The corticopontine projection from the visual cortex in the cat. II. The projection from areas 18 and 19

BRA1N RESEARCH

319

THE CORTICOPONTINE PROJECTION FROM THE VISUAL CORTEX IN THE CAT. II. THE PROJECTION FROM AREAS 18 AND 19

PER BRODAL Anatomical Institute, University of Oslo, Oslo (Norway)

(Accepted October 30th, 1971)

INTRODUCTION This paper is the sixth in a series that deals with the corticopontine projection from different parts of the cerebral cortex in the cat. It has been possible to demonstrate a precise and complicated organization within this projection. The primary sensorimotor cortex, the second somatosensory area, the proreate gyrus and the orbital gyrus all project upon partly common, partly separate, sharply delimited longitudinally oriented cell columns in the caudal two-thirds of the pontine nuclei 6-9. There is a somatotopical localization within several of these components of the corticopontine projection. In a preceding paper 10 certain results concerning the pontine projection from the visual cortex were presented. It was found that the visual cortex as a whole (cortical areas 17, 18 and 19 as defined by Otsuka and Hassler 3a) projects upon several sharply delimited, mainly transversally oriented bands or columns in the rostral half of the pontine nuclei. Area 17 was studied in particular by making use of small, differently placed lesions. It projected upon practically all the total pontine area supplied from the visual cortex as a whole. Not all parts of area 17 have an equally heavy pontine projection. The middle part, roughly corresponding to the representation of the central visual field, gives off few fibers to the pontine nuclei, while rostral and caudal parts, representing peripheral parts of the visual field, project heavily. Furthermore, there is a topical localization within the pontine projection from area 17. Caudal parts project more medially within the pontine nuclei than do rostral parts. Medial and lateral parts of area 17 also project to different areas within the pontine nuclei. In the present study results concerning the pontine projection from areas 18 and 19 are presented. Although a great number of students have dealt with the corticopontine projection from the visual cortex, only few have attempted to decide whether all or only certain parts of the visual cortex contribute. Among authors looking specifically for it, there seems to be agreement that area 18 gives off a substantial projection, terminating rostrolaterally and rostroventrally in the pontine nuclei. This is so in the monkey14,3z, Brain Research, 39 (1972) 319-335

320

P. BRODAL

the prosimian Ga[ago 1;~, the cat is, the rat 31 and the rabbit 21 (see, however, Kusama et al. 27 and Gerebtzoff'~0). Area 19 appears to project onto the pontine nuclei in the monkey 14, but whether this is so in the cat is not known. Furthermore, the exact site of termination of the corticopontine fibers from areas 18 and 19 has not been determined, and it is unknown whether a topical localization exists within the pontine projections from areas 18 and 19. The aims of the present study have been to obtain answers to the following questions. (1) Is there a pontine projection from area 19 in the cat'? (2) Do areas 18 (and 19?) project onto the total pontine projection area of the visual cortex or only certain parts of it? (3) Do all parts of area 18 (and 19?) project onto the pontine nuclei? (4) Can a topical localization be demonstrated within the pontine projection from area 18 (and 19?)? MATERIAL A N D M E T H O D S

A full description of the methods employed is given in a preceding paper dealing with the pontine projection from area 1710. Lesions of areas 18 and 19 were made in 17 cats, and of non-visual regions adjoining area 19 in 5. In addition, a few cases with lesions of area 17, presented previously 1°, were used for comparison. Since the pontine projection from the visual cortex is almost entirely ipsilateraP 0, bilateral lesions were made in most of the animals. For the identification of the particular cortical area involved by the lesion, the criteria given by Otsuka and Hassler a3 were used. A check on the exact location of the lesions and on the possible presence of accidental damage to other parts of the visual cortex was obtained by studying the ensuing degeneration in the superior colliculus since this is known to receive a strong point-to-point projection from all parts of the visual cortex 18. The animals were killed after 4-18 days, in most instances after less than 7 days. Frozen sections from the brain stem were impregnated according to the procedure I of Fink and Heimer 17 and in a few instances also according to the Nauta method 30. The mesencephalon with the superior colliculi was cut transversally, the pons and medulla oblongata horizontally or transversally (in most instances horizontally). The sections from the pontine nuclei were drawn in an electronic pantograph, and the degeneration observed was entered as dots. Three-dimensional transparent reconstructions of the pontine nuclei showing the arrangement of the degeneration were always made (see Figs. 4 and 7). RESULTS

