CONNEXIONS OF THE SOMATIC SENSORY CORTEX OF THE RHESUS MONKEY

Transcription

1 Brain (1969) 92, CONNEXIONS OF THE SOMATIC SENSORY CORTEX OF THE RHESUS MONKEY I. IPSILATERAL CORTICAL CONNEXIONS BY E. G. JONES AND T. P. S. POWELL {From the Department of Human Anatomy, Oxford) INTRODUCTION IN recent years there has been an increasing number of experimental investigations on the inter- and intrahemispheric fibre connexions of the main sensory areas of the cerebral cortex. In these experimental studies two main lines of interest may be discerned. The first, and wider, theme appears to be concerned with the pathways involved in the flow of impulses from the primary sensory areas, and in the progressive elaboration and integration, within the cortex, of information derived from different sensory systems (Myers, 1962; Kuypers, Szwarcbart, Mishkin, and Rosvold, 1965; Diamond, Jones and Powell, 19686). The second theme is more concerned with the finer details, particularly the organization of the connexions within and between the subdivisions of the main sensory areas (Jones, 1967; Wilson, 1968; Jones and Powell, 1968c). This theme is narrower than the first, and is probably more immediately relevant to contemporary neurophysiological studies of sensory mechanisms. These two spheres of interest, however, are closely interrelated, and, indeed, Hubel and Wiesel (1965) have stated that in the main visual sensory areas "one is... dealing with what are undoubtedly building blocks of perception." In the main somatic and visual sensory areas of the cortex, it is apparent that there is an anatomical segregation of "building blocks" of different types in that neurons with similar response properties tend to be grouped in different architectonic subdivisions of the primary sensory areas. Thus, in the postcentral gyrus of the monkey neurons responding specifically to light tactile stimuli are concentrated in area 3 while those excited only by pressure or rotation of a joint are aggregated in areas 1 and 2 (Powell and Mountcastle, 19596). Similarly, in the visual cortex of the cat, the majority of neurons in area 17 are "simple" in responding to appropriately orientated slits and bars of light, while those in areas 18 and 19 respond to increasingly more complex types of stimuli (Hubel and Wiesel, 1962, 1965). This segregation of 24 BRAIN VOL. XCH

2 478 E. G. JONES AND T. P. S. POWELL function between different architectonic subdivisions is also seen within individual subdivisions because, in both the somatic (Mountcastle, 1957; Powell and Mountcastle, 19596) and visual (Hubel and Wiesel, 1965, 1968) areas, neurons with similar modality and topographic properties tend to be arranged in columns disposed at right angles to the surface and extending through all the cortical layers. All the connexions of a sensory area are undoubtedly important in establishing the functional differences exhibited by neurons in different architectonic fields and in different columns. The part played by the various connexions in the maintenance or the reverse of the specificity of different functional columns has not been established, but anatomical investigations on the somatic and auditory areas of the cat's cerebral cortex suggest that some connexions respect the columnar organization while others may not. Thus, axonal degeneration in the contralateral cortex is usually a mirror image of the area destroyed by a lesion, or, if the damaged area projects to two contralateral fields, it sends fibres to the same topographic representation in each (Jones, 1967; Pandya and Vignolo, 1968; Jones and Powell, 19686; Diamond, Jones and Powell, 1968a). Association fibres, on the other hand, may serve to link together cells or columns with different functional properties, for in the visual (Hubel and Wiesel, 1965; Wilson, 1968), auditory (Diamond et al., 19686) and somatic sensory (Jones and Powell, 1968a) areas of the cat most, if not all, of the architectonic subdivisions seem to be connected by this type of fibre. The previous study of the cortical and thalamic connexions of the somatic sensory cortex in the cat has been extended to the monkey because in this animal, the architectonic subdivisions in being larger and more clear-cut, are more amenable to investigation, and in the present paper the ipsilateral cortical connexions of these subdivisions will be described. MATERIAL AND METHODS Under nembutal anaesthesia and with aseptic precautions, lesions were placed in the cerebral cortex of 25 rhesus monkeys (Afacaca mulatto). Large cortical lesions were made with a suction aspirator, and smaller (some very restricted) ones by careful removal under a dissecting microscope of a portion of the pia mater. Together, the lesions cover most of the cerebral cortex, but the majority are concentrated in the somatic sensory and motor regions. Eight to fourteen days postoperatively, the animals were perfused with 10 per cent formalin, and after a further period of fixation in formalin varying from one to three months, the brains were cut at 25ft on a freezing microtome. A 1 in 10 or 1 in 20 series of sections was stained by the Nauta and Gygax (1954) method or the modification of Fink and Heimer (1967). To improve the quality of the staining in all cases the brain was immersed in the mixture of calcium chloride, hydroquinone and formalin recommended by Albrecht and Fernstrom (1959). In certain experiments an alternate series of sections was stained with thionin. Before cutting, the brains were photographed to record the gyral and sulcal pattern and the approximate position of the lesion. The exact site and extent of the lesion, together with the distribution of the ensuing degeneration were recorded on projection drawings of individual sections and reconstructed on tracings of the photograph of the surface of the brain. In order to show degeneration buried in the walls of the lateral sulcus an orthogonal reconstruction was prepared from the normal hemisphere of one of the experimental brains and will be used as a standard diagram (fig. 1).

3 CORTICAL ASSOCIATION CONNEXIONS 479 ANT. Inftrior fact FIG. 1. Top left and right, two figures reproduced respectively from Powell and Mountcastle (1959a) and Roberts and Akert (1963) to show the three architectural subdivisions (areas 3,1 and 2) of SI and the architectonic fields of the insulo-opercular area. Bottom right, a reproduction of one of the maps of Woolsey (1958) showing the positions of, and topographic organization within, SI and SI I as determined by the evoked potential method, and of the motor (MI) and supplementary motor (MIT) areas as determined by electrical stimulation. Bottom left, the reconstruction of the insulo-opercular region which is used as a standard diagram in the present study. Abbreviations used: (i) top left; A - arcuate sulcus; CS - central sulcus; IP - intraparietal sulcus; L - lunate sulcus; P - principal sulcus; PCS - postcentral sulcus; PR - superior precentral sulcus; S - Sylvian fissure; SC - anterior subcentral sulcus; ST - superior temporal sulcus. Numbers with arrows to the left indicate positions of sections shown in other figures of original paper and in fig. 13B of present paper, numbers without arrows refer to the three architectural subdivisions of the somatic sensory cortex, areas 3, 1 and 2. (ii) top right; Allo - allocortex; CS - central sulcus; Tns a - agranular insular cortex; Ins d - dysgranular insular cortex; Ins g - granular insular cortex; IP - intraparietal sulcus; IPD - anterior subcentral sulcus; OFO - orbitofrontal cortex; PrCO - precentral opercular cortex; SA - arcuate sulcus; SP - principal sulcus; SSII - second somatic sensory area; tr - transitional zone. RESULTS In each experiment the lesions and the distribution of the resulting degeneration will be described in terms of both the functional and architectonic subdivisions of the

