Brain Research, 123 (1977) 209-227

209

© Elsevier/North-Holland Biomedical Press, Amsterdam - Printed in The Netherlands

T H E P O N T I N E P R O J E C T I O N TO T H E C E R E B E L L A R V E R M A L VISUAL AREA S T U D I E D BY MEANS OF T H E R E T R O G R A D E A X O N A L TRANSP O R T OF H O R S E R A D I S H P E R O X I D A S E

G. H. HODDEVIK, A. BRODAL, K. KAWAMURA and T. HASHIKAWA (G.H.H. and A.B.) Anatomical Institute, University of Oslo, Oslo 1 (Norway), and (K.K. and T.H.) Department of Anatomy, School of Medicine, Iwate Medical University, Morioka (Japan)

(Accepted July 2nd, 1976)

SUMMARY Following injections of horseradish peroxidase (HRP) in cerebellar vermal lobules VI, VIIA and B, VIIIA and B in the cat, the distribution of labeled cells in the pontine nuclei was mapped in drawings of serial transverse and horizontal sections. The labeled pontine cells are distributed in 4 largely longitudinal columns, situated in the dorsolateral, peduncular, lateral and paramedian pontine nucleus (referred to as columns A, B, C and D, respectively). The majority of afferents to the vermal, visual areas come from columns A and B. To some extent cells projecting to the various sublobules have their preferential location within each column (Fig. 5). The majority of the fibers end in lobule VII. Available data from the literature show that only columns A, D and rostral part of B may be involved in the transmission of visual impulses to the vermal area, since these columns receive afferents from the superior colliculus, the lateral geniculate body and the visual cortex, respectively. The route via the superior colliculus-dorsolateral nucleus appears to be quantitatively the most important. As judged from data on fiber connections, impulses from various sources (inferior colliculus, cerebellar nuclei and "non-visual" parts of the cerebral cortex) are transmitted to certain parts of the 4 columns. The functional importance of this convergence and some general features in the organization of the pons are discussed.

INTRODUCTION A preceding paper al dealth with the projection from the inferior olive to the cerebellar visual area of Snider and StowellSa, 54 as determined with the horseradish peroxidase (HRP) method. This cerebellar region (corresponding mainly to vermal lobules VI-VIII of Larsel141) was found to receive its olivary afferents from a horse-

210 shoe-shaped area in the caudal half of the medial accessory olive. Lobules VI, VII and VIII receive their fibers from particular, although in part overlapping, parts of this area. However, descending pathways which might be assumed to transmit impulses of visual origin to the olive appear to be very scanty and only to a little extent to reach the areas projecting to lobules V I - V I I I (see ref. 31). The pontine nuclei appear to be a far more important relay station than the inferior olive in pathways mediating visual impulses to the cerebellum, since the pontine nuclei have repeatedly been shown to receive fibers from the visual areas of the cerebral cortex12,13,24,2~,40,4~,47, and others, as well as from the superior colliculus 1'19,36'44,46,4s,49,56,57, and the pons projects to the cerebellar cortex including the vermis6,55, 5s. (For further references see ref. 33.) Recent studies have shown that the pontine afferents from the visual cortex as well as those from the superior colliculus terminate in well circumscribed minor regions of the pons. P. Broda112,13 found the former to end in several, well delimited, mainly transverse bands in the rostral half of the pontine nuclei, and K a w a m u r a and Brodal a~ traced the latter to a rather large area in the dorsolateral part of the pons. Brodal and Jansen 6 concluded from the distribution of retrograde cellular changes following lesions of various cerebellar lobules (modified Gudden method z) that the cerebellar vermis receives its fibers from the dorsolateral, the paramedian and part of the ventral gray. However, these rather crude data do not permit a satisfactory correlation with the recent data on the pontine terminal areas mentioned. The occurrence of labeling of pontine neurons following cerebellar injections of H R P is briefly mentioned in some recent studies27,2s,42, 51. In a previous study a0 it was shown that the method of tracing the axonal retrograde transport of H R P permits a mapping of the pontocerebellar projection in considerable detail. It was, therefore, decided to use this method in an attempt to determine the precise sites of the pontine nuclei from which fibers pass to the cerebellar vermal visual area, and secondly to see if it is possible to correlate the pontine areas determined in this way with the sites of termination of pontine afferent fiber systems which may mediate visually evoked impulses to the pons. MATERIAL AND METHODS Most of the material used in the present study is the same as that used in the preceding study of the olivary projection to the cerebellar vermal visual area al. It consists of 14 cats and 5 kittens. For particulars concerning methods the reader is referred to that paper and to Walberg et al. 60. Suffice it here to mention that following injections of H R P (type Sigma VI, in one case type Serva, most often 0.15-0.5 #1 of a 5 0 ~ wt./vol, suspension) in vermal lobules VI, VII or VIII and survival periods of 1-3 days, serial frozen sections of 50-60/~m were prepared of the cerebellum (sagittal) and pons (tranverse or horizontal) and treated according to G r a h a m and Karnovsky z6 to visualize HRP. The serial sections were collected in groups of five. From each group one section was mounted unstained, the other was weakly stained with cresyl violet. The injection site and the brown staining of the cerebellar cortex were entered in

