The connections of area PG, 7a, with cortex in the parietal, occipital and temporal lobes of the monkey

Brain Research, 532 (1990) 249-264

249

Elsevier BRES 16014

The connections of area PG, 7a, with cortex in the parietal, occipital and temporal lobes of the monkey J.W. Neal, R.C.A. Pearson and T.P.S. Powell Department of Human Anatomy, Oxford (U.K.) (Accepted 15 May 1990)

Key words: Cortex; Area PG, 7a; Cortico-cortical connections; Monkey

The cortico-cortical connections of area PG, 7a, in the parietal, occipital and temporal lobes have been studied after injections of HRP in this area and in certain of the areas connected with it. After such injections in PG there are labelled cells in architectonic areas OA and PE (visual area PO), the cingulate and retrosplenial areas situated medial to PG; posteriorly labelled cells are present in OA, visual areas MST, MT, V2, V3, V4 and in the walls and floor of the lower part of the superior temporal sulcus. Injections in PE and V4 show that these connections are reciprocal. Small injections in PG result in cell labelling in different parts of the areas connected to PG, suggesting that the connections are well organized and that there may be an ordered representation of the visual field in PG. In the lower wall of the lower part of the superior temporal sulcus there is overlap of the two visual pathways in the cortex, that to the temporal lobe with that to the parietal lobe; and in a restricted part of this sulcus there is convergence and overlap of the sequences of cortico-cortical connections related to the visual, somatic and auditory sensory systems. There may be certain common principles in the sequences of cortical connections to the parietal and temporal lobes from the primary visual and somatic sensory areas; in both there are well organized hierarchical and parallel pathways, and both are related to the superior temporal sulcus and to the cingulate cortex. tional visual areas, and to d e t e r m i n e w h e t h e r t h e r e is any

INTRODUCTION

o r g a n i z a t i o n in t h e s e c o n n e c t i o n s . F r o m t h e i r physiological studies on a r e a 7 of the

P r e l i m i n a r y c o m m u n i c a t i o n s o f certain of t h e o b s e r -

p a r i e t a l l o b e of the m o n k e y H y v a r i n e n and M o u n t c a s t l e

vations h a v e b e e n p u b l i s h e d 39-41, a n d in t h e m e a n t i m e

and t h e i r c o l l e a g u e s c o n c l u d e d that the activity of t h e n e u r o n s in this a r e a was p r e d o m i n a n t l y r e l a t e d to visual

the results of a n o t h e r p e a r e d 9.

similar i n v e s t i g a t i o n h a v e apo

and m a n u a l e x p l o r a t o r y b e h a v i o u r in the a n i m a l ' s closely r e l a t e d e x t r a p e r s o n a l space, and that the activity was i n f l u e n c e d by the d e g r e e of interest and a t t e n t i o n that the stimuli a r o u s e d in t h e a n i m a l 25'26"36'37. T h e s e studies s t i m u l a t e d a n u m b e r o f e x p e r i m e n t a l a n a t o m i c a l investigations which h a v e s h o w n that a r e a 7 has w i d e s p r e a d and r e c i p r o c a l cortico-cortical c o n n e c t i o n s with m a n y areas in b o t h the ipsi- and c o n t r a l a t e r a l h e m i s p h e r e s 4' 17,23,34,44,54,55-58. A t t h e t i m e of t h e s e a n a t o m i c a l studies, h o w e v e r , it was not k n o w n that the two a r c h i t e c t o n i c subdivisions of a r e a 7 of B r o d m a n n 8, d e s c r i b e d by the Vogts 66 and

by

Bonin

and

B a i l e y 7, differ

in their

c o r t i c o - c o r t i c a l c o n n e c t i o n s , n o r h a d m a n y of the functional visual areas in the p r e s t r i a t e c o r t e x b e e n delim i t e d 15. It has since b e e n s h o w n that a r e a P G , 7a, is r e l a t e d to the visual sensory system 9"4° and PF, 7b, to the s o m a t i c system 9"39, and that the two subdivisions are n o t i n t e r c o n n e c t e d . In the p r e s e n t study an a t t e m p t has b e e n m a d e to d e f i n e the cortico-cortical c o n n e c t i o n s of a r e a P G , 7a, in t e r m s o f the a r c h i t e c t o n i c and m a j o r func-

MATERIALS AND METHODS Two distinct types of material have been used in this study, and all of it was from the macaque (rhesus) monkey. For the study of the cyto-architecture of the cortex and for making the planar reconstructions several series of sections of a number of normal brains were available; series of paraffin- or celloidin-embedded sections cut in either the sagittal, coronal or horizontal plane, and stained with thionin, were used. The planar reconstructions were made in the same way as described in detail in a previous study 59. The experimental material was the same as that which has been used in earlier studies. Injections of various amounts of 15% HRP or W.G.A.-HRP were made into the cortex of area PG in 10 macaque monkeys, into the visual functional area V4 on the prelunate gyrus in 2 monkeys and into areas PE and OA on the medial surface of the hemisphere in a further monkey. All the experiments were done with the monkeys under general anaesthesia and with full aseptic precautions. The injections were made iontophoretically by passing current of between 2 and 5 k~A for 10-20 min in pulses of 7 s with 7-s intervals, and either a single injection was made or 2 or 3 at approximately 1 mm, apart; the pipette was left in the cortex for 20 min after the injection. The animals were allowed to survive for 24-72 h and were then deeply anaesthetised and perfused through the heart with White's saline