4 480 E. G. JONES AND T. P. S. POWELL cortex which are affected. For this purpose several maps have been consulted: for the cytoarchitecture of the upper part of the postcentral gyrus that of Powell and Mountcastle (1959a) was used, and for the lower part of the gyrus and the insuloopercular region that of Roberts and Akert (1963). Other architectonic fields were located by reference to the maps of Brodmann (1909) and the functional subdivisions of the somatic sensory and motor regions by reference to those of Woolsey (1952, 1958). Three of these maps are reproduced in fig. 1. It may be noted that in the cytoarchitectonic map of Roberts and Akert (1963) areas 3, 1 and 2 which together constitute the first somatic sensory area (SI) extend for some distance beyond the confines of SI as denned by the method of evoked potentials (Woolsey, 1952, 1958). Area 3 spreads forwards below the lower end of the central sulcus, and parts of areas 1 and 2 come to occupy the anterior half or so of the fronto-parietal operculum. Unless otherwise specified, for convenience and because the functional map is better known, use of the terms "first somatic sensory area" or "SI" will be restricted to the area delimited by evoked potentials. The Total Efferent Projection of the First Somatic Sensory Area (ST) The total extent of the efferent projection from SI is shown by experiment OM 53 (fig. 2). In this brain, most of SI has been destroyed by a lesion extending from the medial surface along the postcentral gyrus to a point just below and in front of the lower end of the central sulcus. The posterior margin of the lesion is formed by a line joining the postcentral sulcus to the lower end of the intraparietal sulcus; anteriorly, the lesion extends into the posterior wall of the centraf sulcus. Areas 3a, 3, 1 and 2 are, therefore, involved. At the lower end of the central sulcus the lesion, in extending forwards below the sulcus, passes beyond SI but remains within the confines of areas 3, 1 and 2. Degenerating fibres leaving the damaged area of cortex can be traced to the small part of SI remaining undamaged (including parts of area 3a lying in the depths of the central sulcus) and to four other cortical regions the precentral gyrus, the frontoparietal operculum, the superior parietal lobule, and the marginal gyrus on the medial surface of the hemisphere. The whole precentral gyrus contains dense degeneration; anteriorly, it extends forwards into the posterior bank of the arcuate sulcus, medially it is continuous with that in the marginal gyrus but laterally it does not extend below the inferior precentral sulcus. This area of degeneration conforms closely both to the "motor cortex" as defined by electrical stimulation and to the cytoarchitectonic field, area 4. Even in the Nauta-stained sections it is possible to see that the degeneration does not extend beyond the region of Betz cells, so that on the convexity of the brain area 6 is not involved. On the medial surface of the brain, for some distance in front of and behind the lesion, degenerating fragments fill the cortex covering the marginal gyrus, including that in the upper bank and the deeper part of the lower bank of the cingulate sulcus. There is a continuous rostro-caudal band of degeneration extending from a point directly above the rostrum of the corpus callosum to the upturned caudal end of the cingulate sulcus. It thus fills that part of area 5 which lies behind SI on the

5 CORTICAL ASSOCIATION CONNEXIONS 481 FIG. 2. To illustrate Experiment OM 53 in which most of SI has been destroyed by a large lesion (black). The total extent of the ensuing cortical degeneration (stipple) is shown on reconstructions of the dorsal, lateral and medial surfaces and of the insulo-opercular region (A). The presence of degeneration buried in the cingulate sulcus is indicated by the small arrows. In B, the distribution of terminal degeneration (stipple) and of degenerating fibres (short lines) is shown on a series of representative sections taken from the levels indicated in A- Apart from undamaged parts of SI, four other cortical areas contain degeneration the motor (area 4) and supplementary motor areas, SII and area 5 (cf. fig. 1). medial surface and those parts of both areas 4 and 6 which lie in front of it. In functional terms, the part of area 6 involved conforms almost exactly to the "supplementary motor area" of Woolsey (1958), the affected region even extending slightly on to the dorsal surface of the brain opposite the upper end of the arcuate sulcus, as shown by Woolsey for the supplementary motor area. Inferior to the lesion, degenerating fragments extend deeply into the lateral sulcus. In the superior face of the sulcus the degeneration reaches from a point opposite the rostral end of the insula almost to the posterior end of the sulcus. The inner face of the frontoparietal operculum is filled by degeneration except at its most rostral end. This degeneration extends shghtly into the cortex covering the posterodorsal aspect of the insula. At the point at which the superior and inferior faces of the lateral sulcus come together, posterior to the insula, the degeneration in the insular cortex continues for a short distance into the deeper aspect of the inferior face. In the insular-opercular region, therefore, the parts of areas 1 and 2 which are found here

6 482 E. G. JONES AND T. P. S. POWELL are involved, together with the second somatic sensory area (SII). The degeneration lying in the posterodorsal aspect of the insula is interpreted as being in the trunk area of SIT. Posterior to the lesion degeneration is present in parts of the inferior and superior parietal lobules. In the cortex of the inferior parietal lobule terminal fragments extend to the posterior margin of SI but not beyond. There is also a small patch of degeneration immediately above the lateral sulcus where the exposed part of the face area of SII is filled, the degeneration being continuous with that in the buried part of SII. Area 7, occupying the greater part of the inferior parietal lobule is unaffected. The cortex of the superior parietal lobule, on the other hand, is virtually full of coarse degenerating fragments, only a narrow region just in front of the lunate sulcus (area 7) escaping. Medially, this degeneration is continuous with that on the medial surface; laterally, it extends into the medial bank of the intraparietal sulcus, disappearing at the fundus. The affected area in the superior parietal lobule conforms almost exactly to area 5. In summary, SI projects to other parts of areas 3, 1 and 2 (including area 3a), to SII, to the motor (area 4) and supplementary motor areas, and to area 5. Degenerating fibres passing to undamaged parts of SI lie mainly within the cortex, in the deeper aspects of layers IV and V, but a few spread out for a few millimetres beyond the lesion in the most superficial part of layer I (fig. 3). Degenerating fibres passing to more distant areas enter the white matter close to the lesion and re-enter the cortex near their destination, curving smoothly up towards layers III and IV. In all areas, including SI itself, fine terminal fragments are visible in all cortical layers, including layer I, but are particularly concentrated in layers III-V (figs. 3, 4). The Efferent Projection of the Second Somatic Sensory Area {SIP) Because the greater part of SII is buried in the lateral sulcus, it is virtually impossible to damage selectively all of it. In one animal, OM 73, however, most of the face and fore-limb parts of SII were destroyed by carefully inserting a needle into the upper bank of the lateral sulcus, opposite the lower end of the intraparietal sulcus (fig. 5). The lesion is confined to the cortex and degenerating fibres can be traced from it to the undamaged parts of SII, to the portions of areas 3, 1 and 2 lying below the lower end of the central sulcus and in the frontal operculum, and to certain parts of SI, area 4 and the supplementary motor area. No degenerating fibres, however, can be traced to area 5. The undamaged parts of SII are filled with degenerating fragments, and these are continuous with others in the parts of areas 1 and 2 occupying the superior and inner faces of the fronto-parietal operculum. On the exposed surface of the brain, the forward extension of area 3 below the motor cortex contains heavy degeneration which extends dorsally behind and in front of the central sulcus to fill the parts of SI and the motor cortex containing the representations of the face and fore-limbs. The degeneration in the motor cortex is noticeably less intense than that in SI. In SI itself areas 3, 1 and 2 are involved. There is no degeneration in area 5. The only other cortical area containing degeneration is a small portion of the

