The Olivocerebellar Projection in the Cat as Studied with the Method of Retrograde Axonal Transport of Horseradish Peroxidase. II. THE PROJECTION TO THE UVULA A. BRODAL Anatomical Institute, University of Oslo, Oslo, N o r w a y
ABSTRACT Following injections of small quantities of horseradish peroxidase (HRP) suspension i n the uvula of the cat, the distribution of labeled cells i n the inferior olive has been mapped. The findings confirm the conclusion made on the basis of studies of retrograde cell loss i n the olive following ablations of the uvula (Brodal, '40b) that two small olivary subdivisions, the nucleus J and the dorsomedial cell column project heavily to the uvula. In addition the HRP-study shows that the uvula receives a smaller number of fibers from two circumscribed areas of the contralateral medial accessory olive. These areas appear to project to the lateralmost parts of the uvula (fig. 4). The findings thus support the presence of a longitudinal zonal subdivision in the uvula. Labeled cells are found i n the nucleus J and the dorsomedial cell column also following injections of the fastigial nucleus and to a lesser degree of lobulus VII of the vermis (Hoddevik et al., '76). This may be due to collateral branching of olivary efferents. There is some evidence for a topographical correlation between dorsal and ventral parts of the uvula and rostral and caudal parts, respectively, of the nucleus J and the dorsomedial cell column. This may be related to functional differences between the two parts of the uvula. The method of tracing the retrograde axonal transport of horseradish peroxidase (HRP) to determine the origin of nervous connections (Kristensson et al., '71 ; LaVail and LaVail, '72; and others) has been used in our laboratory for studies of various afferent connections to the cerebellum (P. Brodal, '75; Hoddevik, '75; Rinvik and Walberg, '75). Among the projections from the inferior olive those to the paramedian lobule (Brodal et al., '75) and to the vermal lobules VI-VIII (Hoddevik et al., '76, submitted) have been described. On account of the complex topography of the cerebellum and of the inferior olive it is essential that the many small subdivisions of the cerebellum are studied separately. The present report is restricted to the olivary projection onto the uvula (lobule IX of Larsell). Using the modified Gudden method (Brodal, '40a) of mapping retrograde cellular changes in the olive following cerebellar lesions in neonatal kittens and rabbits, Brodal ('40b) concluded that the uvula reJ.
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417426.
ceives fibers from two characteristic and well delimited subdivisions of the olive, the dorsomedial cell column of Mareschal ('34) and the nucleus J3 (distinguished by Brodal, '40b). Recent electrophysiological studies (see especially Armstrong et al., '74) have shown that the olivary projection is far more complexly organized than appears from the map constructed on the basis of studies of retrograde cell changes in the olive. Thus several lobules receive fibers from more than one olivary subdivision. This was confirmed anatomically with the HRP method as concerns the paramedian lobule. This receives afferents from all four major olivary subdivisions (Brodal et al., '75). The present study was undertaken in order to check the findings from 1940 and to see if the HRP method might reveal projections to the uvula from other olivary areas in addition to those from the dorsomedial cell column and the nucleus 3. Physiological studies are inconclusive 417
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concerning the olivary projection to the divisions are indicated). Different densities uvula (see DISCUSSION). This is a further of dots indicate relative differences in the reason for undertaking a renewed ana- proportion of labeled cells. tomical study. MATERIAL AND METHODS