Correspondence: T.ES. Powell, Department of Human Anatomy, Oxford OX1 3QX, U.K. 0006-8993/90/$03.50 © 1990 Elsevier Science Publishers B.V. (Biomedical Division)

250 and a mixture of 2% paraformaldehyde and 1% glutaraldehyde for the HRP injections or 1.25% paraformaldehyde and 1% glutaraldehyde for the WGA-HRP injections. The brains were removed, photographed and cut into blocks before being immersed in 30% phosphate-buffered sucrose at 4 °C until they sank. Frozen sections were cut in either the sagittal or coronal plane at 40 ¢tm and a 1:20 series processed with the dianisidine and nitroprusside (DAS) method 12 and with the tetramethylbenzidine (TMB) method 33. The site of the injection and the distribution of the labelled cells were transferred from individual sections of the different brains to planar reconstructions of the parietotemporal cortex. Series of sections from several of these brains were stained with the Gallyas method~-2 for the study of the myeloarchitecture. RESULTS O u r own study of the cytoarchitecture of the cortex of the superior and inferior parietal lobules and of the adjoining medial surface of the hemisphere has confirmed the descriptions and the limits of the areas given by Bonin and Bailey 7. For the present experimental investigation the designation P G is used for the medial part of the inferior parietal lobule, and PE for the adjoining area on the medial surface and the anterior wall of the medial part of the intraparietal sulcus. The validity of separating PE from P E m on cytoarchitectonic features is confirmed by finding that the limits of P E m coincide closely with the extent of the projection of the primary somatic sensory area and what was described as area 5 in an earlier study 45, and also by the finding in the present experiments that area PE is reciprocally connected with a r e a PG. A r e a PE is broadly equivalent to Pm of C a v a d a and G o i d m a n - R a k i c 9 and to P G m of Pandya and Seltzer 44. The many small subdivisions within P G described by o t h e r authors have not been considered here. The extent of P G as described by Bonin and Bailey and followed here includes the functional visual area t e r m e d the medial superior temporal area (MST) 15. The structure of the cortex in the walls of the lower parts of the superior t e m p o r a l sulcus, lateral to P G , has not been studied, but the relationship of the distribution of the cell labelling to the architectonic maps of other workers has already been discussed 41. The planar reconstruction of the superior temporal sulcus and the adjoining region of the lateral surface of the hemisphere has been made from sagittal sections, and that of the medial and lateral surfaces of the posterior parietal and occipital regions from coronal sections. The latter have been used because labelled cells were found over a p p r o x i m a t e l y the same extent on the medial and lateral surfaces of the hemisphere and because the cortex on both these surfaces is present on coronal sections. T h e r e are great differences in the curvature and in the depth of the sulci on the medial and lateral surfaces, and these inevitably m a k e for some degree of inaccuracy; reconstructions m a d e from sections cut in different planes

were, for this reason, slightly different, but the distortion is p r o b a b l y least in that m a d e from coronal sections. The limits of the architectonic areas have b e e n superimposed upon the planar reconstructions (Figs. 1 and 2) as have also the limits of the m a j o r functional visual areas (Fig. 3); the latter are those that have b e c o m e generally accepted from other studies m32"64. E x a m i n a t i o n of the sections stained by the Gallyas m e t h o d 22 for myelin fibres has confirmed the earlier descriptions of the myeloarchitecture of the cortex in the walls of the superior temporal and intraparietal sulci. The afferent cortico-cortical connections of area P G have been d e t e r m i n e d in an e x p e r i m e n t in which a large injection has involved a considerable extent of this area on the surface of the inferior parietal lobule, and which has spread into the posterior wall of the intraparietal sulcus and into the anterior wall of the superior temporal sulcus but without reaching the fundus of either sulcus (Figs. 1, 4 and 5). The injection is virtually limited to the cortex with minimal involvement of the underlying white matter. Labelled cells are present in the cortex of widespread areas of the parietal, occipital and temporal lobes, on the surface and in the walls of sulci on both the medial and lateral aspects of the hemisphere. On the medial surface there is cell labelling in the cortex anterior to the parieto-occipital sulcus and below the cingulate sulcus in what are considered to be areas O A and PE, the

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Fig. 1. The extent of the cortex (within broken lines) on the medial and lateral surfaces of the cerebral hemisphere of a macaque monkey which is included in the planar reconstruction. The site and extent of the large in~ection of HRP in area PG are indicated by stipple and the positions of the sagittal sections in Fig. 5 are shown. AS, arcuate sulcus; CG, cingulate sulcus; CL, calcafine sulcus; CS, central sulcus; IOS, inferior occipital sulcus; IPS, intrapa~etal sulcus; LS, lateral sulcus; LUNS, lunate sulcus; POS, parietooccipital sulcus; PS, principal sulcus; STS, superior temporal sulcus.