7 CORTICAL ASSOCIATION CONNEXIONS 483 OM 73 FIG. 5. To illustrate Experiment OM 73 in which the lesion mainly destroys the face and forelimb subdivisions of SO. Degeneration affects the topographically related parts of SI, and of the motor and supplementary motor areas but not area 5 (cf. fig. 2). supplementary motor area on the medial surface of the hemisphere, and again within the representation of the face and fore-limb. Here, the degeneration is very sparse. Topographic Organization of Efferent Projections from SI Four experiments in which topographic subdivisions of SI were damaged without regard to architectonic fields demonstrate the organization of the efferent projections from this area. In the first of these, OM 43, most of the hind-limb area at the upper end of the postcentral gyrus and on the adjoining medial surface of the hemisphere was destroyed (fig. 6). As in the first experiment with a large lesion, terminal degeneration is found in SI and SIT, in area 4 and the supplementary motor areas, and in area 5. In each of these regions, however, it is restricted to a small part of their extent. In the cortex of SI, degeneration is found on all sides of the lesion but does not extend laterally beyond the level of the postcentral sulcus and medially it does not reach deeply into the cingulate sulcus. Thus, only the hind-limb subdivision contains degeneration and all other subdivisions, including the immediately adjoining trunk and tail regions, are free. In SII, as in SI, only the hind-limb area is affected; degenerating fragments are found only in the cortex in the most posterior part of the superior face of the lateral sulcus and do not encroach on the inferior face or insula (trunk area). In area 4 and the supplementary motor area, again only the hind-limb subdivisions contain degeneration. That in area 4 is situated at the upper end of the

8 484 E. G. JONES AND T. P. S. POWELL precentral gyrus and on the medial surface and is virtually a mirror-image of the affected area in SI. The motor area for the tail, low down on the medial surface of the marginal gyrus, is spared, but there is a further, very localized focus of degeneration below this in the depths of the cingulate sulcus. This is interpreted as being in the supplementary motor area for the hind-limb. Most of the degeneration in area 5 is in that part of this architectonic field situated in the marginal gyrus on the medial surface, about, and in the banks of, the upturned posterior end of the cingulate sulcus; a few fragments, however, encroach upon the dorsal surface immediately posterior to the hind-limb subdivision of SI. OM 43 FIG. 6. Showing the lesion affecting the hind-limb subdivision of SI in OM 43 and the ensuing degeneration in the topographically related parts of SII and of the motor and supplementary motor areas, and in a restricted part of area 5. In the next experiment, OM 55 (fig. 7), there is a small lesion confined to the cortex just in front of the postcentral sulcus and affecting the portion of SI topographically related to the trunk. Degeneration in SI spreads rather more widely than in the preceding experiment and appears in the shape of a T: a relatively narrow band, containing the lesion, spans the postcentral gyrus, from the fundus of the central sulcus back to the postcentral sulcus, while a second band, at right angles to the first, stretches along the posterior margin of the postcentral gyrus from the lower end of the intraparietal sulcus laterally, through the postcentral sulcus, to the cingulate

9 CORTICAL ASSOCIATION CONNEXIONS 485 0M55 FIG. 7. Showing the lesion in the trunk area of SI in OM 55 and the consequent degeneration in the trunk areas of SII and of the motor and supplementary motor areas and in a small part of area 5. sulcus medially. This whole T-shaped region is interpreted as the SI representation of the back of the head and neck, the trunk and the tail. In SII the localized patch of degeneration lies deeper in the lateral sulcus than in the preceding experiment, mainly occupying the deeper aspect of the superior face of the sulcus, but encroaching upon the inner face, insula and lower face. This is consistent with it being in the representation of the trunk and tail. Degeneration in area 4 is concentrated in a small region of cortex approximately opposite the lesion and containing the representation of the trunk, but numerous fragments spread laterally towards the head region and medially towards the representation of the tail. There is a small focus of degeneration in the supplementary motor area: this is largely confined to the depths of the cingulate sulcus and occupies a position immediately rostral to that affected in OM43. Posterior to SI, degeneration in area 5 occupies a small portion of the superior parietal lobule behind the postcentral sulcus. The full rostro-caudal extent of this segment of area 5 is, however, affected. The brain of the third experiment of this group, OM 63 (fig. 8), has a lesion in, the cortex of the distal fore-limb region of SI. The resulting degeneration in SI is confined to the fore-limb region, not extending above the level of the postcentral

10 E. G. JONES AND T. P. S. POWELL Fio. 8. To illustrate Experiment OM 63 in which the distal fore'limb subdivision of SI is damaged. sulcus nor below the lower end of the intraparietal sulcus. Anteriorly, it extends into the depths of the central sulcus. In SII terminal degeneration is also restricted to the fore-limb subdivision. The affected region mainly occupies the superior and inner faces of the parietal operculum, approximately opposite the caudal half of the insula. This area of degeneration is anterior to that in OM 43 and more superficial than that in OM 55. In the motor and supplementary motor areas degeneration is found throughout the fore-limb subdivisions, while in area 5 there is a band of degeneration stretching caudally from SI across the lower half of the superior parietal lobule, but only extending into the upper half of the medial bank of the intraparietal sulcus. The lesion in the final experiment of this group, OM 57 (fig. 9), is mainly in the anterior prolongation of area 3 below and in front of the lower end of the central sulcus. It extends dorsally, however, into the lower end of the sulcus so that a small part of the representation of the face in SI is destroyed. Degenerating fragments reach deeply into the cortex of the lateral sulcus to fill those parts of areas 1 and 2 which lie in the fronto-parietal operculum, and continue caudally in the superior face of the sulcus to involve most of the face region of SII. Terminal degeneration is also found mbre dorsally, behind the central sulcus, filling most of the head region of SI, and also the part of area 5 forming the medial bank of the intraparietal sulcus. In front of the central sulcus, degeneration extends dorsally to fill that part of area 4

11 CORTICAL ASSOCIATION CONNEXIONS 487 OM 57 I 23 4 FIG. 9. Showing the lesion and extent of the degeneration in Experiment OM 57 in which the face area of.si is affected together with the rostral extension of area 3 below the central sulcus. Note that apart from degeneration in the same cortical areas as in preceding figures, the parts of areas 1 and 2 occupying the frontal operculum also contain degeneration. topographically related to the face.' There is a further small focus of sparse degeneration in the most anterior part of the supplementary motor area, just at the medial margin of the hemisphere (face area). Connexions of Individual Architectonic Subdivisions of SI In eight experiments it was possible to place small lesions selectively within areas 3, 1 or 2 of the postcentral gyrus. These areas were located at operation by reference to the maps of Powell and Mountcastle (1959a) and of Roberts and Akert (1963), and in most cases the restriction of the lesion to one or other of these fields could be confirmed by examination of Nissl-stained sections of the brains. The lesion in OM 74 (fig. 10) is in area 3 at the upper end of the central sulcus, and degenerating fibres spread forwards in the cortex to terminate in area 3a, at the bottom of the sulcus. Other fragmented fibres pass in the white matter under the sulcus and end in a narrow wedge of area 4 along the medial margin of the hemisphere. The greatest density of terminal degeneration is in that part of area 4 lying in and adjacent to the central sulcus but the whole rostro-caudal extent of the gyrus contains a few terminal fragments; all are within the hind-limb area. Within area 3 itself degeneration spreads a little on each side of the lesion and on the medial surface of the brain reaches the cingulate sulcus. The fragments, however, remain within the hind-limb representation.