211 projection drawings of the sections from the cerebellum and transferred to a diagram of the cerebellar surface taken from Larsel141. Labeled cells in the pons were entered in drawings of the pons made under a projection apparatus, in some cases an x-y writer was used. The broken lines in the drawings of the pons refer to Brodal and Jansen's 6 subdivision of the pontine gray in subnuclei. Since the borders between the various subnuclei (indicated in Figs. 2 and 5) are not sharp, the subdivision serves mainly to facilitate the description. Although labeled cells have been found in the reticular tegmental nucleus they have not been systematically mapped, and the nucleus is not indicated in the diagrams. Areas of the pontine nuclei proper containing labeled cells are indicated by dots, the density of dotting serves to give an impression of the relative density of labeled cells. To give a better view of the distribution of labeled cells which occur mainly as longitudinal columns (see below) a simple diagram of these columns is added in the figures. In the diagram summarizing our results (Fig. 5) the findings in the pons in the transversely cut cases were transferred to a standard diagram of the pons. This is only slightly different from the standard diagram worked out for the pons in 2-3-week-old kittens by Brodal and Jansen 6. RESULTS Following injections of H R P in the vermal visual areas, labeled cells are consistently found in the pontine nuclei. The intensity of labeling varies somewhat a m o n g cases. The picture of labeled neurons corresponds to those seen elsewhere, for example in the pontine nuclei and other precerebellar nuclei following cerebellar injec-

Fig. 1. Photomicrographs showing labeled cells in the pontine nuclei following injection of horseradish peroxidase (HRP) in the vermal visual area. a: cell group A in the dorsolateral pontine nucleus at level V in the case shown in Fig. 2. Dark-field illumination, x 115. b: single cell from the same cell group. Dark-field illumination, x 560.

212 tions3,7,15,a0,31, 60. Fig. l b shows an example. Even if scattered labeled cells occur in m a n y p a r t s o f the p o n t i n e nuclei it is characteristic t h a t in all cases the m a j o r i t y o f labeled cells are d i s t r i b u t e d in the form o f a p p r o x i m a t e l y l o n g i t u d i n a l c o l u m n s (as is the case following injections in the p a r a m e d i a n lobulea0). The b o r d e r s between these c o l u m n s t o w a r d s the s u r r o u n d i n g p o n t i n e g r a y are often quite s h a r p (Fig. l a). In some cases there has been s p r e a d i n g o f H R P to small p a r t s o f the fastigial nucleus, evidenced by a light b r o w n staining o f the neuropil or by the presence o f some labeled cells (see ref. 60 for particulars). F o r this reason some cases with injections into the fastigial nucleus have been studied as controls. There are only m i n o r v a r i a t i o n s in the d i s t r i b u t i o n o f labeled cells between cases with injections o f lobules VI, VII or VIII. Cases where larger p a r t s o f m o r e t h a n one o f these lobules are s t a i n e d are best suited to give an i m p r e s s i o n o f the a p p r o x i m a t e total distribution. The findings in c a t B.St.L. 642 m a y serve as an example. In this a n i m a l (weight 2.7 kg, 0.5 #1 ,survival time 2 days, Fig. 2) the staining o f the cerebellum covers the majorpart oflobules VI, VIIA and B bilaterally. In the fastigial nuclei there is a faint b r o w n i s h staining, a n d some labeled cells occur. In the pons l a b e l e d cells are present at all transverse levels in a p p r o x i m a t e l y equal n u m b e r s on b o t h sides. In the c a u d a l 2/3-3/4 o f the pons, labeled cells are a g g r e g a t e d in 4 groups. W h e n followed in successive sections these g r o u p s constitute a p p r o x i m a t e l y longit u d i n a l l y oriented columns. M o s t o f these g r o u p s are s h a r p l y delimited f r o m the s u r r o u n d i n g areas c o n t a i n i n g unlabeled cells (Fig. la). One o f the columns (in the following referred to as c o l u m n A) is a l m o s t entirely restricted to the d o r s o l a t e r a l nucleus and extends r o s t r o c a u d a l l y f r o m level V I I I to level IlI. M o s t o f the second m a i n c o l u m n (B) is situated in the v e n t r o m e d i a l p a r t o f the p e d u n c u l a r nucleus f r o m level X to I, b u t at levels V I I I - I V it encroaches u p o n the ventral nucleus. A t c a u d a l levels ( I I I - I I ) it is connected b y small cell s t r a n d s with a third group, situated in the ventral p a r t o f the lateral nucleus. This g r o u p can be t r a c e d rostrally a n d is f o u n d to continue as a t h i r d c o l u m n (C) extending f r o m level II to IX. A f o u r t h c o l u m n (D) is present f r o m level I X to I I a n d is represented by a few cells lying closely t o g e t h e r in the p a r a m e d i a n nucleus, n o t far f r o m the midline, at some levels it slightly invades the m e d i a n