251 retrosplenial area and areas 23 and 24 of the cingulate cortex. Of these architectonic areas only the part of O A

on the medial surface appears to have been recognised as a functional visual area and called PO; in this area a representation of the p e r i p h e r a l visual field has been

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Fig. 2. A planar reconstruction made from coronal sections on which the limits of the architectonic areas, according to Bonin and Bailey~, are indicated by broken lines. The banks of the sulci are shown by thick lines and the fundi as thin lines. Arrows indicate the medial margin of the hemisphere. POM, medial pafieto-occipital fissure.

Fig. 3. The same planar reconstruction with the boundaries of the main, generally accepted functional visual areas shown by broken lines.

252

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Fig. 5. Outlines of sagittal sections of the cortex of the parietal lobe at the 4 levels shown in Fig. 1. The injection is shown by stipple and the distribution of the cell labelling is given by dots.

Fig. 4. The site and extent of the large injection (stipple) and the distribution of the cell labelling (dots) on a planar reconstruction.

found in electrophysiological studies 11. Cell labelling is also present in the u p p e r wall of the calcarine sulcus in what is i n t e r p r e t e d to be OB or visual area V2, and in the parieto-occipital sulcus in area O A or visual area, V3. On

the lateral surface of the h e m i s p h e r e there are labelled cells in the anterior wall of the medial part of the intraparietal sulcus, in areas O A and PE, and around the injection site in the posterior wall of this sulcus. Within the walls of the superior t e m p o r a l sulcus there is extensive cell labelling with only the rostral part being free of labelled cells; labelled cells are present in both the anterior and posterior walls and in the broad floor (Fig. 6). The labelling in the anterior wall of the medial part of the sulcus is in the posterior part of area P G of Bonin and Bailey 7, P G a of Seltzer and P a n d y a 56 or the medial superior t e m p o r a l area, MST, of D e s i m o n e and Ungerleider 15. The labelled cells in the posterior wall of this part of the sulcus are in area O A or V4 and possibly overlapping into the medial t e m p o r a l area, MT, as

253

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STS Fig. 6. The site of the injection (stipple) and the distribution of the cell labelling within the walls and floor of the superior temporal sulcus on a planar reconstruction made from sagittal sections.

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determined by its position and myelin staining 64. The cortex in the walls of the lower parts of the sulcus has been the subject of different interpretations and there is no clear correlation of the distribution of the cell labelling with any of the architectonic maps4t; however, most of the labelled cells in this experiment are in those parts termed TPO, IPa and T E a by Seltzer and Pandya 56. Over most of their extent in the superior temporal sulcus the labelled cells are arranged in clusters of approximately 500 /~m width, and when transposed to the planar reconstructions they appear to be in longitudinal bands along the length of the sulcus. Further cell labelling is present in the anterior wall of the lunate sulcus and in the occipito-temporal sulcus on the inferior surface of the hemisphere; the cortex in all of these sites is O A or V4. Thus, area P G is receiving cortico-cortical fibres from all the known prestriate visual areas and also from the cingulate cortex and the walls of the superior temporal sulcus. There are no connections with the other major subdivision of area 7, 7b or PF, nor with any area related to the somatic or auditory sensory systems. In all areas the labelled cells are predominantly in the

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Fig. 7. The sites of 2 small injections (stipple and solid black) at different antero-posterior positions in area PG and the distribution of the resulting cell labelling (open circles and dots) on a planar reconstruction. deep part of layer III of the cortex. No fine granularity indicative of orthograde axoplasmic transport of H R P was seen in this or any other brain after injections in PG, but there is evidence from earlier studies 9'11,27,55-5s'63 and from the experiments with injections in certain of the areas connected with P G to show that these corticocortical connections are reciprocal.

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Fig. 8. The sites of 2 small injections (stipple and cross-hatched) in the lateral and medial parts of area PG on an outline of the hemisphere (above) and on a planar reconstruction. The resulting cell labelling after each of these injections (open circles and dots) is within either the medial or the lateral parts of PG and the visual areas posterior to PG.

Fig. 9. The sites of 2 small injections in area PG (stipple) and the distribution of the cell labelling (dots) in the walls and floor of the lower part of the superior temporal sulcus on an planar reconstruction made from sagittal sections. The injection shown in A is in the posterior wall of the intraparietal sulcus and that in B is on the surface of the inferior parietal lobule.

255

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Such injections have been placed in most parts of PG, and throughout most of its antero-posterior and medio-

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Fig. 10. Photomicrograph of clusters of labelled cells in the cortex in the depth of the superior temporal sulcus after a small injection in area PG. ×30.

Small injections in area PG result in cell labelling in restricted parts of the areas containing labelled cells after the large injection, and the systematic differences in the distribution of this labelling suggest that the corticocortical projections upon PG may be well organised. IP,~

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~ Fig. 11. Photomicrograph of an injection of H R P in area PE on a coronal section. The injection involves the cortex on the medial and lateral surfaces of the hemisphere and the superficial part of the medial end of the intraparietal sulcus. ×2.