Like the pontine terminal areas projected upon by area 17, those supplied from areas 18 and 19 do not coincide with particular nuclei outlined on a cytoarchitectonic basis by Brodal and JansenL In the present study the various subdivisions of the Brain Research, 39 (1972) 319-335

CORTICOPONTINE PROJECTION FROM AREAS 18 AND 19

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Fig. 1. A, Photomicrograph of a small well-restricted area of degeneration in the pontine nuclei 15 days after a small lesion of area 18 in cat C.Co.L.152 (cf. Fig. 2). Fink-Heimer method, x 230. B, Photomicrograph showing relatively sparse degeneration in the pontine nuclei 5 days after a small lesion most probably limited to area 19 in cat C.Co.L.147L (cf. Fig. 5). Fink-Heimer method, x 280.

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Fig. 2. Diagrammatic representation of 10 lesions of area 18, referred to in the text. The lesions are indicated in black in the drawings of the brains. In one of the brains the outlines of area 18 are indicated (cfi Fig. 3C). Abbreviations used in all figures: Br.p., brachium pontis; G.I., lateral gyrus; G.pl., postlateral gyrus; G.sp., splenial gyrus; G.ss., suprasylvian gyrus; L.m., medial lemniscus; N.d., dorsolateral nucleus; N.I., lateral nucleus; N.p., peduncular nucleus; N.pm., paramedian nucleus; N.y., ventral nucleus; Ped., cerebral peduncle and its continuation through the pontine nuclei; S.I., lateral sulcus; S.pl., postlateral sulcus; S.sp., splenial sulcus; S.ss., suprasylvian sulcus.

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pontine nuclei will therefore be referred to only to facilitate the description. In Fig. 3A the borders between the nuclei are indicated as appearing in horizontal sections. In the present study the terminalfieMs of the corticopontine fibers from areas 18 and 19 were determined. The criteria for the identification of a terminal field in the pontine nuclei have been given elsewhere 6. The caliber of the degenerated fibers and fragments present within the pontine nuclei appears to be the same regardless of whether the lesion is situated in area 171°, 18 or 19 (Fig. IA and B). This conclusion is based mainly upon the study of cases with bilateral lesions of different areas (Figs. 2, 4 and 6). In the following the main features of the pontine projection from areas 18 and 19 will be described and illustrated. In all cats the degeneration was found within sharply delimited bands in the rostral half of the pons.

(I) The projection from area 18 (1) Origin within area 18 of fibers to the pontine nuclei. Since the caudal part of area 18 is largely buried in the postlateral sulcus (see Fig. 3C), this part cannot be selectively destroyed. Thus the results presented concern only the rostral part of area 18 (the part related to the lower visual field3,Zs,39). In 8 cases with small lesions, together covering most of area 18 not buried in sulci, degeneration is present in the pontine nuclei (cats C.Co.L. 75R, 9OR, 133, 139R, 141R, 146R, 146L, 152 and 159R, killed after 5, 4, 13, 7, 6, 5, 15 and 5 days, Figs. 2 and 4). In cats C.Co.L. 90R, 139R, 141R, 146R the lesions do not extend beneath the cortex, in the others there is only slight involvement of the white matter. When the amount of degeneration in the pontine nuclei and the size of the lesions of area 18 in these cases are compared, it appears that all parts of area 18 investigated project about equally heavily onto the pontine nuclei. However, since no cases with bilateral, equally large lesions within different parts of area 18 have been obtained, smaller differences may have escaped recognition. (2) Sites of termination of the corticopontine fibers.from area 18. Since only the rostral parts of area 18 can be destroyed without considerable damage to neighboring areas (see above and Fig. 3C), the total pontine projection area of area 18 has not been determined. However, in cat C.Co.L.134 (killed after 12 days, Fig. 3A) the lesion of area 18 is as large as possible without encroachment upon neighboring areas. It extends slightly beneath the cortex, but most probably does not involve fibers from area 17. It does not extend into area 19 rostrally (compare with Fig. 3C). In the ipsilateral pontine nuclei (Fig. 3A) the degeneration is distributed within sharply delimited, mainly transverse bands in the rostral half. The bands curve along the ventral aspect of the peduncle*. In 10 other experiments with lesions of area 18 (see above and Figs. 2 and 4), all with lesions limited to the cortical gray matter or with only slight involvement of * The term 'peduncle' is here used for the longitudinally running fiber bundles of the corticospinal and corticobulbar tracts both in the mesencephalon (as usual) and in the pons.