12 E. G. JONES AND T. P. S. POWELL FIG. 10. Showing the small lesion affecting area 3 in OM 74. This causes a band of degeneration stretching through the pre- and postcentral gyri into area 5, and other localized foci of degeneration in topographically related (hind-limb) parts of SII and the supplementary motor area. Posterior to the lesion, degenerating intracortical fibres distribute terminal degeneration in a narrow antero-posterior band, of about the same width as the lesion and spanning areas 1 and 2, along the dorsomedial margin of the hemisphere. Justbehind the level of the postcentral sulcus this band continues on to the medial surface to lie within a small anteroposterior segment of area 5. Other small foci of degeneration are found in the hind-limb regions of SII and of the supplementary motor area. In OM 75 the damage is confined to area 1 just in front of the postcentral sulcus (fig. 11). As in the previous experiment, terminal degeneration in the cortex forms a narrow band passing forwards from the lesion to affect areas 3, 3a and 4, and backwards to involve areas 2 and 5. Within area 1 itself terminal degeneration is restricted to a few millimetres on each side of the lesion. The degenerating fragments remain within the trunk representation of SI and of area 4, and in the latter they are concentrated on the exposed surface of the precentral gyrus, but a few are also present in the anterior bank of the central sulcus. The full anteroposterior extent of area 5 receives degenerating terminals, but the mediolateral extent of the portion involved is restricted to a very narrow band close to the dorsomedial margin of the hemisphere. Additional small foci of degeneration are again found in the trunk regions of SII and of the supplementary motor area.

13 CORTICAL ASSOCIATION CONNEXIONS 489 OM75 FIG. 11. To illustrate OM 75 in which a part of area 1 situated within the trunk subdivision of SI has been destroyed. The lesion in the brain of OM 54 (fig. 12) is in area 2, at the lower end of the intraparietal sulcus. It affects that part of SI containing the representation of the fore-limb, but, from the distribution of the ensuing degeneration it would appear that certain regions related to the head are also destroyed. Terminal degeneration in area 2 itself follows the posterior margin of SI and extends upwards to the postcentral sulcus and downwards to a point just below the lower end of the intraparietal sulcus. There is also a wide band of degeneration reaching forwards in the cortex, through areas 1, 3 and 3a to area 4 where there is heavy terminal degeneration in the parts related to the fore-limb and back of the head. Posterior to the lesion heavy terminal degeneration is distributed to that part of area 5 lying along the lateral margin of the superior parietal lobule and in the medial bank of the intraparietal sulcus. Other foci appear in the head and fore-limb regions of SII and of the supplementary motor area. In the next three experiments, in which the lesions are very small about 1-2 mm. square the brains were cut in the sagittal plane. This permits the degeneration to be plotted more accurately in relation to areas 3,1, 2, 4 and 5. Degeneration can also be detected in SII and in the supplementary motor area but in this plane of section it can be less readily localized. The lesions in the three experiments, OM 46, 76 and 47, are situated respectively in areas 3, 1 and 2 (fig. 13A). All were confined to the cortex (fig. 13c). In experiment OM 46 the lesion affects a small part of area 3

14 E. G. JONES AND T. P. S. POWELL FIG. 12. Showing the lesion affecting area 2 in OM 54 and the ensuing degeneration which affects the same cortical areas as the lesions in figs. 10 and 11. situated within the part of SI related to the distal portion of the fore-limb. Degenerating fibres pass forwards and slightly medially to areas 3a and 4 and backwards and slightly laterally to areas 1, 2 and 5. There is terminal degeneration in each of these areas and in area 3 itself, and it is concentrated in a band no more than 5 mm. wide passing across the central sulcus. The band is continuous but there are definite foci of increased terminal degeneration in each individual area. This is particularly noticeable in area 4 where degenerating fragments are found across the full extent of the precentral gyrus but are concentrated in the rostral bank of the central sulcus; area 3a also shows a very localized patch of degeneration. The terminal degeneration in area 3 is only slightly more extensive, mediolaterally, than that in all of the other areas except area 5 where the band of degeneration is at its widest. The damage in OM 76 is restricted to a small part of area 1 contained within the representation of the hind-limb at the medial margin of the hemisphere. There is degeneration in the same cortical areas as in the preceding experiment, and there is again a continuous band of degeneration extending forwards and backwards from the lesion with foci of increased degeneration in each area. The foci in areas 3a and 2, however, are situated slightly more lateral than those in areas 4, 3 and 5 so that the whole band acquires a somewhat staggered appearance. In the final experiment of this group,

15 CORTICAL ASSOCIATION CONNEXIONS 491 0M46 0M7S 0M47?J t. FIG. 13. To illustrate three experiments in which very small lesions were confined to individual architectonic subdivisions of SI. In OM 46, OM 76 and OM 47 (A), the lesions are respectively in areas 3, 1 and 2. In B, a series of sagittal sections showing the disposition of architectonic fields in approximately the same regions as those destroyed have been redrawn from figs. 2, 4 and 5 of Powell and Mountcastle (1959a). In c, the distribution of the degeneration in the three experiments has been plotted on a 1 in 10 series of sagittal sections through the central sulcus. Note that in each experiment, all architectonic subdivisions of SI contain degeneration as also do areas 4 and 5 and the transitional field, area 3a. AS - arcuate sulcus; CS - central sulcus; CgS - cingulate sulcus; I-PS - intraparietal sulcus; LS - lunate sulcus.

16 492 E. G. JONES AND T. P. S. POWELL OM 47, the lesion is in area 2, just above the lower end of the intraparietal sulcus and within the part of SI related to the distal segments of the fore-limb. Terminal degeneration affects the same areas, in front of and behind the lesion, as in the first two experiments. As in the other two there are distinct foci of intense degeneration in areas 4, 3a, 3, 1 and 5 with relatively sparse degeneration in between. In this case the degeneration in area 5 is at a more medial level than that in the other areas. In each of the foregoing experiments unequivocal foci of terminal degeneration were found in SII and in the supplementary motor area. Its distribution varied in each ' experiment according to the part of the representation of the body surface destroyed in SI. Afferent Cortical Projections to the Somatic Sensory Cortex Brains are available with lesions affecting most functional and architectural areas of the cortex but only those with lesions in area 4 cause degeneration in SI and SII. Lesions in the supplementary motor area, areas 5 and 6 do not. OM 70 is an example of an experiment in which most of area 4 has been destroyed by a large lesion reaching across the precentral gyrus from the medial surface of the brain to just above the inferior precentral sulcus (fig. 14). In the frontal lobe terminal degeneration is present in the undamaged parts of area 4, in the whole of area 6 (including the supplementary motor area) and a few fibres also reach area 8 in the anterior bank of OM 70 FIG. 14. Showing the lesion and the extent of the degeneration in Experiment OM 70 in which the motor cortex (area 4) was destroyed. Note degeneration in SI and SO and throughout the whole of area 6.