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Fig. 12. The site of the injection in areas PE and O A (stipple) on a planar reconstruction. The distribution of the cell labelling in the vicinity of the injection and in area P G is indicated by dots.

256 lateral extents. Within area PG itself the labelling may be confined to certain parts depending upon the site of the injection, and when the medial part is involved the labelling is present only in this portion whereas the converse is true after injections in the lateral part. Injections limited to the posterior wall of the intraparietal sulcus result in labelling that is restricted to within the sulcus, and after injections situated more posteriorly on the lateral surface of the hemisphere the labelled cells are also present only on the surface. These findings indicate that the cortex in the medial and lateral parts of PG are not interconnected, and neither is that on the surface connected with the posterior wall of the intraparietal sulcus. There is likewise a clear variation in the distribution of the labelling in other areas after injections in different parts of PG. The more anterior an injection is in PG (that is, deeper in the posterior wall of the intraparietal sulcus) the more lateral is the labelling in those parts of OA and PE that are in the anterior wall of the intraparietal sulcus and on the medial surface of the hemisphere, and the more posterior the injection in PG the more medial are the labelled cells in these areas (Fig. 7). After injections in the medial part of PG, the labelled cells are in the medial parts of the visual areas posterior to PG, V2, V3 and V4, and the converse is so after laterally situated injections (Fig. 8). Of particular interest in relation to the organisation of the cortico-cortical connections is the finding that after a small injection deep within the posterior wall of the intraparietal sulcus the cell labelling in the lateral part of the prelunate gyrus is in the representation of the central part of the visual field in V4 (refs. 15, 61). The cell labelling in areas 23 and 24 of the cingulate cortex also varies in distribution with differences in the site of the injection, and there are distinct patches of labelled cells following the small injections in PG. The lateral parts of areas 23 and 24 are related to the more posterior parts of PG and the medial parts to the posterior wall of the intraparietal sulcus. The posterior part of area 23 is connected to the lateral portion of PG and the anterior part of area 23 and area 24 to the medial region of PG. Except for the rostral part of the superior temporal sulcus, the entire cortex in the walls and floor of this sulcus is connected to PG, and in view of its considerable extent it is not surprising that the small injections in PG have shown that different parts of the sulcus are related to different portions of PG (Fig. 9). The anterior wall of the upper part of the superior temporal sulcus is considered here to be the posterior part of PG, and cell labelling is present here and in the posterior bank of this part of the sulcus (in O A or V4) after injections on the

surface of the inferior parietal lobule but not after involvement of the posterior wall of the intraparietal sulcus. The deep parts of the latter are related to the medial temporal visual area, MT, in the posterior wall of this part of the sulcus. The anterior and posterior walls of the lower part of the sulcus also have a differential relationship to PG, although even small injections in PG result in surprisingly widespread cell labelling within the sulcus. After an injection in PG that is limited to the lateral surface of the hemisphere (Fig. 10) the cell labelling is almost restricted to the anterior wall of the sulcus with only slight encroachment upon the floor, and the medio-lateral extent of the labelling is essentially the same as after the large injection. The cell labelling only extends across the floor of the superior temporal sulcus and into the posterior wall with injections extending into the posterior wall of the intraparietal sulcus, and if the injections are limited to the posterior wall of the intraparietal sulcus the labelled cells are found only in the floor and posterior wall of the superior temporal sulcus. There is, therefore, a distinct organization in the anteroposterior dimension, with anterior parts of PG being related to the posterior wall of the superior temporal sulcus and vice versa. Although there does not appear to be an organization in the medio-lateral extent, this may not have been recognised because of the widespread labelling even after small injections. After injections of whatever size in PG there are more labelled cells in the cortex within the superior temporal cortex than in any other area which suggests that the cortex within this sulcus is the major source of afferent cortico-cortical connections to PG. For reasons that are not clear, no fine granularity indicative of orthograde axoplasmic transport has been seen after any injection in area PG, but experiments with injections involving either areas PE and O A (visual area PO) on the medial surface or in O A on the prelunate gyrus (visual area V4) show that the connections of these areas, at least, with PG are reciprocal. Approximately the middle thirds of the extents of areas PE and OA that are on the medial surface of the hemisphere have been involved by an injection that is in the cortex just behind the posterior end of the cingulate sulcus and in the superficial half of the adjoining anterior wall of the parieto-occipital sulcus and the medial wall of the intraparietal sulcus (Figs. 11 and 12). There are labelled cells in both OA and PE medial and lateral to the injection, and in area PG they are on the lateral surface of the inferior parietal lobule and in the anterior bank of the most medial part of the superior temporal sulcus. This distribution of cell labelling in area PG agrees closely with the extent of the terminal degeneration described by Pandya and Seltzer after a lesion corre-

257

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Fig. 13. The sites of 2 small injections in V4, stipple and solid black, on an outline of the hemisphere (above) and on a planar reconstruction (below). The distribution of the cell labelling around the in~ections and in PG is shown by open circles and dots.