Brain Research, 39 (1972) 319-335

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Fig. 4. Comparison of the pontine regions supplied from parts of areas 17 and 18, representing corresponding parts of the visual field in cat C.Co.L.139. Above, the lesions (black) are indicated in drawings of the brain. The lesion on the left side is situated within the rostral part of area 17, on the right side within the rostral part of area 18 (cf. Fig. 3C). Note that the lesions are of the same size. Below is shown a photograph of a three-dimensional reconstruction based on the series of horizontal sections through the pons. The model is photographed from the ventral aspect. The ventralmost sections have been omitted since no degeneration was found in these. Note that the degeneration is distributed symmetrically and in equal amounts on the two sides. the white matter, the degeneration in the pontine nuclei is confined to the area shown in Fig. 3A, even if minor differences exist. F o r comparison Fig. 3B shows some representative horizontal sections from cat C.Co.L.70 with a large lesion o f the visual cortex affecting areas 17, 18 and 19 (described in detail elsewhere1°). Only certain parts of the total pontine projection area o f the visual cortex receive afferents from the rostral part of area 18 (Fig. 3A). Thus, degeneration extends further medially and rostrally after the total lesion than after the lesion of area 18. The regions not projected u p o n by the rostral part o f area 18 are supplied from caudal and rostromedial parts o f area 171°. Since at least most o f the pontine area projected u p o n by the rostral part of area 171° also receives afferents f r o m the rostral part of area 18, it seems likely that corresponding parts of areas 17 and 18 supply identical pontine areas. This question was further investigated by use o f small bilateral lesions within parts of areas 17 and 18 corresponding with regard to the part of the visual field represented. In cat C.Co.L.139 (killed after 7 days, Fig. 4) the lesion on the right side is located within the rostral part of area 18, close to the border towards area 17. (The vertical meridian o f the visual field coincides with this border3,2~,2s,~a.) The lesion on the left side is situated at the same rostrocaudal level, but within area 17 close to the border towards area 18. Both lesions are limited to the cortical gray matter, and are o f equal size. In the pontine nuclei the degeneration is nearly symmetrically distributed on the two sides (Fig. 4) and situated within the total projection area of area 18 shown in Fig. 3A. The a m o u n t o f degeneration is also approximately equal on the two sides. Closely corresponding observations are

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CORTICOPONTINE PROJECTION FROM AREAS 18 AND 19

325

made in another animal with similar lesions (cat C.Co.L.141, killed after 6 days, Fig. 2). Here, too, the lesions are limited to the cortical gray matter. Even after small, bilateral lesions of different parts of the rostral part of area 18, no conclusive evidence of a topical organization of the pontine projection from this area has been found. In cat C.Co.L.146 (killed after 5 days, brain stem cut horizontally, Fig. 2) the small lesion on the right side is situated within the rostralmost part of area 18. The lesion on the left side is located more caudally within area 18 and is smaller than the lesion on the right. It does not encroach upon area 19 laterally or area 17 medially. Neither lesion extends beneath the cortical gray matter. The location of the lesions is verified by the findings in the superior colliculi where the wellrestricted degeneration in the superficial layers is located more rostrally on the left side than on the right, in harmony with the results of Garey et al. is. In the pontine nuclei the degeneration is distributed as in other cats with lesions of area 18 (Figs. 3A and 4), and no clear differences can be found when the two sides are compared. An entirely corresponding distribution of the degeneration both in the pontine nuclei and the superior colliculi is found in another animal with bilateral lesions similar to those described above in cat C.Co.L.146 (cat C.Co.L. 159, killed after 5 days, brain stem cut horizontally, Fig. 2), even when the caudally situated lesion (left side) in this case affects mainly area 17 and only slightly area 18. Since area 18 is narrow mediolaterally (Fig. 3C), existing differences between medial and lateral parts concerning their pontine projection would have to be marked in order to be discovered with the present method. No convincing difference has been found when cases mainly involving medial parts of area 18 (cats C.Co.L.139R,141R, 152, Figs. 2 and 4) are compared with cases involving the most lateral parts (cats C.Co.L.9OR, 140R and 146L, Fig. 2). Minor differences found are inconsistent and, therefore, presumably represent only individual variations. In summary, the rostral part of area 18 projects onto certain parts only of the total pontine projection area of the visual cortex (Fig. 3). The regions supplied from the rostral part of area 18 are also projected upon by the rostral part of area 171°. At least certain corresponding parts of areas 17 and 18 project onto identical pontine regions (Fig. 4), and about equally heavily. Although a topical localization within the pontine projection from area 18 could not be definitely proved, there is suggestive evidence that some degree of localization is, nevertheless, present (see Discussion).