17 CORTICAL ASSOCIATION CONNEXIONS 493 the arcuate sulcus. Degeneration elsewhere in this brain is confined to SI and SII, including the rostral extension of areas 3, 1 and 2 below the central sulcus and in the frontal operculum. Degenerating fibres reach these areas by running in the white matter and distribute terminal fragments to all cortical layers, but the heaviest concentration is in layers III, IV and V. The whole of SI and SII contain degeneration but that in SII is less intense than in SI. In SI, areas 3, 1 and 2 and area 3a in the depths of the central sulcus are equally affected with heavy degeneration, but that in the parts of these areas lying below the motor cortex and in the frontal operculum is noticeably sparser. Experiments with small lesions affecting area 4 indicate that the projection from this area to SI and SII is topographically organized in a similar manner to the projection of these areas to it. DISCUSSION The chief findings of this investigation are that the first (SI) and second (SII) somatic sensory areas are connected with one another and with area 4 in a reciprocal, organized manner and that each has a further projection to the supplementary motor area, but SI alone sends fibres outside the sensorimotor region to area 5. The projections to the supplementary motor area and to area 5 are organized but are not reciprocal (fig. 15). The fibres passing from SI to the above areas arise in all three of its architectonic subdivisions (areas 3, 1 and 2). In addition, areas 3, 1 and 2 are interconnected with one another and with the transitional field between sensory and FIG. 15. A schematic diagram to show the anatomical pathways outlined in the present investigation. Reciprocal connexions join SI and SII to one another and to area 4, and small projections pass from SI and SII to the supplementary motor area (SMA), but only SI sends fibres to the parietal field, area 5.

18 494 E. G. JONES AND T. P. S. POWELL motor cortex, area 3a, by intracortical association fibres. The fibre connexions passing within and between SI and SII may be termed intrinsic connexions while those joining SI and SII to cortical areas outside the classical somatic sensory region may be regarded as extrinsic connexions. Basically, the extrinsic connexions are similar to those already described in the cat (Jones and Powell, 1968a) but the use of the monkey has permitted a greater degree of certainty in determining that all of the architectonic subdivisions of SI contribute to all efferent cortical pathways from SI, and also in establishing a projection to the supplementary motor area. In addition, it has been possible in the monkey to define with greater precision the organization of intrinsic connexions within SI. The intrinsic connexions of SI will be considered first. The findings are of interest from two points of view: in the first place, these fibres respect the broader topographic subdivisions of SI in that when a lesion is confined to the head, trunk or hind-limb subdivisions, degeneration fills the affected subdivision but does not spread into other subdivisions. From the experiments with very small lesions, it is probable that this spatial organization is even more precise; for example, in experiment OM 46 (fig. 13) the lesion was apparently confined to the representation of the fore-paw digits and the ensuing degeneration, though spreading across the full rostro-caudal extent of a segment of the postcentral gyrus did not fill the whole fore-limb region. Thus, no integration between different subdivisions of the body representation in SI would seem possible. Secondly, although the intrinsic fibres respect topographic boundaries in SI they cross the boundaries between its architectonic subdivisions and, therefore, because of the differentiation of function between these fields (Powell and Mountcastle, 19596), they probably unite cellular columns with different response properties. In other words, functional columns in area 3, the majority of which respond preferentially to light tactile stimuli are firmly and reciprocally interconnected with those in areas 1 and 2 which respond mainly to deep stimuli, that is, to pressure or rotation of a joint. Within these individual areas, however, columns with similar response properties are only connected within the limits of topographic boundaries. It is probable, therefore, that the significance of the intrinsic association fibre connexions of the somatic sensory cortex lies in their connecting parts of the cortex with different response properties but within the same peripheral representation. This pattern of intrinsic connexions has many similarities with the situation in the visual cortex of the cat. Cellular columns in the three main architectonic (and functional) subdivisions of the visual cortex, areas 17, 18 and 19 (or visual I, visual II and visual HI) are selectively activated by peripheral stimuli of different orders of complexity (Hubel and Wiesel, 1962, 1965). Hubel and Wiesel found that single units in area 17 could be classified as simple on the basis of the type of peripheral stimulus required to evoke a response, those in area 18 as complex and at least 50 per cent of those in area 19 as hypercomplex. In the somatic sensory cortex, areas 3, 1 and 2 are interconnected and the similarity between areas 3 and 17 on the one hand and between areas 1 and 2 and 18 and 19 on the other is striking.

19 CORTICAL ASSOCIATION CONNEXIONS 495 The analogy between the somatic sensory and visual cortex may be carried even further for areas 17, 18 and 19 project to a fourth area which also receives fibres from the lateral geniculate nucleus the lateral suprasylvian area (Vastola, 1961; Thompson, Johnson and Hoopes, 1963; Garey and Powell, 1967; Glickstein, King, Miller and Berkley, 1967; Wilson and Cragg, 1967). The further connexions and functional properties of this area are unknown, but it could be analogous to SII, because the latter receives fibres from areas 3, 1 and 2 and from the ventrobasal complex of the thalamus (Macchi, Angeleri and Guazzi, 1959; Guillery, Adrian, Woolsey and Rose, 1966; Jones and Powell, 1969a). This analogy between the somatic sensory and visual systems is by no means conclusive chiefly because of lack of information on the visual areas of the monkey. A further difficulty is that areas 17, 18 and 19 in the cat seem to contain separate representations of the retina (Hubel and Wiesel, 1965; Bilge, Bingle, Seneviratne and Whitteridge, 1967), whereas in SI the available evidence is that there is only a single representation of the contralateral half of the body (Woolsey, Marshall and Bard, 1942; Woolsey, 1958). The trunk and proximal parts of the body are represented posteriorly (mainly in area 2) and the representation of the apical portions of the limbs and the face are predominantly in the depths of the central sulcus (area 3). The representation pattern in SI could, however, be more complex because Powell and Mountcastle (19596) have emphasized that "even the most apical portion of the hand or the foot is represented in a band of cortical tissue extending across the entire rostrocaudal extent of the postcentral gyms," and in the squirrel monkey Werner and Whitsel (1968) found that some neurons at the anterior margin of SI could be driven from the dorsum of the back. The possibility exists, therefore, that a triple representation could be present in SI, though this might be modified and obscured in some subtle and hitherto unsuspected manner. It is not known whether area 3a, at the rostral margin of SI sends fibres to the other three fields in the monkey but it receives fibres from all of them, and like areas 3, 1 and 2 it receives further fibres from areas 4 and SII. Furthermore, it receives a projection from the ventrobasal complex (Jones and Powell, 1969a) of the thalamus. This similarity of connexions makes it probable that area 3a should be considered an integral part of SI and there are grounds for believing that it may represent a further functional as well as an architectonic subdivision. Powell and Mountcastle (19596) found that, in distinct contrast to the immediately adjoining area 3, area 3a seemed to receive a heavy projection from deep tissues. In the cat, Oscarsson and Rosen (1966) described a cortical projection area for Group 1 muscle afferents from the fore-limb, the maximal response region of which lay in area 3a. As area 3a in the cat has the same cortical and thalamic connexions as SI proper it was predicted (Jones and Powell, 1968a) that a projection area for Group 1 afferents from the hind-limb should be present in the part of area 3a situated on the medial surface of the hemisphere and this has been shown physiologically (Landgren and Silfvenius, 1968). It therefore seems possible that area 3a may be a specific cortical projection area in SI for Group 1 muscle afferents in much the same way as area 3 is the main