Six adult cats, weighing about 2 kg, were used as experimental animals. Surgery was performed under Nembutal anesthesia. 0 . 3 4 . 5 pl of HRP (Sigma VI P8375) suspension (50% wt./vol.) was slowly injected through a Hamilton syringe. Following a posterior craniotomy only the rostralmost part of the uvula can be discerned underneath the intact dura. For injections in the rostralmost folia the needle was inserted through a slit in the dura. To gain access to the caudal and ventral, not visible, parts of the uvula the needle was either inserted under visual guidance with the animal's head ventroflexed, or stereotactically. After 1-2 days the animals were killed by intracardic perfusion under Nembutal anaesthesia of a mixture of 0.4% paraformaldehyde and 1.25% glutaraldehyde with phosphate buffer. Following dissection, post-fixation and serial sectioning on the freezing microtome (sagittally of the cerebellum, transversely of the brain stem) at 50p, two sections out of groups of 5 were treated with 3,3'-diaminobenzidine tetrahydrochloride according to Graham and Karnovsky ('66). One of the sections was left unstained, the other was weakly stained with cresyl violet. For particulars concerning the method used, see Walberg et al. ('76). The stained cerebellar areas and the labeled cells in the olive were plotted in drawings of sections made under a projection apparatus. The findings in the cerebellum were transferred to Larsell's ('70) diagram of the cerebellar cortex. Regions where the molecular layer is stained are shown in black. The distribution of labeled olivary neurons as seen in the drawings of the sections was transferred to a standard series of 15 equally spaced transverse sections through the olive (see fig. 1C) taken from Brodal ('40b). To facilitate comparisons the olivary areas containing labeled cells in this diagram were finally transferred to a diagram of the inferior olivary complex imagined unfolded (see fig. ID, where the various olivary sub-
RESULTS
Following injections in the cerebellar cortex or the immediately underlying white matter the spreading of the injected fluid is rather uncontrollable (see Walberg et al., '76, for particulars). In mapping the staining of the cortex particular attention has been paid to the molecular layer, since at least most olivocerebellar fibers end as climbing fibers. The labeled neurons in the olive are easily distinguished, particularly under dark field illumination (fig. 2). A systematic plotting of the distribution of Abbreviations
B,
NucleusJ (Brodal, '40b) of inferior olive
D, Dorsal accessory olive
d. cap., Dorsal c a p d. l., Dorsal lamella of principal Olive dm. c. col., Dorsomedial cell column (Mareschal, '34) Flocc., Flocculus F. pr., Primary fissure l., Lateral Lob. ant., Anterior lobe L. pm., Lobulus paramedianus M, Medial accessory olive m., Medial Nod., Nodulus P. fl. d., Paraflocculus dorsalis P. fl. v., Paraflocculus ventralis v. I., ventral lamella of principal olive v. 1. o., ventrolaterd o-tgrowth Fig. 1 Presentation of the findings i n cat B . St. L. 668 following a n injection of HRP in the dorsal part of the uvula. A. Nearly midsagittal section of the cerebellum, showing the stained cortex in the uvula. B. The total stained area a s projected onto a diagram (from Larsell, '70) of the cerebellar surface. Open circle indicates point of entrance of injection needle. In both diagrams black denotes staining of molecular layer, hatching staining of granular layer or white matter. C. A diagram of 15 equally spaced transverse serial sections through the cat's olive showing its subdivisions (from Brodal, '40b). The different subdivisions of the olivary complex are indicated, Dotted areas contain HRP labeled neurons; variations in density of dotting indicate variations in numbers of labelled cells. Rectangles at levels V I and XI11 indicate position of photomicrographs of figure 2. D. Reconstruction of the inferior olivary complex imagined unfolded in o n e plane (from Brodal, '40b) by pulling its components a p a t in the latero-medial direction (see section XI below). To the right the entire right olivary complex, to the left the left medial accessory olive. No labelled cells a r e present in other parts of the left olive. For abbreviations see list above.