(II) The projection from area 19 (1) Origin within area 19 of corticopontine fibers. Since area 19 is very long and narrow (Fig. 3C) it is virtually impossible to make total lesions of it without concomitant damage to other areas. Furthermore, it is extremely difficult to decide whether a lesion is limited to area 19 or in addition involves adjoining areas. Consequently, the results concerning the pontine proiection from area 19 are not as clearcut as those obtained with regard to areas 1710 and 18. The presence of a pontine projection from the parts of area 19 situated on the convexity of the cerebral hemisphere is suggested by the findings in a few cases with Brain Research, 39 (1972) 319-335

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Fig. 5. The distribution of the degeneration in the pontine nuclei after a lesion most probably limited to area 19 in cat C.Co.L.147L. In the horizontal sections through the pons the main amount of the degeneration is located within a transversally oriented band in the rostralmost part of the pontine nuclei (compare with Figs. 3 and 7). Ventrally (sections 5-7) and dorsomedially (section 17) the degeneration extends more caudally. For abbreviations see legend to Fig. 2.

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Fig. 6. Diagrammatic representation of 7 lesions involving area 19, referred to in the text. In some brains the border between areas 17 and 19 is indicated by a broken line. For abbreviations see legend to Fig. 2. small and relatively pure lesions of area 19 (cats C.Co.L.75L, C.Co.L.144R, 144L, 147L and 162L, killed after 5, 6, 5 a n d 5 days, respectively, Figs. 5 and 6). In cats C.Co.L.75L, 144R a n d L, the lesions are limited to the cortical gray matter, but in cats C.Co.L. 147L a n d 162L they extend slightly into the white matter. All lesions are situated on the medial b a n k of the suprasylvian gyrus. I n all cases moderate degeneration is present within the ipsilateral p o n t i n e nuclei. Since the lesions involve very little (if any) cortex outside area 19, it is unlikely that the degeneration seen is due only to i n v o l v e m e n t of cortex outside area 19. This is particularly so in cats C.Co.L. 144 and 162L where the lesions are very small. The experiments m e n t i o n e d above indicate that certain parts of area 19 have a

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stronger pontine projection than others. Thus in cat C.Co.L.144 the lesion on the left side, situated in the middle part of area 19 (Fig. 6), on histological examination is seen to be considerably larger than that on the right side, located more rostrally. This is verified by the presence of a larger amount of degeneration in the left superior colliculus than in the right. However, in the pontine nuclei the degeneration is more marked on the right side than on the left. In agreement with this it appears that in all cases with lesions of the middle part of area 19 on the convexity the degeneration found in the pontine nuclei is somewhat less heavy than would be expected from the size of the lesions when compared with lesions of similar size within area 18 (eats C.Co.L.75L, 147L and 162L, Figs. 5 and 6). (2) Sites of termination of the eortieopontine fibers from area 19. In all the cases mentioned above with relatively pure lesions of area 19, the degeneration is located mainly within a transverse band in the rostralmost part of the lateral, the ventral and paramedian nuclei (eats C.Co.L.75L, 144L, 144R, 147L and 162L, Fig. 6). In some cases with lesions of the caudal part of area 17, extending considerably into area 19, some degeneration is located within the same pontine region as after more rostrally situated lesions of area 19 (eats C.Co.L.135L, 156R and 156L, Fig. 6). This distribution of the degeneration is not seen following lesions restricted to area 17 in its caudal part (cats C.Co.L.145L, 143L and 149, not illustrated, described elsewhere1°). In cat C.Co.L. 135L the main part of the lesion is presumably located within area 19, and area 17 is involved only to a lesser degree. However, the main amount of the degeneration is distributed as after lesions restricted to area 17. This may be due to area 17 extending farther caudally in this case than usual, or it may mean that this part of area 19 projects both to its 'own' pontine region and onto the projection regions of area 17. It may also be explained by a much stronger projection from area 17 than from area 19. Since no pure lesion of this part of area 19 has been obtained, no decisive choice can be made between these possibilities. None of the lesions of area 18 (Figs. 2, 3 and 4) involves area 19 to such an extent that any degeneration due to damage of the latter may be expected. In agreement with this no degeneration is found within the area projected upon by area 19 in any of the cases with lesions of area 18. In cases with lesions affeeting non-visual eortieal regions adjoining area 19, the pontine degeneration is located within the same territory as after lesions of area 19, but the degeneration is more extensive (compare Figs. 5 and 7). The degeneration occurs within a band located ventromedially with a longitudinal orientation which rostrally is divided into two parts, one bending medially and one laterally (Fig. 7). This distribution of the degeneration is present in two cases with lesions of the middle suprasylvian gyrus (eats C.Co.L.83L and 140L, killed after 5 and 7 days, respectively, Fig. 7), in two cases with lesions of area 72z in the rostral part of the suprasylvian gyrus (eats C.Co.L.147R and 162R, both killed after 5 days) and in one case with a lesion of the cingulate gyrus (cat B.St.L. 181, killed after 18 days). Even if it cannot be decided whether area 19 contributes to the pontine degeneration present in these cases, it is clear that area 19 need not be involved to produce this pattern of degeneration, since in cat C.Co.L.83L the lesion is limited to the cortical gray matter and does