sponding closely to the site of the injection 44, and also with the distribution of the cell labelling in the experiments of Colby et al. with injections of HRP in this region (their visual area PO) 1]. In another experiment a small injection was placed in area O A or V4 on the lateral surface immediately above the tip of the inferior occipital sulcus (Fig. 13), and this is in the representation

of the central 10" of the visual field ]4"6a. As would be expected from earlier studies, labelled cells are present in a number of other visual areas, V2, V3, TE, but perhaps the most significant finding is a small patch of labelling in the depth of the posterior wall of the intraparietal sulcus about the middle of the medio-lateral extent of area PG. Confirmation of these reciprocal connections between PG and V4 is given by another experiment in which a small injection has involved the posterior bank of the superior temporal sulcus at the level of the posterior end of the lateral sulcus. The labelled cells in PG are at the same medio-lateral position as in the previous brain, but they are not so deeply placed within the posterior wall of the intraparietal sulcus; instead they form a narrow band in the posterior bank and superficial half of the posterior wall of this sulcus. The site of this injection is in the representation of a more peripheral part of the visual field and the cell labelling is more superficial in the posterior wall of the intraparietal sulcus. In each of these experiments with injections in PE or in V4 the labelled cells in PG are mainly as layer III of the cortex. DISCUSSION The present experimental findings confirm and extend those made in earlier studies in showing that area 7 has cortico-cortical connections with widespread parts of the prestriate and temporal cortex, including all of the known prestriate functional visual areas 9. As the injections of HRP were restricted to the cortex of area PG, 7a, it may now be concluded that it is specifically this architectonic subdivision that is related to the visual system which is in accord with the functional observations 24-26'36'37. In addition to its connections with the visual areas, PG is also connected to the cingulate cortex and to the walls of the superior temporal sulcus; the latter is the site of overlap of the two cortico-cortical visual pathways, to the parietal and temporal lobes, respectively, and it may be the source of the majority of afferent cortical connections to PG. Areas O A and PE on the medial surface of the hemisphere probably correspond to PGm or 7m of other classifications 9"44 and to the functional visual area PO ix. The finding of connections between this region of cortex and PG is in agreement with these other studies. These cortico-cortical connections are reciprocal and are sufficiently well ordered to raise the possibility at least that there may be some degree of a representation of the visual field in area PG. Other investigations, both anatomical and physiological, have shown that the other major subdivision of area 7 on the lateral surface of the hemisphere, 7b or PF, is related to the somatic sensory system24"30'39'49"5°'6°, but any interpretation of the corrico-cortical connections of the inferior parietal lobule is

258 critically dependent upon which classification of the cytoarchitecture of this region is accepted. For this reason, therefore, it should be emphasised that here the descriptions and limits given by Bonin and Bailey 7 have been used, and in particular that the cortex in the posterior wall of the medial part of the intraparietal sulcus and of the anterior wall of the upper part of the superior temporal sulcus have been included within area PG. It may be reasonable to accept that the experimental findings have justified this definition of PG because in their cortico-cortical connections these parts of the cortex of the inferior parietal lobule differ only in being with different parts of the same prestriate visual area and not with different structural or functional areas. The distinct differences in the distribution of the cell labelling after injections in different parts of PG suggest that there is an organization within these connections. Where an organization of the cortico-cortical connections has been shown in sensory and motor areas of the cortex it has invariably been related to a representation of the periphery, and there is a definite representation of the visual field in the visual areas connected with PG. Small injections of HRP in PG result in restricted distributions of cell labelling within this area, in both the anteroposterior and medio-lateral dimensions, and in the other areas connected with PG. Certain parts of PG are connected with the cortex in other areas containing known parts of the representation of the visual field; thus, the deeper part of the posterior wall of the intraparietal sulcus is reciprocally connected with the part V4 that is known to contain the representation of the central part of the visual field 14"61. Further evidence that this part of the posterior wall of the intraparietal sulcus is related to central parts of the visual field comes from a study of the cortico-cortical connections of area MT. An injection of tritiated amino acids at the site in MT containing the representation of the central 2° of the visual field has shown it to be connected to the depth of the intraparietal sulcus, in what has been called area VIP 63. In contrast, the posterior parts of PG, on the exposed surface of the inferior parietal lobule and in the anterior wall of the superior temporal sulcus, are connected with what is known to be the cortex containing the representation of the peripheral fields in areas V2 and V4 (ref. 16) and also with the cortex on the medial surface of the hemisphere that contains area PO in which there is also a large representation of the peripheral visual field 11. Electrophysiological studies of the anterior part of area MST, which is within the posterior part of PG in the anterior wall of the superior temporal sulcus, have shown it to contain the representation of the peripheral visual field, and this is in accord with the cortico-corticai connections of this part of PG 27'29"43'44'56. The cortico-

cortical connections of PG with the frontal eye-field are also well organized; the parts of the eye field related to movements of the eye in the periphery of the visual field are connected with the posterior parts of PG, and conversely the region related to central eye movements is connected to the part of PG in the posterior wall of the