OLIVOCEREBELLAR PROJECTION TO THE UVULA
A
I -V, L o b ant
N
.L.668
M, Uvula
Left
caudal Left
V
Righi
d coo
D
LIEDIAL ACC OLIVE
...
caudal
v
Left
MEDIAL ACC OLIVE
PRINCIPAL OLIVE
DORSAL ACC OLIVE
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Fig. 2 Dark field illumination photomicrographs ( X 6 5 ) from the inferior olive in cat. B. St. L. 668. A. Ample occurrence of labeled cells in the right nucleus 8.Photo corresponds approximately to level V I in figure 1C. B. Most of the cells in the right dorsomedial cell column are labelled. Photo from level XI11 of figure 1C.
labeled olivary neurons following injections of HRP in the uvula shows that they have a restricted spatial distribution. Cat l3.St.L. 668 (survival time 1 day) received an injection of 0,4 pl in the dorsal part of uvula (lobule IX) a little to the left of the midline. There is a strong brown staining of the molecular layer in most of the dorsalmost folia of the lobule (black in figs. 1A and B), mainly on the left side of the midline. In most places the granular layer and the white matter of these folia are stained as well, but the staining cannot be followed to the fastigial nuclei, and no labeled cells are found in these. Due to spreading of the fluid the medialmost parts of some folia of the left paramedian lobule are stained. (In fig. 1 B the folia lying closest to the uvula and marked as stained appear to be separated from the uvula by some distance, due to distortion of the mutual relations in the diagram of the cerebellar cortex.) In the inferior olive numerous conspicuously labeled neurons (fig. 2) occur throughout the entire extent of the nucleus j3 and the dorsomedial cell column on both sides. The number of labeled cells is a little less on the left side than on the right, where in some sections more than three quarters of the neurons are labeled. On the right side (figs. 1C, D) there are in addition two other areas of labeled cells, one in the rostral part of the medial accessory olive, another in the ventral lamella. In both these areas the labeling is less intense, and relatively fewer cells are labeled than in the nucleus 3 and the dorsomedial cell column, except for the ventral lamella at level X, where
most cells are heavily labeled. Finally, a few faintly labeled cells are found in the caudal part of the medial accessory olive. On the left side, a few labeled cells in the corresponding area of the caudal half of the medial accessory olive are the only ones present, except for those in the nucleusJ and the dorsomedial cell column. Very similar findings are made following an injection in the ventral part of the uvula (cat B.St.L. 690, injection 0.3 pl, survival time 2 days, fig. 3A). Except for staining of the ventralmost folia of the uvula, mainly on the right side, there is some spreading of the staining to the middle folia of the right paramedium lobule. There is no staining of the fastigial nuclei. In both inferior olives many cells in the nucleus j3 and the dorsomedial cell column are heavily labeled, fewer on the right side than on the left, where at some levels more than half of all neurons are labeled. The rostralmost parts of the two groups are free. In the left olive, but not in the right, there are in addition some, more lightly, labeled cells in two rather circumscribed areas, one caudally in the ventral lamella, the other in the rostral half of the medial accessory olive. Finally a few faintly labeled cells occur in the caudal half of the medial accessory olive. In cat B.St.L. 698 injection 0.3 p1, survival time 2 days) a stereotactically made injection has resulted in staining of a restricted part of the middle folia of the uvula (fig. 3B). The staining is limited to the median area. There is no spreading to the fastigial nuclei. In the inferior olive there is good labeling of a considerable pro-
42 1
OLIVOCEREBELLAR PROJECTION TO T H E UVULA
A
l3. MEDIAL ACC OLIVE
PRINCIPAL OLIVE
DORSAL
ACC OLIVE
Right
Left
B
MEDIAL ACC OLIVE
B.St.L. 6 98
Left
Right
Fig. 3 A. Diagrammatic presentation of the findings in cat B.St.L. 690. Above to t h e left part of the cerebellar surface showing the staining of the cortex following an injection of HRP in the ventral part of the uvula. Above to the right three representative levels of the transversely c u t olive with indications of the distribution of labeled cells. Below the entire left olivary complex and the right medial accessory olive are shown unfolded to illustrate the distribution of labeled cells. B. Diagram of the findings i n cat B.St.L. 698. To t h e left the staining of the cerebellar cortex i n a small area in the middle of the uvula following a stereotactically made injection (the insertion point of the needle in lobulus VIIIB (circle) and its track a r e indicated). In the middle two representative sections through the olive. To the right the distribution of labeled olivary cells, restricted to parts of both medial accessory olives. Symbols a s in figure 1. For abbreviations see list o n p. 418.