Brain Research, 39 (1972) 319-335

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Fig. 7. Different cortical regions adjoining area 19 (cf. Fig. 3C) projecting in a uniform manner onto the pontine nuclei. Above are represented the lesions (black) in 7 different cats. Two of the lesions (C.Co.L.160R and 148) are situated within the rostromedial part of area 17 (cf. Fig. 3C) and have been described previously 1°. Below are shown photographs of a three-dimensional reconstruction of the pons of cat B.St.L.181. The pons is seen from the ventral aspect. For the sake of clarity the ventral and dorsal parts of the pontine nuclei have been reconstructed separately. All other lesions shown above produced a pattern of degeneration corresponding to that in cat B.St.L.181. Note that the pattern of degeneration is similar to that seen after a lesion most probably limited to area 19 (cf. Fig. 5). Below to the right is shown a free-hand three-dimensional illustration of the shape of the pontine terminal area seen in cat B.St.L.181.

n o t extend into area 19. I n the other animals the lesions destroy a little of the white matter, and some fibers from area 19 may possibly have been interrupted, even if direct i n v o l v e m e n t of area 19 is f o u n d only in cats C . C o . L 147R and 162R. However, the a m o u n t of degeneration in the p o n t i n e nuclei is too large to be caused by a rather small lesion of area 19. I n cat C.Co.L.147R the findings i n the superior colliculus s u p p o r t the conclusion that the lesion is situated mainly within the anterior suprasylvian gyrus (area 7), since degeneration is confined to the deeper layers. I n all cases with lesions of the visual cortex a n d the middle suprasylvian gyrus, degeneration is f o u n d in the superficial layers (Garey et al. 18, a n d personal observations). I n cat C.Co.L.162R (Fig. 7) the lesion extends into area 18 in its rostral part, and some degeneration in this case is distributed as in other cases with lesions of area 18 (Figs. 3 a n d 4). The present material is n o t well suited to reveal a topical localization within the p o n t i n e projection from area 19. First of all, large parts of area 19 have n o t been

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18 AND

19

329

accessible for investigation (especially the part located on the medial surface, see Fig. 3C), and only one case with relatively pure bilateral lesions at different levels within area 19 has been obtained (cat C.Co.L. 144, Fig. 6). In this case the distribution of the degeneration is practically symmetrical in the pontine nuclei on the two sides. However, cases with the lesions placed farther apart than here are probably necessary to reveal small differences (see Discussion). In summary, there is fairly good evidence that area 19 projects onto the pontine nuclei. The degenerated fibers after lesions assumed to be restricted to area 19 terminate more rostrally within the pontine nuclei than do those from area 18 (compare Figs. 3A and 5). This area falls within the territory supplied from certain regions located outside area 19 (the suprasylvian and the cingulate gyri). DISCUSSION