20 496 E. G. JONES AND T. P. S. POWELL receiving area for cutaneous afferents and areas 1 and 2 for afferents from deep tissues. Recent work has tended to discount the older view that afferent impulses from muscle spindles and Golgi tendon organs reach the sensory cortex (Rose and Mountcastle, 1959; Matthews, 1964). The main body of evidence has pointed to their being directed almost exclusively to the spinal cord and cerebellum. If, however, area 3a is an architectonic subdivision of SI devoted to receiving such afferents this view may have to be reconsidered. From its position adjacent to the motor cortex and with intimate cortical connexions joining it to both the motor cortex and all subdivisions of the somatic sensory cortex, area 3a would appear to be strategically situated for a role in sensorimotor integration in the pre- and postcentral gyri. Significantly, the cortical area, stimulation of which gives rise to effects upon transmission in the dorsal spinocerebellar tract of the cat (Hongo, Okada and Sato, 1967) would appear to lie in area 3a. Area 3a and the three fields of SI also have direct connexions with SII. In the case of areas 3, 1 and 2 it has been shown that these are reciprocal, and it seems likely, both on a priori grounds and from the limited information available from the cat (Jones and Powell, 1968a) that area 3a sends fibres to SII as well as receiving from it. Because of the considerable overlap in the projections of all these fields to SII, it seems possible that SII could be a region of convergence and integration, at a relatively low level, for all somatic sensory modalities. As its main cortical outflow is to the motor and supplementary motor areas, rather than to "association" cortex, SII could be concerned in effects upon the motor areas at a slightly higher level than those mediated by fibres passing from the individual subdivisions of SI, and at a considerably lower level than those mediated by the pathways passing through parietal, temporal and frontal cortex. The main topographic subdivisions of SI are preserved in its projections to the parietal field, area 5 there is only slight overlap in the distribution of fibres from head, limb and trunk regions. Area 5, in both the cat (Jones and Powell, 1968a) and monkey (unpublished observations) projects to the premotor cortex, area 6, and it is here that the topographic parcellation begins to break down. Area 6 also receives direct or indirect projections from the cortical auditory and visual systems as well as from the prefrontal and temporal cortex (Kuypers et ai, 1965; our unpublished observations) and sends efferent fibres to area 4. Therefore, activity passing from SI to the motor cortex via this route, in contrast to that passing directly, or through SII, must be considerably modified. There thus appear to be several cortical pathways, each carrying somatic sensory information of varying levels of integration to the motor cortex: (1) Direct from each of the architectonic (and functional) subdivisions of SI, probably including area 3a; (2) from each of these subdivisions via SII; (3) from SI and SII via the supplementary motor area (a part of area 6); (4) from SI through areas 5 and 6. It is the last pathway which is open to the greatest number of influences from other sensory systems and to influences from the temporal and frontal lobes. This is not to say, of course, that the sole function of the latter pathway should be considered in terms of its relationship with the motor cortex.

21 CORTICAL ASSOCIATION CONNEXIONS 497 One of the most remarkable features of the extrinsic connexions of the somatic sensory cortex is the firm interlocking of topographic subdivisions. Only those parts of SI, SII and the motor cortex related to the same portion of the periphery are interconnected. This interlocking of topography is also found in the thalamic connexions, for only parts of SI and SII receiving fibres from a given part of the ventrobasal complex send fibres back to that part of the nucleus (Jones and Powell, 1968c, 1969a). To a certain extent, the same is true of the projections from SI to area 5 and from SI and SII to the supplementary motor area, though these are not reciprocal connexions and in the case of the projection of SI to area 5 there is a small amount of overlap. Area 5 in the cat has been equated (Jones and Powell, 1968a) with the "third somatic sensory projection area" of Darian-Smith, Isbister, Mok and Yokota (1966), which, as far as it has been studied, contains a detailed representation of the contralateral half of the body surface. There are grounds for considering that area 5 with its heavy, organized corticocortical projection from SI may also represent the "supplementary sensory area" described in man by Penfield and Jasper (1954) and in the squirrel monkey by Blomquist and Lorenzini (1965). The region described by these authors is in both cases situated on the medial surface of the hemisphere, immediately posterior to the leg area of SI, which is the situation of a large part of area 5. Area 5 in man, as in the macaque, actually extends beyond this region on to the dorsolateral surface, but it is here either very narrow and closely applied to area 2 or buried in the medial bank of the intraparietal sulcus (Brodmann, 1909). Allowing for this and for the individual variability which architectonic fields must undoubtedly display in different individuals, it seems reasonable that responses in the lateral part of area 5 could be missed or interpreted as being in SI itself. The latter is particularly possible in view of the fact that the topographic organization of area 5 is essentially continuous with that of SI. It is significant that no effects of stimulating Penfield's supplementary sensory area have been referred to the face and, similarly, no responses were recorded in the supplementary sensory area of the squirrel monkey to stimulation of the face (Penfield and Jasper, 1954; Blomquist and Lorenzini, 1965), for in both cases the part of area 5 receiving fibres from the face subdivision of SI should be situated on the lateral surface in or just above the intraparietal sulcus. Whether evoked responses in area 5 are mediated entirely by corticocortical fibres from SI or by these together with fibres ascending from the nucleus lateralis posterior of the thalamus (Le Gros Clark and Boggon, 1935; Walker, 1938; Jones and Powell, 1969a) cannot at present be answered. The projections of SI and SII to the supplementary motor area, though not as dense as those to other cortical areas, also display a considerable degree of topographical organization, fitting remarkably well into the topographic map illustrated by Woolsey (1958). The supplementary motor area forms a part of area 6 as denned by Brodmann (1909) and others, and a projection to a small part of area 6 was also described in the cat (Jones and Powell, 1968a). In the cat, it was suggested (Jones and Powell, 1968a) that this small region was the supplementary motor area, although