portion of neurons throughout the nucleus j3 and the dorsomedial cell column on both sides. In addition a few faintly labeled cells are present in the lateralmost part of the medial accessory olive at levels VII-
VIII, in another place than in the other two cases. Labeled cells are found in the nucleus j3 and the dorsomedial cell column in all cases where the injection has resulted in
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staining of the uvula, thus in cat B.St.L. 670 (0.3 pl, survival time 1 day) where there is staining along the track of the inserted needle as a narrow longitudinal strip close to the midline through the caudal folia of lobule VIIIB and of the rostralmost uvula. Cats B.St.L. 669 (0,4 p1, survival time 1 day) and B.St.L. 692 (0,4 p1, survival time 1 day) are of particular interest. In addition to parts of the uvula also parts of the paramedian lobule andlor lobule VIIIB are stained. However, as in cat B.St.L. 690 (fig. 3A) the lateralmost part of the uvula is not stained on one (B.St.L. 692) or both (B.St.L. 669) sides. As in that case, in the olive contralateral to the side(s) of the unstained lateral uvula there is no labeling in the part of the medial accessory olive labeled in cats B.St.L. 668 and 690, described above, while the area in the ventral lamella (see figs. 1 and 3 ) contains labeled cells as do the nucleus J3 and the dorsomedial cell column.
Interpretation of findings The cases described above show that following injections of HRP in the uvula there is consistently labeling of a considerable proportion of neurons in the nucleusJ3 and the dorsomedial cell column. When the staining of the uvula extends to its lateral border and has spread to the paramedian lobule (as in figs. 1, 3A), there are in the contralateral olive in addition labeled cells in an area in the ventral lamella of the principal olive and in two restricted areas in the medial accessory olive. These additional areas might be assumed to be due to the concomitant staining of the paramedian lobule. Indeed, the area in the ventral lamella coincides with the area projecting onto that lobule, as determined previously (Brodal et al., ’75). The paramedian lobule receives fibers also from a n area of the rostral half of the medial accessory olive. However, this area is found more medially than that shown in figures 1 and 3A, although the two areas overlap a little (fig. 4). No evidence has been found for a projection to the paramedian lobule from the caudal part of the medial accessory olive. It appears, therefore, that labeling in the caudal and (at least most of the) rostral area in the medial accessory olive in the cases shown
MEDIAL
ACC OLIVE
Fig. 4 Diagram showing the main features in the pattern of the olivary projection to the uvula as determined here. The areas in the medial accessory olive may be more extensive than shown. The heavy broken line in the medial accessory olive outlines the area of this which projects to the paramedian lobule according to Brodal et al. (’75). Cp. text. For abbreviations see list on p. 418.