Unfortunately, it has not been possible to obtain definite answers to all questions raised in the Introduction. This is due to the technical difficulties involved in producing isolated lesions of all parts of areas 18 and 19. Nevertheless, some interesting new information has been obtained. The pontine projections from areas 18 and (most likely) 19 are arranged mainly in the same manner as the projection from area 171°. The fibers terminate within sharply delimited bands with a mainly transverse orientation in the rostral half of the pons. There is some degree of topical localization within these bands, at least with regard to the projection from area 171°. Although largely similar, there are certain differences between the projections from areas 17, 18 and (most likely) 19. The terminal areas of the pontine projections from other parts of the cerebral cortex so far studied by the present author 6-9 are also arranged as bands, but with a mainly longitudinal orientation and located within other parts of the pontine nuclei than the bands supplied from the visual cortex.

(1) Identification of the lesions An exact identification of the lesions is of the utmost importance for the interpretation of the results concerning efferent connections of the cerebral cortex, and in the visual cortex this problem is of particular significance owing to its anatomical organization. The methods employed in the present study for making the cortical lesions and for their identification are the same as those used in the preceding study of the pontine projection from area 171° and will not be discussed here. Only certain points relevant to areas 18 and 19 need some comment. For the identification of these areas the criteria and the map of Otsuka and Hassler 33 have been used. The area 18 can be recognized in most sections by the presence of its well-developed layer III. However, the borders of area 18 towards areas 17 and 19 are not sharp. This makes it difficult to decide whether a lesion located close to the border encroaches somewhat upon the neighboring area. However, most of the lesions of area 18 used in the present study have been placed at some distance

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from the border, making possible the identification of a remaining small zone of normal area 18 on all sides of the lesion. Only certain parts of area 18 have been studied in the present paper. The rostral part (related to the lower visual field) is easily accessible, whereas the caudal part is narrow and mainly buried in the postlateral sulcus (Fig. 3C), and therefore very difficult to destroy in isolation. It is especially difficult to obtain satisfactory lesions restricted to area 19, since the area is narrow and mainly buried in sulci. On the medial surface of the hemisphere, area 19 is virtually inaccessible without the infliction of considerable damage to other areas (Fig. 3C). For these reasons this part of area 19 could not be studied. Furthermore, the lesions have to be of a certain size in order to produce detectable degeneration in the pontine nuclei. Finally the border between area 19 and the cortical areas of the suprasylvian gyrus is more difficult to identify than the borders between areas 17 and 18 and between 18 and 19. Therefore, none of the lesions used in the present study can be said to be definitely limited to area 19, even if the involvement of other areas is certainly very small in several of the lesions (Fig. 6). Most of the lesions used in the present study are limited to the cortical gray matter. In the remaining lesions there is only very slight involvement of the underlying white matter.

(2) The pontine projection.from area 18 For reasons given above, the results presented here concern only the rostral part of area 18. All of this appears to project onto the pontine nuclei, a finding in general agreement with those made by most other workers (for references see Introduction). No clear difference in the intensity of projection from different regions within the rostral part of area 18 has been found. As concerns area 171°, and probably also area 19 (see below), the middle parts (related to the central visual field 3,25) project less heavily onto the pontine nuclei than do rostral parts. Whether a corresponding difference exists within the projection from area 18 cannot be decided from the present material, since no lesion has been obtained restricted to the part of area 18 corresponding (with regard to the representation of the visual field) to the parts of areas 17 and 19 projecting relatively sparsely onto the pontine nuclei. The pontine projection from area 18 terminates within the same pontine regions as does the projection from area 17 l°. The two projections are about equally heavy, as judged from cases with lesions of area 17 on one side of the brain and of area 18 on the other (Figs. 2 and 4). Although no clear topical localization has been found within the pontine projection from the rostral part of area 18, it appears likely that some degree of localization is, nevertheless, present. This emerges from the observation that the rostral part of area 18 projects onto the pontine region supplied from the rostral part of area 17, but not onto the region receiving afferents from the caudal part of area 17. If the caudal part of area 18 projects onto the pontine nuclei, as is likely, the fibers probably end in the same pontine area as do those from the caudal part of area 17. Parts of areas 17 and 18 representing identical parts of the visual field project