intraparietal sulcus 10"42. A number of combined anatomical and electrophysiological investigations have shown that the distribution of the origin and termination of callosal fibres in the visual areas are closely related to the representation of the vertical meridian 65'67. The observations on the distribution of these connections in the region of PG differ to some extent between authors, with the technique used and between individual animals4'23'28'65; a further difficulty is that they become less well defined and more diffuse further away from the primary visual area, V165. Despite these difficulties it would seem reasonable to draw certain conclusions about their distribution in and around area PG. Although apparently present throughout most of the area, they are most dense close to its anterior and posterior margins, around the fundus of the intraparietal sulcus and at the boundary with V4 in the superior temporal sulcus, respectively. There is continuity between these, around the medial margins of PG where it again abuts on V4, and laterally at the boundary with area PF. In the part of PG on the exposed surface they are sparse, and may be absent altogether in the small region deep in the posterior wall of the intraparietal sulcus which is connected with the cortex containing the central representation in area V4. These anatomical findings on the callosal connections would be consistent with the physiological observations that the majority of the cells in PG have bilateral receptive fields 24"36"51. The finding of cell labelling being confined to the medial or lateral parts of PG after small injections restricted to these parts, suggests that the horizontal meridian is passing antero-posteriorly across about the middle of its extent. This suggestion is supported by the fact that cell labelling is found only in the medial or lateral parts of the peripheral representation in the other prestriate visual areas after these small injections in the medial or lateral parts of PG. It is also in accord with the results after injections of tritiated amino acids in known parts of the representation in area MT 63. From the evidence on the organization of its corticocortical connections it may be suggested that there is an ordered representation of the visual field in area PG of the inferior parietal lobule (Fig. 14). At present only a crude representation can be formulated, but the vertical meridian is situated around the periphery of PG and the horizontal meridian passes antero-posteriorly across about the middle of its medio-lateral extent. With the

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Fig. 14. Above, the extent of the cortex (within broken lines) on the lateral surface of the brain which is included in the planar reconstruction. Below, schematic figure of the proposed representation of the visual field in area PG (stipple) on a planar reconstruction. The vertical meridian is at the periphery of PG, and its continuity at the anterior margin of V4 is shown by the broken line. The horizontal meridian in both PG and V4 is represented by a line of dots. C, central visual field; L, lower quadrant of visual field; P, peripheral visual field;-U, upper quadrant of visual field. Arrows indicate medial margin of the hemisphere.

representation of the vertical meridian around the periphery, area PG would be similar to most of the other visual areas 63'65,67. The representation of the central part of the visual field may be relatively small, and there is good evidence for it being deep in the posterior wall of the intraparietal sulcus 63. The peripheral representation, however, is large and occupies the exposed lateral surface and anterior wall of the superior temporal sulcus. The inferior quadrant of the visual field is represented medially in PG and the superior quadrant laterally. Physiological studies already done indicate t h a t - t h e representation is crude because most neurons in PG have receptive fields that are large 5'24'36'37, but they may be restricted to certain parts of the visual field 5"36. It should be emphasised that what has been proposed must be considered to be very tentative, and it would be impor-

tant to investigate such a representation in further anatomical and functional studies. It is interesting to note that the proposed organization of the visual field in the posterior parietal lobe is also in accord with the neurological signs following damage to area P G ; for example, a tumour in the exposed part of area PG was shown to affect peripheral vision rather than the central parts of the visual field 46'47. If there is no representation of the visual field in area PG it is difficult to explain the anatomical observations of several workers, and it would suggest that this area of cortex is fundamentally different from all other cortical areas which are related to either the sensory systems or the control of movement, including the other subdivision of area 7 (ref. 49). If it is accepted that such a representation, although crude and overlapping, is present in PG it would Seem reasonable to infer that there is also an organization in other areas which have not so far been studied in detail. A r e a PO is known to contain a large representation of the peripheral parts of the visual field 11, and it is connected with the part of P G that is also considered to be related to the peripheral part of the visual field. The connections between area P G and the cingulate cortex represent the first relationship between the visual system and this part of the limbic system, and they are also well ordered; if there is a representation of the visual field in PG and if this is continued to the cingulate cortex, the representation of the central field of vision is medial and that of peripheral fields is lateral. Before discussing the possible significance of the distribution of the cell labelling in the superior temporal sulcus it should be emphasised that this labelling after injections of H R P in area 7 shows the organization of the efferent connections of the cortex in the walls of the sulcus. It is known from several previous studies that area 7 sends fibres to, and receives fibres from, the superior t e m p o r a l sLllcus 9"17'27"33'34'39-41"43"55'56 and the projections from area 7 and the auditory cortex to the superior temporal sulcus are precisely organised 9'41"56. It would seem reasonable, therefore, to assume that the distribution of the cell labelling in the present experiments indicates the sites in the superior temporal sulcus which are reciprocally connected with the cortex involved by the injection; it would be technically difficult to place injections in the walls of the superior temporal sulcus to determine this directly. For the same reasons the same assumptions are made for the connections between the inferotemporal cortex and the superior temporal sulcus 16' 27,29,43,56

The findings are largely in agreement with those of previous studies and especially with the detailed investigations of Seltzer and Pandya 56. Taken together with the evidence for the two subdivisions of area 7 being distinct