Fig. 2. Diagrams showing the findings in cat B.St.L. 642. A: the HRP-positive areas are indicated in a drawing of part of the cerebellar surface (after Larsel141). Black denotes staining of the molecular layer. Hatching indicates staining of the other cortical layers or the white matter. Staining involves lobules VI, VIIA and part of VIIB. B: the stained areas as seen in a midsagittal section of the cerebellum. C: drawings taken with equal intervals from a series of transverse sections through the pons from rostral (level X) to caudal (level I). Labeled cells are equally distributed on the two sides, but are indicated only on the right side by dots. Different densities of dotting indicate varying densities of labeled cells. The left half of the pons shows a schematic presentation of the areas with a large number of labeled cells. These form approximately longitudinal columns marked A, B, C and D. More diffusely occurring labeled cells are not indicated (cf., right side of pons). The borders between the subdivisions of the pontine gray (according to Brodal and Jansen') are indicated by broken lines. D: a diagram to visualize the columns and their longitudinal extent through the pons when reconstructed on the basis of the transverse drawings above. Abbreviations: N.dl., dorsolateral pontine nucleus; N.I., lateral pontine nucleus; N.m., medial pontine nucleus; N.p., peduncular pontine nucleus; N.pm., paramedian pontine nucleus; N.v., ventral pontine nucleus; L, left; R, right.

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214 a n d the p e d u n c u l a r nuclei. T h e c o l u m n has a m o r e ventral p o s i t i o n at rostral t h a n at c a u d a l levels. The c o l u m n s often have a s o m e w h a t t o r t u o u s course a n d frequently emit small s t r a n d s o f labeled cells in different directions. A p a r t i c u l a r l y distinct s t r a n d is t h a t c o n n e c t i n g c o l u m n s B a n d C at c a u d a l levels ( I I I - I I ) . This is m o r e obvious in h o r i z o n t a l sections (Fig. 3, arrows). A smaller n u m b e r o f labeled p o n t i n e cells t h a n in cat B.St.L. 642 (Fig. 2) b u t a c o r r e s p o n d i n g d i s t r i b u t i o n are f o u n d in cat B.St.L. 660 (1.5 kg, 0.5 ffl × 3, 1 day, n o t

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Fig. 3. Diagrammatic representation of the distribution of labeled cells as seen in a series of equally spaced horizontally cut sections from ventral (level 1) to dorsal (level 11) following an injection which has resulted in staining mainly of lobules VI, VIIA, VIIB, V i l l a and VIIIB as shown in the diagram of the cerebellum above. Arrows point to cell strand connecting columns B and C. Symbols and principles of presentation as in Fig. 2. For abbreviations see legend to Fig. 2.

215 illustrated) in which the staining of the cerebellum is limited to 3 small areas on the surface of lobules VI, VIIA and VIIB, respectively. A horizontally cut case, cat B.St.L. 724 (2.6 kg, 0.5 #1 x 2 and 0.4 x 3, 3 days, Fig. 3), with staining of major parts of lobules VI-VIII supplements the findings described above. There is no staining of the fastigial nucleus which contains a few labeled cells. In the pons well labeled cells are concentrated in certain regions, which correspond to the columns described above. At caudal levels the cell strand connecting columns B and C, described above, is clearly seen, particularly at horizontal levels 3-5, but visible also at level 6 (arrows in Fig. 3). Following injections of individual lobules of the vermal visual area most labeled cells are found within the areas described above. However, the projections of the different lobules show slight variations. Lobule VI