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CORTICOPONTINE PROJECTION FROM AREAS 18 AND 19

331

onto identical pontine regions (Fig. 4). However, within the rostral parts, at least, this holds true only for the regions situated close to the border between areas 17 and 18 (representation of the vertical meridiana,25,2s,39). The rostromedial part of area 17 projects differently from the rest of area 171°, but within area 18 no such difference has been found, even if lesions (Fig. 2) have been placed within rostrolateral parts of area 18, corresponding (with regard to the representation of the visual field) to rostromedial parts of area 173. Areas 17 and 18 project onto identical parts of the superior colliculi is. Further, as a rule the pontine projections of these two areas are identical, as discussed above. However, the projection onto the superior colliculi shows a sharp point-to-point organization, whereas the pontine projection has a more complicated pattern (Fig. 3). Each point within the visual cortex projects onto several sharply delimited tortuous bands within the pontine nuclei, but the topical localization is apparently not sharp. However, the presence of topical localization is more difficult to demonstrate within this type of projection than when there is a point-to-point relation (see ref. 10 for some comments upon this point).

(3) The pontine projection from area 19 As mentioned above, only the parts of area 19 situated on the convexity have been studied (see Figs. 3C and 6). All parts studied appear to give off fibers to the pontine nuclei, although the material does not permit final conclusions on this point (see below). Middle parts of area 19 (representing the central visual fielda, 25) seem to give off less fibers than more rostral (peripheral) parts. A quantitative difference of this kind between central and peripheral parts is present within area 1710 concerning its pontine projection, but not concerning other efferent connections of the visual cortex (see for example refs.14,18,3s,41). The fibers from area 19 appear to terminate within other pontine regions than do those from areas 17 and 18 (compare Figs. 3 and 5), except for the rostromedial part of area 17, which projects onto a pontine region that appears to be supplied from area 19 as welP °. A corresponding difference between areas 17 and 18 on one hand and area 19 on the other is present within their thalamic connections. Thus, of the 3 visual areas only area 19 receives afferents from the medial interlaminar nucleus of the lateral geniculate body19, 4~, and projects back onto the same nucleus18, 24. The present study shows that most probably area 19 and certain regions surrounding it (the suprasylvian and the cingulate gyri*) project onto virtually identical pontine areas (Fig. 7). Also the thalamic connections of area 19 and the suprasylvian gyrus appear to be similar, since most likely both are connected with the medial interlaminar nucleusXg,24,42. However, the cingulate and the suprasylvian gyri are dissimilar with regard to their thalamic connections16, 22. * A pontine projection from the cingulate gyrus has been demonstrated previously in the rabbit and the rat1,15,16.

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Although it appears likely from the present experiments (see Results) that area 19 projects onto the pontine nuclei, it cannot be entirely excluded that the degeneration seen in the pontine nuclei after lesions of area 19 {Figs. 5 and 6) is due to inadvertent damage to, for instance, the suprasylvian gyrus, since the distribution of the degeneration is closely similar in both (Fig. 7). The reverse possibility, that the degeneration observed after lesions of the suprasylvian and the cingulate gyri is due to damage to area 19 is extremely unlikely, since the amount of degeneration seen in all these cases is much too large to be caused by a small lesion of area 19.

(4) Relations between the visual cortex and the cerebellum It is known from physiological studies that electrical stimulation of the visual cortex evokes potentials in certain parts of the cerebellum in the cat a~ and monkeyZL These impulses may be transmitted along two main routes: the corticopontocerebellar pathway, of which the first link has been studied here, and the corticocolliculopontocerebellar pathway*. On several points the anatomical data concerning the various links in these pathways are difficult to reconcile with the physiological observations on the relations between the visual cortex and the cerebellum. When the present results are evaluated in conjunction with those of Brodal and Jansen 5 concerning the pontocerebellar projection in the cat it appears that the pontine fibers from the visual cortex terminate within pontine regions projecting onto the vermis as well as within regions supplying the cerebellar hemispheres. However, physiologically only the folium, the tuber vermis and the vermal part of the lobulus simplex appear to be responsive to stimulation of the visual cortex 26,36,37. A possible explanation of the discrepancy between the anatomical and the physiological data may be that quantitatively the connections between the visual cortex and the vermis are the most important, and that the use of anesthetics blocks a less-marked influence on the hemispheres. However, it appears from the present and preceding 1° studies, as well as from others, that the pontine projection from the visual cortex terminates mainly within pontine regions which appear to project onto the cerebellar hemispheres. While the pontine projection from the superior colliculus in the cat is usually said to end in pontine regions which project onto the vermis (the dorsolateral nucleus 2,35) it appears from recent studies that the colliculus in addition sends fibers to pontine regions projecting onto the cerebellar hemispheres in the cat 12 and the opossum z9,34. Thus, even if the connections between the visual cortex and the vermis (corticopontine and corticotectopontine) should turn out to be quantitatively most important, those with the cerebellar hemispheres should not be overlooked. Another point of controversy concerns the parts of the visual cortex from which cerebellar potentials may be evoked. In the cat, such potentials are evoked after stimulation of visual area I (area 17) as well as visual area 1I (area 18), whereas in the * Among the other brain stem nuclei projecting onto the cerebellum the most important ones, the lateral reticular nucleus, the tegmental pontine reticular nucleus and the inferior olive do not receive fibers from the visual cortex 4,n,4°.