in figures 1 and 3 A is caused by the presence of HRP in the uvula. The olivocerebellar projection is practically completely crossed. Labeling in the medial accessory olive is seen only in the olive contralateral to the side where the staining of the uvula extends to its lateral border. It appears thus that the two areas in the medial accessory olive project to the most lateral part of the uvula, while the dorsomedial cell column and the nucleus j project heavily to a large medial zone of the uvula. The few faintly labeled cells laterally in the medial accessory olive in cat B.St.L. 698 (fig. 3B) are found in the projection area of lobulus VIII (Hoddevik et al.,’76, submitted) and can be explained by some leakage of fiuid along the track of the needle, which was inserted through this lobule. Labeling in the dorsomedial cell column and the n u c l e u s j does not extend to their rostral poles when the injection is restricted to the ventral parts of the uvula (fig. 3A), but does so with injections placed in its middle or dorsal folia (figs. 1, 3B). This suggests that there is some topical correlation between the uvula and each 1 When the paramedian lobule-projecting areas in the dorsal lamella and dorsal and medial accessory olives (see Brodal et al., ’75) were not labeled in the cases described here, this may h e d u e to the projection from the ventral lamella being the “main” o n e to the paramedian lobule. In the retrograde cell loss mappings (Brodal, ’40b) this olivary area was theonly o n e showing changes following ablation of the paramedian lobule
OLIVOCEREBELLAR PROJECTION TO THE UVULA
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of the two olivary cell groups, even if there fastigii,Z and some cells in the nucleus is considerable overlapping. j3 appear to project to the vermal lobulus Figure 4 summarizes the conclusions VII (Hoddevik et al., ’76). Alley et al. drawn from the present material. It (’75) found labeled cells in the nucleus should be noted that the “uvular” areas j3 following injections in the nodulus. in the medial accessory olive may be some- Even if there was spreading to the uvula what larger than shown, since the lateral in their cases, it is quite possible that part of the uvula was never stained in its the nodulus as well a s other, so far not studied, cerebellar lobules may receive totality . fibers from the nucleus j3 and the dorsoDISCUSSION medial cell column. The dorsomedial cell column and the The fact that three-fourths or more of nucleus j3 are characteristic and well de- the cells in the nucleus j3 and dorsofined morphologic units of the inferior medial cell column are heavily labeled fololivary complex i n the cat (Brodal, ’40b; lowing injections in the uvula suggests, Taber, ’61; seen but not labeled in Ber- but does not prove, that the other projecman’s atlas, ’68) and rabbit (Brodal, ’40b; tions, to the fastigial nucleus and other Meessen and Olszewski, ’49). They can destinations, may be established by colbe identified in man (Mareschal, ’34; laterals of axons passing to the uvula. Brodal, ’40b), in Cetacea (Korneliussen (For some comments on this problem, see and Jansen, ’64), in the rhesus monkey Walberg et al., ’76.) This may explain (Bowman and Sladek, ’73), and are prob- why only following ablations of this lobule ably present in many species, including clearcut retrograde cell loss was obthe opossum (Martin et al., ’75). The fact served in the nucleus j3 and the dorsothat a majority of their cells sends axons medial cell column (Brodal, ’40b). Furto the uvula, may be a n expression of ther studies may well reveal that the their morphologic and probably function- areas found here in the medial accessory olive have projections to other cereal individuality. The distribution of retrograde cell loss bellar areas in addition to the uvula. Physiological studies, performed so far, in the olive following ablations of various cerebellar lobules (Brodal, ’40b) were in- do not give much information on the terpreted as showing that all axons of olivary projection to the uvula. Only its neurons in the nucleus j3 and the dorso- rostralmost folium is accessible to surface medial cell column pass to the uvula and recordings of evoked potentials or surface only to this. While it has been confirmed stimulation. Following electrical stimulathat these two small nuclear groups pro- tion of the inferior olive in cats Dow (‘39) ject heavily to the uvula the use of the recorded