Three cases, each with circumscribed injections in lobule VI, visualize the pontine projection onto this lobule. The cases will be described separately, but the findings are summarized in one figure (Fig. 4A). In cat B. St. L. 655 (1 kg, 0.075/A, 1 day, Fig. 4A), the cerebellum is mainly stained on the left side of lobule VI with only a slight spreading to lobule VIIA. There is no spreading to the fastigial nuclei. In cat B.St.L. 658 (1.9 kg, 0.2/~1, 1 day, Fig. 4A), the staining of the cerebellum is restricted to parts of the two rostralmost folia of lobule VI, mainly on the right side. There is no spreading to other cortical areas or to the fastigial nuclei. In cat B.St.L. 657 (1.2 kg, 0.075 #1, 1 day, Fig. 4A), there is staining only of a small part of the rostralmost folium of lobule VI on the left. In the pons in these cases rather few, chiefly weakly, labeled neurons are found in the caudal two-thirds, bilaterally distributed with a contralateral preponderance. Column A (levels VII-III) and column B (levels VI-I) are those containing most labeled cells, while column D (levels II-IV) contains only a few labeled neurons. Column C (levels VI-V and II) is likewise faintly outlined. Lobule VIIA In cat B.St.L. 641 (2.4 kg, 0.5 #1,1 day, Fig. 4B), most of lobule VIIA is stained

on both sides. There is a little spreading to the adjoining folia oflobules VI and VIIB, but no spreading to the fastigial nuclei. In the pons well labeled cells are present in apparently equal numbers on both sides between levels IX and I. All 4 columns can be identified. Column A (levels VIII-IV) is particularly conspicuous. Column B (levels IX-I) is clearly most dense caudally, column C (levels VIII-V and IV-II) contains relatively few labeled cells, while column D (levels IX-III) is quite marked. Corresponding findings are made in cat B.St.L. 640 (350 g, 0.15/A, 1 day, not illustrated) in which the staining of the cerebellum is restricted to the rostralmost folia of lobule VIIA, with a slight spreading to lobule VI and to the fastigial nuclei. Lobule VIIB

In cat B.St.L. 687 (1.2 kg, 0.3 #1, 3 days, Fig. 4C), the staining of the cerebellum is restricted to both sides of the rostralmost folium of lobule VIIB with insignificant

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217 spreading to the adjoining folia rostrally and caudally. Homogenous brown fibers run to the fastigial nuclei, but there is no staining of these. In the pons distinctly labeled cells occur in apparently equal numbers on the two sides. Column A (levels VIII-IV) is the most dominating. In column B (levels X-II) the preponderance of labeled cells at caudal levels seen following injection of lobule VIIA (Fig. 4B) is not present. Column C (levels V-IV) contains only few labeled cells. Column D (levels VIII-Ill) is well outlined. A similar distribution of labeled cells in the pons is found in cat B.St.L. 679 (4 kg, 0.5 #I, 2 days, not illustrated) in which the staining of the cerebellum is restricted to the caudal part of lobule VIIB, mainly on the right side. There is no spreading to the fastigial nuclei. In the pons labeled neurons are present mainly on the left side. Corresponding findings are also made in cat K E N 7 (2.3 kg, 0.08 #1 x 1, 0.15 #1 x 3, 2 days, horizontally cut, not illustrated). The staining of the cerebellum comprises mainly lobule VIIB, but extends to the adjoining folia of lobule VIIA. There is no spreading to the fastigial nuclei. In the pons labeled neurons are distributed in columns corresponding to those described above. Lobule V i l l a In cat B.St.L. 682 (750 g, 0.3/A, 2 days, Fig. 4D), mainly the middle folium of

lobule VillA on the left side is stained. There is no spreading to the fastigial nuclei. In the pons labeled neurons are distributed bilaterally mainly in the caudal half with an overweight on the right side. Only three of the main columns can be identified. Column A (levels VIII-II) is situated more ventrally than in the preceding cases with most of the cells crowded in its caudalmost portion. In column B (levels VII-II) labeled cells are most densely packed at level III. Column D (levels VIII-VII) is faintly outlined. A corresponding distribution of labeled cells is found in cat B.St.L. 681 (2.7 kg, 0.4 #1, 2 days, not illustrated) where the staining of the cerebellum is restricted to the middle and rostral folia of lobule VillA, mainly on the right side, and in cat B.St.L. 680 (2.6 kg, 0.4 #1, 2 days, not illustrated) where the staining of the cerebellum covers the caudal folium of lobule VIIIA and the adjoining part of lobule VIIIB. In cat K E N 14 (2.7 kg, 0.09/A x 3, 0.15 #1 x 1, 1 day, horizontally cut, not illustrated), there is staining almost exclusively of lobules VIIB and VillA. In the pons column B is most conspicuous, column A contains many labeled cells, column C relatively few, and column D only scattered ones. Lobule VIIIB In cat B.St.L. 722 (0.9 kg, 0.3 #I H R P type Serva, 1 day, Fig. 4E), the staining