260 in their other c o n n e c t i o n s 9'1°'39'4°, these observations show that there is overlap of the somatic and visual systems in the superior temporal sulcus (Fig. 15). Although the two subdivisions of area 7 are not interconnected, their connections do overlap in the superior temporal sulcus. Area PG is connected with widespread parts of the anterior and posterior walls and floor of the superior temporal sulcus, while area PF is connected to a relatively small part and which is mainly in the f l o o r 39. Small injections show that the anterior wall of the superior temporal sulcus is related to that part of area PG on the surface of the inferior parietal lobule, while the posterior wall of the superior temporal sulcus is connected with the part of PG in the posterior wall of the intraparietal sulcus. The latter part of PG is in turn connected with the part of V4 containing the representation of the central visual field and the surface of the inferior parietal lobule is related to the peripheral visual field representation in V4. The auditory areas of cortex in the superior temporal gyrus are connected with widespread parts of the anterior wall of the superior sulcus 56 SO there is extensive overlap with the visual system and with that part of area 7a related to the peripheral visual field. There is far more overlap between the visual and auditory systems than between these and the somatic system, but the latter overlaps with parts of the anterior and posterior walls related to both the central and peripheral visual fields. These anatomical findings are in agreement with those made in electrophysiological studies of this region 6. The earlier conclusion about the walls and floor of the superior temporal sulcus being a region of convergence of the three major sensory systems is confirmed by these observations 27. Another important conclusion that may be drawn from this study of the connections of area PG is that the lower wall of the superior temporal sulcus is also the site of convergence of the two separate visual pathways from the prestriate visual areas, one related to the inferotemporal cortex on the middle temporal gyrus and the other to area PG, in the inferior parietal lobule (Fig. 16). The infero-temporal cortex, area TE of Bonin and Bailey 7, projects into the lower wall of the superior temporal sulcHs 27"29"56 and this is the part of the sulcus connected to the part of PG in the posterior wall of the intraparietal sulcus. Both this part of PG, and the inferotemporal cortex are connected a6"44 with the cortex containing the representation of the central visual field in V4 (refs. 13, 14, 61). As there are reciprocal connections between the superior temporal sulcus and the inferotempora116 and inferior parietal cortices (see refs. 9, 41), it is probable that functional activity in the latter two areas can indirectly influence each other. Although the two subdivisions of area 7 are connected

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Fig. 15. Schematic figure to show the extents of the cortex (within interrupted lines) in the walls of the lower part of the superior temporal sulcus that are related to the three major sensory systems.

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Fig. 16. To show the convergence of the two cortico-cortical visual pathways, the temporal and parietal, in the lower wall of the superior temporal sulcus. All these cortico-cortical connections are reciprocal and in the parts of the areas of cortex shown, V4, PG, TE, there is a representation of the central field of vision.

with areas related to distinct sensory systems there are, nevertheless, many similarities in their cortico-cortical connections. These similarities are sufficiently marked to suggest that there are certain c o m m o n principles in the anatomical connections subserving the outward progression and processing of information from the primary visual and somatic sensory areas to the posterior parietal and temporal cortex. Thus the sequences of corticocortical connections for these sensory systems are essentially the same in the details of the patterns and functions of their hierarchical and parallel pathways, in their relation to the cortex in the walls of the superior temporal sulcus and in their links with 2 major components of the limbic system. It is noteworthy, too, that the areas of cortex in the parietal and temporal lobes forming the final steps in these sequences are precisely those parts of the cortex that undergo such an enlargement in the evolution of the mammalian brain and particularly in man. Both areas PG and PF are interconnected with a large number of other areas of the cortex, and indeed respectively with most, if not all, of the areas related to either the visual or the somatic sensory system except the primary sensory areas (Fig. 17). It would seem that in each case there is one area which is a major source of afferent cortical connections, the cortex in the walls of the superior temporal sulcus for area PG and that of area 5 for P F 39. The connections with most of these areas are reciprocal, and these may be either of the feed-forward or the feed-back type 19'2°'32"52. There is .a well-ordered organisation in all those connections so that the representation of the body in other somatic sensory areas is maintained in area PF but with considerable overlap49; some neurons have exceptionally large and bilateral receptive fields, and are sometimes interspersed with cells related to the whole body. The similarly wellordered connections of area PG, together with the fact

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that some of these are with parts of the cortex in other areas that are known to contain the representation of either the central or peripheral visual field, suggests that there is a well-ordered representation of the visual field in area PG; here the receptive fields of the neurons are again usually large and b i l a t e r a l 5'2s'26"36'37, but they may be predominantly in one quadrant s'36. Although the representation of the visual field and of the body in areas PG and PF may be less precise than in the primary sensory areas there is a greater functional complexity of the neurons, and they are usually associated with movement of the eye o r l i m b 24-26'36'37'49 51. The degree of activity of the cells is influenced by the interest aroused and by the attention paid to the stimulus. Thus, in the two subdivisions the neurons are closely related to both the sensory and motor aspects of movement. The connections that pass from the primary sensory areas towards the parietal and temporal areas are recognised as feed-forward 19"21'32 and with these as criteria a hierarchical sequence can readily be constructed for the somatic 21'39, as well as for the visual areas 32'63. There are, however, in each of these sequences distinct parallel pathways and these are functionally different. In the visual connections, those to the temporal lobe are predominantly related to central vision and serve for the discrimination of detail ~3"63 while the pathway to the inferior parietal lobule is related more to the peripheral visual field and is implicated in visuospatial functions 2426,36.37. In the sequence from the somatic sensory area the pathway through area 5 is mainly related to deep t i s s u e s 18"37'53 and that through the second somatic sensory area to cutaneous stimuli, particularly of the hand and