potentials from the entire cereHRP-method has shown that the situation bellar surface, including the uvula. Acis far more complex. The uvula in addi- cording to VanGilder and OLeary (‘70) tion receives fibers from two areas of the responses in the uvula are evoked only contralateral medial accessory olive, and from the caudal part of the medial acit appears that these supply the lateral- cessory olive (their fig. S), but more spemost parts of the uvula (fig. 4). Whether cific sites could not be given. Armstrong, some fibers from the nucleus j3 and the Harvey and Schild (‘74) do not specificaldorsomedial cell column reach the lateral ly mention projections to the uvula in parts cannot be decided from the present their extensive study of the occurrence material, because lateral injections al- of antidromic responses in the olive folways spread medially. It appears, how- lowing stimulation of the cerebellar corever, that the medial zone is considerably tex. From their diagram (their fig. 5) it cannot be decided if the caudalmost part broader than the lateral. Furthermore, our HRP-studies show of the vermis shown in the diagram bethat axons of cells in the two small olivary longs to the uvula. Probably the folium cell groups do not supply the uvula only, 2 It should be noted that in most cases of Injections in but other cerebellar areas as well. Thus a uvula with resulting heavy labeling of the neurons fair number of cells in both groups are the m the nucleus@ and dorsomedial cell column there was labeled following injections in the nucleus no evldence of spreadmg of HRP to the fastigial nucleus
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left white is its rostralmost folium. Recording electrodes were not placed in the dorsomedial cell column (their levels 9.5 and lO.O), while what appears to be the nucleus J3 (their levels 12.5, 13.0 and 13.5) is shown as projecting to what is probably Larsell's lobules VI and VII (cfr. Hoddevik et al., '76, submitted). It appears from the findings made in the present study that the lateral part of the uvula differs from the medial part with regard to its projections from the olive (fig. 4). In general this would fit with the presence of a longitudinal zonal subdivision of the cerebellum, demonstrated physiologically as well as anatomically. Little information can, however, be obtained from the literature concerning this problem as far as the uvula is concerned. Embryogenetic studies indicate that the longitudinal subdivision extends throughout the vermis and includes the uvula (Korneliussen, '69). Voogd ('69) does not specifically mention a zonal subdivision in lobulus IX (the uvula), but from his figure 9 (from the ferret) it appears that his vermal zone B may extend caudally into the uvula. Physiologic a1 studies on longitudinal zones of the uvula are apparently not available, but when performed might give valuable information concerning a longitudinal subdivision of the uvula, suggested by the present findings. The topographical relation of dorsal and ventral parts of the uvula with rostra1 and caudal parts, respectively, of the dorsomedial cell column and the nucleus J3 (fig. 4) parallels a similar arrangement within the olivary projection to the paramedian lobule, particularly from the ventral lamella (Brodal et al., '75). It may be conjectured that the topographical relation between the two small olivary groups and the uvula bears some relation to functional differences between dorsal and ventral parts of the uvula, since primary vestibular fibers have been shown to reach the latter only (Dow, '36; Brodal and Haivik, '64). While the dorsomedial cell column and the nucleus j3 send a majority of their axons to the uvula, as concerns their afferents a quantitatively dominant source has so far not been found. Indeed, it appears that both cell groups receive affer-