Fig. 4. Diagrammatic representation of the findings in some cases where staining of the cortex is restricted to minor regions of the vermal visual area. To the left, diagrams of the stained areas of the cortex, in the middle, representative sections through the pons with indication of the distribution of HRP-labeled cells, to the right longitudinal reconstructions of the columnar distribution of cells. The uppermost series of drawings integrates the findings in 3 cases with injections coveringslightly different areas of lobule VI. Symbols and principles of presentation as in Fig. 2.

218 of the cerebellum is restricted to the 3 rostralmost folia of lobule VIIIB, mainly on the right side. There is no spreading to other parts of the cerebellar cortex or to the fastigial nuclei. In the ports labeled cells are present mainly on the left. Column A (levels VIII-Ill) and column B (levels VII-V) are the most dominating cell groups in this case. Column C is lacking while there are a few cells in column D (levels IV-Ill). Corresponding findings are made in cat B.St. L. 651 (775 g, 0.05/,1, 75 ~ HRP, 1 day, not illustrated).

The fastigial nucleus To decide whether the spreading of H R P to the fastigial nuclei may have any influence upon the results described above, two cases with stereotaxic injections of HRP in the fastigial nucleus were studied. In cat B.St.L. 702 (4.2 kg, 0.2/~1, 3 days, not illustrated), H R P staining is restricted to a circumscribed area in the middle part of the left fastigial nucleus. In the ports 3 labeled cells on the right side are found in the whole series. In another case (cat B.St.L. 695, 2 kg, 0.25/,1, 3 days, not illustrated) with H R P staining of the posterior part of the left fastigial nucleus, there was some spreading across the midline and also some to the cortex of lobule VI. However, in the pons extremely few labeled cells are found, most of them on the right side. Synopsis of findings As described above following HRP injections in lobules VI-VIII, labeled cells in the pons tend to be aggregated in certain areas that largely have the shape of longitudinally oriented cell columns. This is particularly evident in horizontally cut sections. In transversely cut sections the columns appear as groups of cells which are not always well defined, because the columns often show small expansions or constrictions, may have greater or smaller ramifications and may be connected with neighboring columns by small strands of cells. Altogether 4 columns can be distinguished. Within the different columns the distribution of cells which project to the various sublobules follows no general pattern, but in most columns there is an arrangement which indicates that cells projecting to a particular lobule tend to lie together in more or less intertwined longitudinal rows along the length of the columns. In Fig. 5 an attempt is made to visualize the projections from the various columns onto the particular lobules. These are not identical. Since there are only minor differences between the projections to the two sublobules (A and B) of lobules VII and VIII, respectively, these differences are not indicated in the diagram. Some points deserve mention. The majority of pontine cells projecting to the vermal visual area supply lobule VII, while a far smaller number send axons to lobules VI and VIII (see symbols in sections of pons to the right). Lobule VII receives afferents from all 4 columns, and in all columns the majority of cells project to this lobule. Furthermore, such cells occur throughout the length of all 4 columns. In contrast, lobule VIII receives fibers from three of the columns only (A, B and D), the majority from columns A and B. Lobule VI receives fibers from all columns, but in relatively modest numbers. It is seen from Fig. 5 that there is no topographical correlation between particular lobules and the sites of their projection areas along the longitudinal extent of the

219 columns (except that it a p p e a r s that in column D lobule V I I I A receives fibers f r o m a group situated m o r e rostrally than that supplying lobule VIIIB). N o r can any clearcut l:attern be discerned in the transverse plane (see Fig. 5, right pons). ROSTRAL

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Fig. 5. Diagram summarizing the results of the present study. Above a series of equally spaced transverse sections through the pons from rostral (X) to caudal (I). On the right the distribution of cells labeled following injections in lobules VI, VII and VIII is indicated by different symbols, referring to the diagram of these lobules shown below to the left. On the left side of the pontine sections the sites of the 4 columns (A, B, C and D) are indicated. The diagram below to the right shows the longitudinal extent of the columns and the parts of these which project to lobules VI, VII and VIII, respectively. The quantitative differences in the projections to the various lobules are not indicated, but can be seen from the transverse drawings of the pons (right side) above. For abbreviations see legend to Fig. 2.

