, sparse n u m b e r s o f d e g e n e r a t e d fibers are f o u n d in m e d i a l N M while in m o r e lateral areas they are n u m e r o u s (Fig. 1B a n d C). R o s t r a l l y a x o n a l debris is clearly restricted to the lateral h a l f o f the N M and, at the level o f its rostral third, it is p r e s e n t in d o r s o l a t e r a l (dense) a n d d o r s a l ( m o d e r a t e ) p o r t i o n s o f the nucleus (Figs. 1A a n d 2B, C, E). W i t h the exception o f its c a u d a l pole, m e d i a l areas o f the N M are d e v o i d o f a x o n a l debris (Figs. 1 a n d 2F) a n d at m o r e rostral levels v e n t r o l a t e r a l p o r t i o n s o f the nucleus c o n t a i n a l m o s t no

Fig. 2. Photomicrograph (A), lo\\ poucr (B) and high power (C‘, E G) photomicropraphs ofdcg:en~l ,Ition in the NM from a lesion of lobule VIII and dorsal IX. Note the degeneration in dorsol;ltcr;~l (C, detail from B) and dorsal (IL. detail from H) areas of the ipsilateral NM. Medial areas of the ip\ilateral NM (F. detail from BJ are free of debris. Dorsolateral regions of the contralateral NM CO,,tain no degeneration CC;, cornpaw with C‘). Numerous degenerated fibers are present in caudal “\JM (D) from lobule VII while the wmc itrca of the contralateral NM (H) is free of degeneration. ~c,,le,

Fig. 3. Tracings in cross-section from rostra[ (A) to caudal (C) of the cerebellar and vestibular nuclei of an opossum with a lesion of the vermal-paravermal junction (p-v). Debris is obvious in the ipsilateral LVN (E, detail from the area indicated in A) while the contralateral LVN (E, compare with D) contains no degeneration. Note the distinct interface in the NIA between medial areas containing degeneration and lateral areas free of debris (B and F, detail from area indicated in B). Scale, 33/~m for D - F . Fink-Heimer method.

156 degeneration. A sparse amount of degeneration is present in the most medial part of the anterior interposed nucleus (NIA) and in medial and ventral areas o[' lhe posterior interposed nucleus (Fig. 1B and C). Numerous degenerated fibers enter the ipsilateral juxtarestiform body and distribute to the dorsal half of the lateral vestibular nucleus (LVN) (Fig. l A), and to the dorsal and dorsolateral areas of the rostral half of the spinal vestibular nucleus (SpVN) (Fig. I B). Examination of the contralateral NM, NIA, NIP, LVN and SpVN, especially those regions containing the greatest concentration of debris on the ipsilateral side, revealed no degenerated fibers (Fig. 2G). In cases with lesions restricted to a single lobule (e.g. lobule VII) degeneration is found only in caudal and lateral areas of the ipsilateral NM (Fig. 2D), while the same area of the contralateral NM is free of debris (Fig. 2H). Degeneration was never seen in the lateral cerebellar nucleus (NL) from lesions restricted to the vermis. To evaluate the specificity of paravermal projections to the interposed complex a lesion was placed in lobule VII such that it involved medial portions of the paravermis and the lateral vermis (Fig. 3C). Degeneration is sparse in the medial areas of the NM at caudal levels, dense in its caudal lateral half to one-third and sparse in its dorsolateral portions at rostral levels (Fig. 3A and B). When compared to cases with vermal lesions there is a precipitous increase in degenerated fibers which terminate in the NIA and N1P. The medial third of the caudal half of the NIA contains extensive degeneration and the NIP contains degeneration throughout being most concentrated in its central areas (Fig. 3B). Of particular note is the relatively sharp interface that separates those medial portions of the NIA which contain extensive degeneration from those more lateral areas of the nucleus which are degeneration free (Fig. 3B and F). A similar, though less distinct, border exists between those areas of the NM which contain debris and those areas free of degeneration in the above described cases. Degenerated fibers course through the ipsilateral juxtarestiform body and distribute to the dorsal half of the LVN (Fig. 3A and D) and dorsolateral areas of the rostral SpVN (Fig. 3B). No axonal debris is present in either the ipsilateral N L or the contralateral NM, NIA, NIP, N L and vestibular complex (Fig. 3E). A small area ventral to the rostral NM contained debris in almost every case (Figs. I A and 3A). Although detailed cytoarchitectural analyses of the cerebellar nuclei are not available it appears that this debris is related to rostromedial portions of the NIP. The results of the present study offer evidence on both questions posed above. First, cerebellar corticonuclear and corticovestibular fibers of the opossum are ipsilateral. This observation is in agreement with other studies on a variety of mammalian formsl,a 9,15-19,22-25 and does not corroborate the recent report that these fiber systems (in opossum) have bilateral origin from vermal, paravermal and hemisphere lobules 2°. Second, there is clear evidence that specific lobules of the opossum cerebellar cortex project to particular regions of the deep cerebellar nuclei. The present study has shown that lesions of the posterior vermis (VI-IX) produce degeneration in the lateral half of the caudal NM and only in its dorsolateral and dorsal areas rostrally. Medial portions of the caudal NM and the majority of the rostral NM are

157 free o f debris a n d p r e s u m a b l y receive i n p u t f r o m the n o d u l u s (X) a n d a n t e r i o r vermis ( I - V ) , regions u n d i s t u r b e d in this series o f experiments. It is n o t possible to verify the recent r e p o r t on the o p o s s u m 2° which suggested t h a t the cortex o f vermis lobules project essentially t h r o u g h o u t the N M . The o p o s s u m consequently shares with o t h e r m a m m a l s 1,3-9,11,12,15-19,22-25 the characteristics o f (1) ipsilateral cerebellar cortical p r o j e c t i o n s a n d (2) a relatively specific t o p o g r a p h i c a l o r g a n i z a t i o n o f these fibers, thus i n d i c a t i n g t h a t it is m o r e similar to these o t h e r forms t h a n as strikingly dissimilar as recently i m p l i e d 2°. Differences between the o p o s s u m (this study), r a b b i t 22, catS, 7 a n d some p r i m a t e s 15-17 represent m i n o r species specific v a r i a t i o n s o f a general pattern. In light o f the well o r g a n i z e d p a t t e r n o f cerebellar cortical efferents, a n d since o p o s s u m is recognized as a generalized m a m m a l , a d e t a i l e d r e e v a l u a t i o n o f its cerebellar cortical efferents is n e e d e d a n d will c o n t r i b u t e to o u r u n d e r s t a n d i n g o f cerebellar function. This w o r k was s u p p o r t e d , in part, by U S P H S G r a n t NS-11327-02 to D . E . H . a n d G R S G r a n t P H S 5-S01-0543Y The a u t h o r s express their a p p r e c i a t i o n to Ms. A n n e C a r r a n d Ms. S a n d y Z i m m e r for technical a n d p h o t o g r a p h i c help a n d Ms. M a r y M a r t h a K e n t for typing.

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