ents from a number of sources, thus from the cerebral cortex (Walberg, '56), particularly the "motor" region (Sousa-Pinto and Brodal, '69; Sousa-Pinto, '69) and from the spinal cord (Brodal et al., '50; Mizuno, '66, however, considers these fibers as probably passing ones). Fibers have further been traced to one or both of these small subdivisions from various sites in the mesencephalon, thus from its reticular formation (Walberg, '56, '60, '74), from the central (periaqueductal) gray (Walberg, '56, '60, '74), the pretectal areas (Mizuno et al., 73) and the superior colliculus (Escobar and de Ckrdenas, '68). Some authors studying olivary afferents do not comment on these small olivary subdivisions, but from their illustrations it is seen that, for example, some fibers from the dentate-interpositus reach the nucleus J3 (Graybiel et al., '73, their fig. 3). Boesten and Voogd ('75) picture fibers ending in both cell groups following lesions of the dorsal column nuclei. It appears thus that the nucleus J3 and the dorsomedial cell column may serve an extensive integration of impulses from various sources, and that they primarily influence the uvula (in addition to other regions, among them the fastigial nucleus). Their involvement in the transmission of visual impulses to the cerebellum appears particularly likely on the basis of the demonstration of Simpson et al. ('74) that electrical or flash stimulation of the optic chiasm or the retina, respectively, elicits climbing fiber responses in the ventral uvula. (For some further comments on pathways for visual impulses to the cerebellar vermis, see Hoddevik et al., '76, submitted). ACKNOWLEDGEMENTS
I a m greatly indebted to Professor F. Walberg and Dr. Grethe Hoddevik for performing the surgery and the perfusion of the animals. LITERATURE CITED Alley, K., R. Baker and J. I. Simpson 1975 m e r e n t s to the vestibulo-cerebellum and the origin of the visual climbing fibers in the rabbit. Brain Res., 98: 5 8 2 5 8 9 . Armstrong, D. M., R. J. Harvey and R. F. Schild 1974 Topographical localization i n the olivocerebellar projection: A n electro-physiological
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axonal transport of horseradish peroxidase. 111. The projection to the vermal visual areas. J. Comp. Neur. Korneliussen, H. K. 1969 Cerebellar organization in the light of cerebellar nuclear and cerebellar corticogenesis. In: Neurobiology of Cerebellar Evolution and Development. R. Llinas, ed. Chicago, Illinois, pp. 515-523. Korneliussen, H. K., and J. Jansen 1964 The morphogenesis and structure of the inferior olive of cetacea. J. Hirnforsch., 7: 301-314. Kristensson, K., Y. Olsson and J. Sjgstrand 1971 Axonal uptake and retrograde transport of exogenous proteins in the hypoglossal nerve. Brain Res., 32: 399406. Larsell, 0. 1970 The Comparative Anatomy and Histology of the Cerebellum from Monotremes through Apes. J. Jansen. ed. The Unikersity of Minnesota Press, Minneapolis, 269 pp. LaVail, J. H., and M. M. LaVail 1972 Retrograde axonal transport in the central nervous system. Science, 176: 1416-1417. Mareschal, P. 1934 L'Olive Bulbaire, AnatomieOntogenese-Physiologie et Physiopathologie. Paris, G. Doin t 3 Cie., 215 pp. Martin, G. F., R. Dom, J. S . King, M. Robards and C. R. R. Watson 1975 The inferior olivary nucleus of the opossum (Didelphis marsupialis v i r g i n i a n a ) , its organization and connections. J. Comp. Neur., 160: 5 0 7 5 3 4 . Meessen, H., and J. Olszewski 1949 A Cytoarchitectonic Atlas of the Rhombencephalon of the Rabbit. S. Karger, Basel. Mizuno, N. 1966 An experimental study of the spino-olivary fibers in the rabbit and the cat. J. Comp. Neur., 127: 267-292. Mizuno, N., K. Mochizuki, C. Akimoto and R. Matsushima 1973 Pretectal projections to the inferior olive in the rabbit. Exp. Neurol., 39: 498-506. Rinvik, E., and F. Walberg 1975 Studies on the cerebellar projections from the main and external cuneate nuclei in the cat by means of retrograde axonal transport of horseradish peroxidase. Brain Res., 95: 371381. Simpson, J. I., W. Precht and R. Llinas 1974 Sensory separation in climbing and mossy fiber inputs to cat vestibulocerebellum. F'fliigers Arch., 351 : 183-193. Sousa-Pinto, A. 1969 Experimental anatomical demonstration of a cortico-olivary projection &om area 6 (supplementary motor area?) in the cat. Brain Res., 16: 73-83. Sousa-Pinto, A , , and A. Brodal 1969 Demonstration of a somatotopical pattern in the corticoolivary projection in the cat. An experimentalanatomical study. Exp. Brain Res., 8: 364386. Taber, E. 1961 The cytoarchitecture of the brain stem of the cat. I. Brain stem nuclei of cat. J. a m p . Neur., 116: 27-70. VanGilder, J. C., and J. L. O'Leary 1970 Topical projection of the olivocerebellar system in the cat: An electrophysiological study. J. Comp. Neur., 140: 69-80. Voogd, J. 1969 The importance of fiber connections in the comparative anatomy of the mamalian cerebellum. In: Neurobiology of Cerebellar Evolution and Development. R. Llinas ed., Chicago, Illinois, pp. 493514.
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