220 As described above, in some cases there is spreading of the injected HRP suspension to the fastigial nucleus. Following stereotaxically placed injections in this nucleus extremely few labeled cells are present in the pontine nuclei. Most injections in our material, however, are pure cortical ones, and there is no difference in the distribution of labeled cells in the pons between these cases and those with spreading to the fastigial nucleus. The slight spreading to the fastigial nucleus in some cases, therefore, does not invalidate the interpretation of findings made above. DISCUSSION The method of retrograde transport of HRP has been found to be valuable in the study of the pontocerebellar projection (concerning some comments on the use of the method in studies of cerebellar afferents, see ref. 60). The main problem is to determine the cortical area from which absorption of the enzyme has occurred. From studies in other regions of the brain it has been concluded that the distribution of retrogradely labeled neurons is smaller than might be predicted from the extent of the diffusion of HRP as witnessed by the peroxidase-positive area at the injection site (ref. 18, and others). However, in the present material (as well as in our studies of the olivocerebellar projection) the diffuse brownish stained area of the cerebellar cortex around the injection site has been found to be an indicator of the size of the terminal field of axons of labeled cells since there is a consistent correlation between the size (and site) of a stained cortical area and the distribution of pontine (or olivary) cells. It appears, therefore, that in the cerebellar cortex the enzyme is absorbed not only in the immediate vicinity of the injection site or by injured fibers along the needle track 20, but more or less from the entire brownish stained area. In order not to underestimate the size of the terminal field our diagrams are made under the assumption that the enzyme has been absorbed from the total stained cortical area. Topography of the pontine projection to the vermal visual areas Following injections of H R P in lobules VI-VIII the majority of pontine labeled neurons are consistently distributed in 4 longitudinal columns (to facilitate description here called columns A, B, C and D), while a fifth, less marked, concentration at caudal levels is oriented approximately transversely (see Fig. 3, arrows). It is likely that the density of labeled cells in the columns might have been greater, and that the columns might have appeared somewhat larger than found here, if it had been possible to achieve a complete staining of all folia belonging to a particular lobule. For technical reasons this ideal goal has not been reached. Nevertheless, the findings permit a determination of the main features in the pattern of the pontine projection to the vermal visual area. It is worthy of notice that a pattern of multiple columnar pontine projection areas, as found in the present study, is in general agreement with that determined in the pontocerebellar projection onto the paramedian lobule 30 as well as with the pattern of distribution of pontine afferents from several regions of the cerebral cortex 8-14 and the cerebellar nucleiL These findings appear to reflect a general

221

principle in the organization of the pontine nuclei: fibers passing to a restricted part of the cerebellum take origin from several pontine regions, usually of columnar shape. Conversely: afferents to the pontine nuclei from a particular source end in several minor regions, likewise often of columnar shape. Quantitatively the 4 columns distinguished here are not equally important in the projection from the pons to the vermal visual area. The regions consistently found to contain maxima of labeled cells are column A (in the dorsolateral nucleus) and column B (largely situated in the peduncular nucleus). Since it is practically impossible to achieve identical staining of the cortex of a particular lobule in different cases, minor variations in location and/or extension of the pontine area of labeled cells must be expected between cases with correspondingly placed injections. Similar considerations apply to comparisons of cases with injections in different lobules. However, in spite of this, a difference in the projection to the various lobules can be discerned (Fig. 5). In part this is reflected by quantitative differences between the projections to the various lobules. Thus a fair majority of projecting cells supply lobule VII, while rather few pass to lobules VI and VIII. Furthermore, although there is great overlapping, certain regions within each column (often appearing as intertwined bands) appear to project preferentially to a particular lobule. On account of the spreading of the injected suspension in the cerebellar cortex, our material is not suited to determine if the columnar pattern can be related to projections to different longitudinal zones of the vermal visual area39.ss,59. Evidence for this was not found in the projection from the olive to this cerebellar area 31. Several mainly unilateral injections show that the projection is bilateral with a contralateral preponderance, as concluded by several previous authors (see refs. 6, 55, 58). Among previous studies of the pontocerebellar projection (see refs. 6, 33, 58) the most detailed one is that of Brodal and Jansen n. Following lesions restricted to the middle vermal area in newborn cats and rabbits a massive cell loss was found in the dorsolateral and the paramedian pontine nuclei. Their Fig. 13 shows that these areas of cell loss coincide remarkably closely with our columns A and D. While Brodal and Jansen do not indicate any retrograde cell changes in the areas of our columns B and C, this may be due to difficulties in recognizing minor degrees of cell loss. Or it may be that there have not been any changes, because the cells are protected from suffering clearcut retrograde cell changes by collaterals to other regions, a phenomenon known from other fiber systems23,32. In studies with silver impregnation methods of the anterograde fiber degeneration following lesions of the pons, Voogd 58 traced degenerating fibers to various parts of the cerebellar cortex, among them lobules VI, VIIA and VIIIA and B. It is in agreement with our findings that degeneration in lobules VI and VIII, particularly the latter, was rather scanty, but conclusions about the areas in the pons giving origin to the fibers to the vermal visual area could not be made. Following injections of tritiated leucine in the dorsolateral pontine nucleus Kawamura and Hashikawaa7 traced fibers to lobule VIIA and B, but few to lobule VI and very few to lobule VIII. Injection in the rostral part of the lateral and peduncular pontine nuclei gave rise to some labeling in lobules VII and VIII.