262

Fig. 18. Schematic figure to indicate the extents of the cortex posterior to the central sulcus in the macaque monkey that are related predominantly to either the somatic (S), the visual (V) or the auditory (A) sensory systems, and the region of convergence of these 3 sensory systems in the walls and floor of the superior temporal sulcus (stipple). Note that area TG at the temporal pole, which receives projections from the area of convergence, has been left clear.

digits 2°'21'48. B o t h subdivisions of area 7 have reciprocal and well-ordered connections to largely separate parts of the superior t e m p o r a l sulcus 41"56, but there is a region Which is connected to each subdivision and also with the auditory cortex 27'41. The portion of the cortex in which there is overlap between the three sensory systems is small c o m p a r e d to that related to the individual systems (Fig. 18). The possibility that this area of overlap is h o m o l o g o u s with the posterior speech area in man has already been considered 27, and this must remain very tentative. T h e final step in the parietal and temporal lobes would a p p e a r to be the projection from the cortex in the walls of the superior temporal sulcus to area T G at the t e m p o r a l pole 31'35. The interconnections of both subdivisions of area 7 with the cingulate cortex and of certain steps in the series of connections to them with the amygdala are of significance in view of the observations in functional studies in the unanaesthetised m o n k e y that the activity of the neurons in area 7 is influenced by the interest and the attention paid by the animal to the stimulus 24-26'36'37'49"50. A r e a s P G and PF are reciprocally connected to separate but adjoining bands of the cingulate cortex, and in both there would a p p e a r to be an orderly representation of the visual field or the body. These connections represent the first relationship between the visual and somatic sensory systems and the cingulate cortex. The functional significance of these connections, like that of the limbic systems in general, is not clear, but these projections from area 7, together With those from the related areas in the frontal lobe, are amongst the m a j o r pathways b e t w e e n the neocortex and h i p p o c a m p a l formation 38. In contrast to the direct connections between area 7 and the cingulate cortex, there are very few with the

amygdala, a n o t h e r m a j o r c o m p o n e n t of the limbic system; such connections are present only with a limited part of P G near the fundus of the intraparietal sulcus 3. Through its connections with o t h e r areas of the cortex, however, each subdivision of a r e a 7 has indirect links with the amygdala. Of the areas which are somatic sensory in function, the insular cortex has the most interconnections with the amygdaloid nuclei2"3"6z; area P F sends ' f e e d - f o r w a r d ' type fibres directly to the granular insular a r e a and it is indirectly related to it through its connections with the second somatic and retroinsular areas a9"21'39. Of the visual areas, V4, T E and the cortex in the wails of the superior t e m p o r a l cortex are all connected to the amygdala3'62; P G is reciprocally connected with V4 and with extensive parts of the walls of the superior t e m p o r a l sulcus, and both these regions are in turn connected to TE. In view of the evidence for the i m p o r t a n t role of the amygdala in m e m o r y 21 it is of special significance that the neurons in the visual areas connected with it have receptive fields which contain the central part of the visual field 13'14, and that the small part of P G deep in the fundus of the intraparietal sulcus that has direct connections with the amygdala also has a representation of this part of the visual field 63. In the second somatic and retroinsular areas the representation of the hand is large and most of the cells are activated by cutaneous stimulation 2°'48'5°. It has already been noted that in the series of steps between the p r i m a r y sensory areas and the amygdala, the second somatic sensory area m a y occupy a position amongst the somatic sensory areas analogous to that of V4 with the visual areas 2x. The analogy may be t a k e n further by considering the situations of these two areas on parallel pathways from the neocortex to the limbic system (Fig. 17). The second somatic sensory area sends fibres to PF 21'39"6°, which in turn projects to the cingulate cortex, and to the insular areas which are connected with the amygdala. V4 is similar in sending fibres to P G , the other subdivision of area 7 and which is also connected with the cingulate cortex, and also to T E which is heavily connected with the amygdala. A l t h o u g h area 7 is not an 'association' area in the traditional sense of this term 37, it is, nonetheless, in m a r k e d contrast to the other sensory and m o t o r areas, a definite site of convergence. B o t h subdivisions are interconnected with areas of cortex in the sensory, m o t o r and limbic systems, their constituent neurons are related to both sensory and m o t o r functions and they receive fibres from a nucleus of the thalamus whose cells r e s p o n d to stimulation of m o r e than one sensory system 1.

Acknowledgements. This work was supported by a grant from the Wellcome Trust.

263

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