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19

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monkey, only stimulation of area 17 is effective. Anatomically, area 18 has a strong pontine projection both in the cat and the monkey (see Introduction). A topical localization has been demonstrated within the pontine projection from area 17 in the cat 10. In the light of this it appears likely that a corresponding localization is present within the pontocerebellar projection, thus permitting a topically localized relationship between the visual cortex and the cerebellum. Physiologically Snider and Eldred 36 were unable to find that different parts of the visual cortex influence different parts of the cerebellum. This may, however, be related to the difficulties with which cerebellar potentials are apparently evoked in the cerebellum from the visual cortex in the cat and monkey. Thus Snider and Eldred 37 state '... of all the systems activated the visual requires the highest voltage and appears to be the most capricious'. However, this, too, is hard to reconcile with the anatomical data, since the corticopontine projection from the visual cortex is quantitatively much more important than that from, for instance, the auditory cortex (personal observations, cat, and Nyby and Jansen 32, monkey), whence cerebellar potentials were more easily evokeda6, 37. In order to achieve a better understanding of the relations between the visual cortex and the cerebellum, a more detailed knowledge of the pathways involved is needed, especially of the organization of the pontocerebellar projection. Furthermore, the tectopontine projection deserves renewed studies with special reference to the possible existence of a topical organization and its sites of termination in relation to those of the corticopontine afferents from the visual cortex. SUMMARY

Small lesions (in most cases bilateral) were made of the cerebral cortical areas 18 and 19 in adult cats, and the ensuing degeneration in the pontine nuclei was studied with the silver impregnation methods of Nauta and of Fink and Heimer. The lesions were made by transdural thermocoagulation. Since large parts of areas 18 and 19 are buried in sulci, isolated lesions of these parts have not been achieved. The main results are as follows. (1) All parts of area 18 studied (rostral part, related to the lower visual field) project onto the pontine nuclei. (2) The fibers from area 18 terminate within mainly transverse bands in the rostral half of the pontine nuclei in the pontine regions that receive afferents from area 17. At least certain corresponding parts of areas 17 and 18 project onto identical pontine areas, and the projections from the two areas are about equally heavy. (3) There is suggestive, but not conclusive, evidence for a topical localization within the pontine projection from area 18. (4) It appears likely that all parts of area 19 situated on the convexity of the hemisphere project onto the pontine nuclei. Middle parts of area 19 (representing the central visual field) seem to project less heavily than more rostral parts. The fibers terminate mainly within a transverse band in the rostralmost part of the pontine nuclei. t5~ The projections from areas 19 and 18 terminate in different parts of the Brain Research, 39 (1972) 319-335

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p o n t i n e nuclei. N o topical l o c a l i z a t i o n has been f o u n d within the p o n t i n e p r o j e c t i o n f r o m a r e a 19, but the m a t e r i a l is i n a d e q u a t e to resolve this q u e s t i o n . (6) A z o n e o f c o r t e x s u r r o u n d i n g a r e a 19 (the s u p r a s y l v i a n and the c i n g u l a t e gyri) p r o j e c t s o n t o the s a m e ( b u t s o m e w h a t m o r e extensive) p o n t i n e r e g i o n as d o e s a r e a 19. (7) T h e results o f the p r e s e n t and the p r e c e d i n g studies 10 are discussed with r e g a r d to p h y s i o l o g i c a l d a t a o n the r e l a t i o n s b e t w e e n the visual c o r t e x and the cerebellum.

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