22 498 E. G. JONES AND T. P. S. POWELL its position was only tentative in that species. Unlike area 4, the supplementary motor area does not project back to the somatic sensory areas. The projection of SI and Sn to the supplementary motor area is the only example in the present study of a projection which does not completely fill an architectonic field. However, as Brodmann (1909) states that his subdivision of the frontal lobe was somewhat arbitrary, the supplementary motor area may display some subtle architectonic differences when compared with the rest of area 6. The somatic sensory cortex both SI and SII in receiving fibres from area 4, is decidedly different from the primary visual and auditory areas. All the subdivisions of these areas are interconnected but as far as is known, no other area of cortex projects into them (Hubel and Wiesel, 1965; Wilson, 1968; Garey, Jones and Powell, 1968; Diamond et al, 19686). This could indicate either that the somatic sensory system is fundamentally different from the visual and auditory, or that area 4 and the somatic sensory areas should be considered together as a single "sensorimotor" area related to the brain-stem and spinal cord,-rather than as independent functional units. In the latter case, however, the fact that area 4 receives fibres from area 6 would still make the organization of such a single area basically different from that of the auditory and visual areas. This problem might be resolved if the frontal eye fields were shown to send fibres to the visual cortex and if a small area of frontal cortex sent fibres to the auditory cortex. A number of points may also be made about the topographic subdivisions of SI. The results of the present study offer confirmatory evidence for Woolsey's (1952, 1958) postulate that the upper and lower parts of the trigeminal nerve representation, which appear to have been separated by the considerable expansion of the hand area in the primate (Woolsey, Marshall and Bard, 1942), are in fact tenuously connected by a narrow strip passing along the posterior border of SI behind the hand area. For example a lesion in the face area of the lower part of the postcentral gyrus causes degeneration throughout the face area and also in such a narrow strip passing up towards the postcentral sulcus. Woolsey (1958) also states that his map of SI is incomplete at its lower end but that evoked potentials may be obtained by stimulation of the tongue in this region. The present evidence, showing that the forward extension of areas 3, 1 and 2 below the motor cortex and in the frontal operculum has strong interconnexions with the head subdivisions of SI, SII and area 4, would support this suggestion. It seems likely, however, that these parts of areas 3, 1 and 2 also contain at least one of the cortical projection areas for taste nerve afferents (Benjamin, Emmers and Blomquist, 1968; Benjamin and Burton, 1968), and for afferents from the pharynx and other parts of the alimentary tract (Penfield and Rasmussen, 1950). A further small region situated in the head region of SI and apparently within area 2 is a projection area for vestibular afferents (Frederickson, Figge, Scheid and Kornhuber, 1966). From the present results, this area seems to receive the same cortical connexions as the rest of area 2. No lesions were placed specifically in it in the present study, but from the available evidence it appears to share the same efferent cortical connexions also.

23 CORTICAL ASSOCIATION CONNEXIONS 499 The results of the present study have also permitted an anatomical delimitation of the boundaries of SII. This has always been difficult in the monkey because the greater part lies buried in the lateral sulcus. On the basis of cortical connexions, SII occupies most of the superior bank of the lateral sulcus, from about the middle of the insula virtually to the posterior end of the sulcus. It encroaches slightly upon the posterodorsal aspect of the insula and also upon the lower bank of the lateral sulcus at the point, posterior to the insula, where the upper and lower banks reunite. There is a possibility that there is an overlap zone here between SII and the secondary auditory field, perhaps similar to that in the anterior ectosylvian gyrus of the cat (Berman, 1961). SUMMARY The ipsilateral cortical connexions of the somatic sensory areas have been studied in the rhesus monkey by means of the Nauta technique. The first (SI) and second (SII) somatic sensory areas are reciprocally connected in a topographically organized manner with one another and with the motor cortex, area 4. Each sends further fibres in an organized manner to the supplementary motor area, but only SI projects to the parietal cortex. The latter projection is heavy and restricted to the cytoarchitectonic field, area 5. This is probably the equivalent of Penfield's "supplementary sensory area" in man. Apart from area 4, no other cortical area sends fibres to the somatic sensory areas. Within SI the three cytoarchitectonic (and functional) subdivisions, areas 3, 1 and 2, are interconnected by intracortical association fibres which respect the broader topographic boundaries but, in crossing cytoarchitectonic boundaries, must link neurons with different functional attributes. There is evidence for considering that the transitional field between sensory and motor cortex, area 3a, is a fourth architectonic and functional subdivision receiving Group 1 afferents from skeletal muscle. Because all functional subdivisions of SI project to SII and because the latter's sole cortical outflow is to SI and the motor areas, it may be an area for integration of all sensory modalities at a relatively low level of cortical function. This work was supported by grants from the Medical and Science Research Councils, and was done during the tenure of a Nuffield Dominions Demonstratorship by E. G. J. on leave from the University of Otago, New Zealand. REFERENCES AiBRECHT, M. H., and FERNSTROM, R. C. (1959) A modified Nauta-Gygax method for human brain and spinal cord, Stain Technol., 34, BENJAMIN, R. M., and BURTON, H. (1968) Projection of taste nerve afferents to anterior opcrcular-insular cortex in squirrel monkey {Saimiri sciureus), Brain Res., Amsterdam, 7, , EMMERS, R., and BLOMQUBT, A. J. (1968) Projection of tongue nerve afferents to somatic sensory area I in squirrel monkey {Saimiri sciureus), Brain Res., Amsterdam, 7,

24 500 E. G. JONES AND T. P. S. POWELL BERMAN, A. L. (1961) Overlap of somatic and auditory cortical response fields in anterior ectosylvian gyms of cat, /. Neurophysiol, 24, BILGE, M., BINGLE, A.; SENEVIRATNE, K. N., and WHITTEIUDGE, D. (1967) A map of the visual cortex in the cat, /. PhysioL, Lond., 191,116P. BLOMQUIST, A. J., and LORENZINI, C. A. (1965) Projection of dorsal roots and sensory nerves to cortical sensory motor regions of squirrel monkey, J. Neurophysiol., 28, BRODMANN, K. (1909) "Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien dargestellt auf Grund des Zellenbaues." Leipzig: Barth. CLARK, W. E. LE GROS, and BOGGON, R. H. (1935) The thalamic connections of the parietal and frontal lobes of the brain in the monkey, Phil. Trans. R. Soc, B, 224, DARIAN-SMTTH, L, ISBISTER, J., MOK, H., and YOKOTA, T. (1966) Somatic sensory cortical projection areas excited by tactile stimulation of the cat; a triple representation, /. PhysioL, Lond., 182, DIAMOND, I. T., JONES, E. G., and POWELL, T. P. S. (1968a) Interhemispheric fiber connections of the auditory cortex of the cat, Brain Res., Amsterdam, 11, (19686) The association connections of the auditory cortex of the cat. Brain Res., Amsterdam, 11, FINK, R. P., and HEIMER, L. (1967) Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system, Brain Res., Amsterdam, 4, FREDERICKSON, J. M., FIGGE, U., SCHEID, P., and KORNHUBER, H. H. (1966) Vestibular nerve projection to the cerebral cortex of the Rhesus monkey, Expl Brain Res., 2, GAREY, L. J., JONES, E. G., and POWELL, T. P. S. (1968) Interrelationships of striate and extrastriate cortex with the primary relay sites of the visual pathway, J. Neurol. Neurosurg. Psychiat., 31, , and Powell, T. P. S. (1967) The projection of the lateral geniculate nucleus upon the cortex in the cat, Proc. R. Soc. B, 169, GUCKSTEIN, M., KINO, R. A., MILLER, J., and BERKLEY, M. (1967) Cortical projections from the dorsal lateral geniculate nucleus of cats, /. comp. Neurol., 130, Gun-LERY, R. W., ADRIAN, H. O., WOOLSEY, C. N., and ROSE, J. E. (1966) Activation of somatosensory areas I and II of cat's cerebral cortex by focal stimulation of the ventrobasal complex. In "The Thalamus," edited by D. P. Purpura and M. D. Yahr, New York: Columbia Univ. Press, pp HONGO, T., OKADA, Y., and SATO, M. (1967) Corticofugal influences on transmission to the dorsal spinocerebellar tract from hindlimb primary afferents, Expl Brain Res., 3, HUBEL, D. H., and WIESEL, T. N. (1962) Receptive fields, binocular interaction and functional architecture in the cat's visual cortex, /. PhysioL Lond., 160, , (1965) Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat, /. Neurophysiol., 28, , (1968) Receptive fields and functional architecture of monkey striate cortex, /. PhysioL, Lond., 195, JONES, E. G. (1967) Pattern of cortical and thalamic connexions of the somatic sensory cortex, Nature, Lond., 216, , and POWELL, T. P. S. (1968a) The ipsilateral cortical connexions of the somatic sensory areas in the cat, Brain Res., Amsterdam, 9, , (19686) The commissural connexions of the somatic sensory cortex in the cat, /. Anat., 103, , (1968c) The projection of the somatic sensory cortex upon the thalamus in the cat, Brain Res., Amsterdam, 10,