222 Recently some relevant observations have been made in studies with the HRP method. Thus Graybie127 in a rat found labeling in the dorsolateral and the paramedian pontine gray following H R P injection in what she refers to as the central vermis, and in a study of the cerebellar projection of the raphe nuclei Shinnar et al. 51 found labeling in the pontine nuclei following injection of H R P in lobule VI, VIIA and B in regions appearing to coincide fairly well with our columns A, B, C and D (their Fig. 2). Physiological studies have likewise demonstrated a pontine projection to the posterior vermis but, unfortunately, the pontine region stimulated is not clearly defined. Dow 21 recorded responses in the tuber, culmen, lobulus simplex and pyramis following pontine stimulation, and Sasaki et al. 50 recorded mossy fiber responses in lobules VI-VII following stimulation of what is referred to as the dorsal pontine border. The available data from the literature thus agree well with our findings.

Functional correlations Following the initial demonstration by Snider and Stowel153,54, it has been repeatedly confirmed physiologically that visual stimuli or electrical stimulation of the optic nerve evoke responses in cerebellar lobules VI, VII and VIII and immediately adjoining areas of the cerebellum (see ref. 22 for some references). Stimulation of cerebral viual areas 52 and of the optic chiasma 17 has been shown to yield responses in the same cerebellar areas. Concerning the pathways mediating these impulses it was concluded in a preceding study 81 that the olive can scarcely be important in this mediation, since regions of the brain receiving visual impulses, such as the visual cortex and the superior colliculus, send only very few fibers to the relevant areas of the inferior olive. It is of interest to see if any conclusions can be drawn as to whether the pontine areas shown here to project to lobules V-VIII receive afferents from areas of the CNS concerned with vision. Even if comparisons between findings obtained with different methods and by different authors must be made with caution, such comparisons give some interesting information. Among the pontine columns projecting onto lobules VI-VII those in the dorsolateral and peduncular nuclei (columns A and B) are most impressive (Figs. 2 and 4). The dorsolateral nucleus has been shown by numerous authors to receive afferents from the superior colliculus. It appears from Kawamura and Brodal's 36 precise mapping that the terminal area of these afferents coincides almost completely with our column A (see their Fig. 2). A few fibers from the visual cortex (areas 17, 18, 19) may end in the dorsolateral gray12,13, z6, but the other pontine terminal regions of these fibers coincide neither with column C nor with column B. However, most probably some visual cortical afferents supply the rostral part of our column BlZ,lz. Recently Graybie127, in an autoradiographic study, briefly described some fibers from the ventral nucleus of the lateral geniculate body to the ports, to the paramedian and what is referred to as the lateral nucleus. The terminal area in the former nucleus appears to coincide rather well with parts of our column D. It appears from the available data that the most important route for impulses of visual origin to cerebellar lobules VI-VIII goes via the superior colliculus and the