25 CORTICAL ASSOCIATION CONNEXIONS 501 JONES, E. G., and POWELL, T. P. S. (1969a) The cortical projection of the ventroposterior nucleus of the thalamus in the cat. Brain Res., Amsterdam, 13, , (19696) Connexions of the somatic sensory cortex of the rhesus monkey, n. Contralateral cortical connexions. Brain (in press).. KUYPERS, H. G. J. M., SZWARCBART, M. K., MISHMN, M., and ROSVOLD, H. E. (1965) Occipitotemporal corticocortical connections in the rhesus monkey, Expl Neurol., 11, LANDGREN, S., and SILFVENIUS, H. (1968) Cortical projection of Group I muscle afferents from the hindlimb, Ada physiol. scand., 73, 14A-15A. MACCHI, G., ANGELEW, F., and GUAZZI, G. (1959) Thalamo-cortical connections of the first and second somatic sensory areas in the cat, /. comp. Neurol., Ill, MATTHEWS, P. B. C. (1964) Muscle spindles and their motor control, Physiol. Rev., 44, MOUNTCASTLE, V. B. (1957) Modality and topographic properties of single neurons of cat's somatic sensory cortex, /. Neurophysiol., 20, MYERS, R. E. (1962) Transmission of visual information within and between the hemispheres: a behavioural study. In "Interhemispheric Relations and Cerebral Dominance." Edited by V. B. Mountcastle. Baltimore: Johns Hopkins Press, pp NAUTA, W. J. H., and GYGAX, P. A. (1954) Silver impregnation of degenerating axons in the central nervous system: a modified technic, Stain Technol., 29, OSCARSSON, O., and ROSEN, I. (1966) Short-latency projections to the cat's cerebral cortex from skin and muscle afferents in the contralateral forelimb, /. Physiol., Lond., 182, PANDYA, D. N., and VIGNOLO, L. A. (1968) Intcrhemispheric neocortical projections of somatosensory areas I and II in the rhesus monkey, Brain Res., Amsterdam, 7, PENFIELD, W., and JASPER, H. (1954) "Epilepsy and the Functional Anatomy of the Human Brain." Boston: Little., and RASMUSSEN, T. (1950) "The Cerebral Cortex of Man." New York: Macmillan. POWELL, T. P. S., and MOUNTCASTLE, V. B. (1959a) The cytoarchitecture of the postcentral gyrus of the monkey Macaca mulatto, Bull. Johns Hopkins Hosp., 105, , (19596) Some aspects of the functional organization of the postcentral gyrus of the monkey: a correlation of findings obtained in a single unit analysis with cytoarchitecture, Bull. Johns Hopkins Hosp., 105, ROBERTS, T. S., and AXERT, K. (1963) Insular and opercular cortex and its thalamic projection in Macaca mulatto, Schweizer Arch. Neurol. Neurochirg. Psychiat., 92, ROSE, J. E., and MOUNTCASTLE, V. B. (1959)'Touch and Kinesthesis. In American Physiological Society "Handbook of Physiology," Section I: Neurophysiology. Edited by J. Field, H. W. Magoun and V. E. Hall. Washington: American Physiological Society, pp THOMPSON, R. F., JOHNSON, R. H., and HOOPES, J. J. (1963) Organization of auditory, somatic sensory, and visual projection to association fields of cerebral cortex in the cat, /. Neurophysiol, 26, VASTOLA, E. F. (1961) A direct pathway from lateral geniculate body to association cortex, /. Neurophysiol., 24, WALKER, A. E. (1938) "The Primate Thalamus." Chicago: Univ. Chicago Press. WERNER, G., and WHTTSEL, B. L. (1968) Topology of the body representation in somatosensory area I of primates, /. Neurophysiol, 31, WILSON, M. E. (1968) Cortico-cortical connexions of the cat visual areas, /. Anat., 102, , and CRAGO, B. G. (1967) Projections from the lateral geniculate nucleus in the cat and monkey, /. Anat., 101,

26 502 E. G. JONES AND T. P. S. POWELL WOOLSEY, C. N. (1952) Patterns of localization in sensory and motor areas of the cerebral cortex. In Milbank Memorial Fund, The Biology of Mental Health and Disease. London: Cassell, pp (1958) Organization of somatic sensory and motor areas of the cerebral cortex. In "Biological and Biochemical Bases of Behavior." Edited by H. F. Harlow and C. N. Woolsey. Madison: Univ. Wisconsin Press, pp , MARSHALL, W. H., and BARD, P. (1942) Representation of cutaneous tactile sensibility in the cerebral cortex of the monkey as indicated by evoked potentials, Bull. Johns Hopkins Hosp., 70, LEGENDS FOR PLATES PLATE XXIX FIG. 3. A, showing fibre and terminal degeneration in the cortex of SII following a lesion of SI. Fink-Heimer technique X38O. B, showing fibre and terminal degeneration in SI following a lesion of SII. Fink-Heimer technique x 380. c, fine degenerating axons caused by a lesion in the immediate vicinity and running in the molecular layer just beneath the pia mater. The surface of the brain is to the left. Nauta-Gygax technique X 600. D, coarse fibre and terminal degeneration in area 5 following a lesion in SI. Nauta-Gygax technique x PLATE XXX FIG. 4. A, fibre and terminal degeneration in SI caused by a lesion in the motor cortex (area 4). Fink-Heimer technique X 580. B, degeneration in SII, in the same brain from which A was taken. Fink-Heimer technique x 580. c, sparse axonal degeneration in the supplementary motor area consequent upon a lesion in SI. Nauta-Gygax technique x 670. (Received 3 January 1969)

27 PLATE XXIX FIG. 3. 7b illustrate article by E. G. Jones and T. P. S. Powell.

28 PLATE XXX te a 9, (; FIG. 4. To illustrate article by E. G. Jones and T. P. S. Powell.