223 dorsolateral pontine nucleus. The lateral geniculate afferents to column D, and probably some afferents from the visual cortex to the rostral part of column B, may present suppplementary routes for visual impulses via the pons to the vermal visual area of the cerebellum*. These conclusions, based on anatomical observations, are in accord with the classical observation of Snider and Stowell~Z, 54 (see also ref. 22, p. 453) that ablation of the neocortex only slightly influences the transmission of visual impulses to the vermal visual area (see, however, ref. 38). According to our findings lobule VII seems to be that receiving the majority of visual impulses mediated via the superior colliculus, since a large proportion of the cells in the dorsolateral nucleus projects to this lobule. This appears to agree fairly well with physiological observations 2~. Under certain experimental conditions visual evoked responses can be recorded from cerebellar regions outside lobules V I - V I I (see ref. 22 for a review). Further studies of the pontocerebellar projection are needed to decide the cerebellar projections of those pontine cell groups which receive fibers from "visual" regions of the brain but which do not project onto lobules V I - ¥ I I I . It is already shown that cells in the dorsolateral nucleus pass to, or give off, collaterals to other cerebellar areas than lobules V I - V I I I , for example the paramedian lobule, crus II and I and the paraflocculus 37. Studies of the pontine projection to the flocculus (and paraflocculus), recently shown to receive impulses of visual origin 4z, are in progress (Hoddevik). Two other questions deserve comments. (1) Do the pontine areas (columns) mediating visual impulses in addition receive other contingents of afferents than those f r o m the superior colliculus, the lateral geniculate body and the visual cortex? (2) Is any information available concerning sources of afferents to those areas of the columns which project to lobules V I - V I I I , but which apparently are not influenced by visual stimuli? The answer to the first question is 'yes'. The pontine projection from the inferior colliculus is restricted to the ipsilateral dorsolateral nucleus, and its terminal area differs only very little from the terminal area of fibers from the superior colliculusa5, 86. Furthermore afferents from the auditory cortex terminate in the dorsolateral nucleus, rather medially14,zs, 36. Fibers from the cerebellar nuclei to the dorsolateral nucleus 5 end in its ventromedial part, but may overlap somewhat with our column A. Further, there appears to be overlapping with fibers from the second sensorimotor area Sm II 9. The dorsolateral pontine nucleus thus appears to be an important site for integration of visual with acoustic impulses. Small differences between the terminal areas of " o p t i c " and "acoustic" afferents to this nucleus (see ref. 35) may bear a relation to the cerebellar projections of different parts of our column A (see sections of pons, right side in Fig. 5) and to minor differences in the distribution of the physiologically outlined visual and acoustic cerebellar areas. * Following injections of HRP in lobules VI-VIII, a few labeled cells are found in the lateral reticular nucleus, a considerable number in the reticular tegmental pontine nucleus (unpublished observations). These nuclei both receive fibers from the cerebral cortex, but the visual cortical areas appear to send only very few fibers to the former16as well as the latter 4, and likewise only few tectal fibers appear to reach them3n. These reticular nuclei, therefore, are scarcely of much importance in the transmission of visual impulses to the cerebellum.

224 The paramedian nucleus, more particularly our column D, receiving afferents from the lateral geniculate z7, appears to be less purely related to teleceptive impulses than the dorsolateral gray. This column seems to be a site of convergence of impulses from the first s and second sensorimotor cortical area 9, the orbital gyrus tl and the cerebellar nucleiC. The second question raised above concerns regions of the pontine gray (column C and most of column B) which project to lobules V I - V I I I but are devoid of (C) or possibly receive only a few afferents (B) from CNS regions concerned with vision. No information can he found in the available literature about sources of afferents to our column C. Our column B, in the ventromedial part of the peduncular nucleus, however, appears to be situated in the ventral part of the area of termination of fibers from the primary motor cerebral cortex (Ms I), particularly its hindIimb part s. Fibers from the proreatO0 and orbital gyrus 11 have terminal fields which in part cover the area of column B, while fibers from sensorimotor areas I and II (Sm I and Srn II)a, 9 appear not to be distributed to the territory of this column. It appears from the above, that a large proportion of the cells in the pontine columns projecting to vermal lobules V I - V I I I must be concerned in the transmission o f impulses of visual origin. However, impulses from other sources (inferior colliculus, the cerebellar nuclei and certain parts of the cerebral cortex) may influence these cerebellar lobuli via the pons. In part, the pontine columns described here must be the seat of convergence and integration of impulses coming from many sources before they influence the cerebellum. It is in agreement with this that responses have been obtained in vermal lobules V I - V I I I following stimulation of other parts of the cerebral cortex than the visual, for example the auditory and somatosensory areas~9, 34. Both short and long latency responses were recorded (assumed to be due to conduction along mossy and climbing fibers, respectively). In a recent physiological study, Buchtel et al. 17 concluded that although the optic pathways project to the vermal visual area of the cerebellum through both mossy and climbing fiber inputs, the former input seems to be more widespread and constant. This is compatible with the anatomical findings made in this and a preceding study on the projection from the olive to the vermal visual area 3~ that the main pathway for visual impulses to this cerebellar area passes via the pons, while the pathway via the olive seems to be of minor importance. It should, however, be remembered in this connection that it remains to be proved that all climbing fibers originate in the inferior olive.

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The pontine projection to the cerebellar vermal visual area studied by means of the retrograde axonal transport of horseradish peroxidase.

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