Functional relationship between somatosensory cortex and specialized afferent pathways in the monkey

EXPERIMENTAL

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Functional Relationship between Somatosensory Cortex and Specialized Afferent Pathways in the Monkey ARTHUR

S. SCHWARTZ’

Barrow Neurological Institute, 350 West Thomas Road, Phoenix, Arizona 85013 Received February 18, 1982; revision received August 13, 1982 Previous work showed that the primate dorsal funiculus (DF) was necessary for tactile discrimination which entailed movement. The extra-DF spinal afferent fibers, by contrast, were sufficient for discrimination of tactile stimuli which did not require movement. This study investigated the association between various cortical regions and the specialized tactile roles of the separate alTere.nt systems.Monkeys learned two sets of tasks, one of which was dependent on DF integrity, and the other was capable of mediation by the extra-DF pathways. The cortical distribution and processing of DF and extra-DF information has been defined here by whether or not these tasks were affectedby lesions in the respective regions. Lesions in area 3b led to impairment of both tasks, but more severe and longer-lasting impairment of the DF tests. Lesions in areas I, 5, or 7 were without effect on either type of function. Ablation of the forelimb region in area 2 selectively damaged only the DF discriminations. These results, in combination with the results of others which are considered here, suggest that (i) both the DF and the extra-DF tactile information converge into area 3b; (ii) the extra-DF information is then projected difisely to widespread regions of the cortex which enables it to survive limited parietal ablations; and (iii) the DF information is transmitted compactly to a focal region in area 2. INTRODUCTION

In the tactile modality, perception of the geometric features of certain objects can be enhanced by movement over time, in contrast to an object whose features can be perceived immediately on contact. For example, a horizontal or curved edge may be easily distinguished from a vertical or straight edge after a brief presentation to the finger tips, but the accurate Abbreviations: DF-dorsal funiculus, IPS-intraparietal sulcus. ’ This work was supported in part by U.S. Public Health Service grant NS-057 15. I thank Dr. Eduardo Eidelberg, P. Marchok, C. Hedin, A. Perey, C. Kreinick, and B. Woolf for their valuable assistance. 316 0014-4886/83/020316-13$03.00/0 Copyright 0 1983 by Academic Press, Inc. All rights of reproduction in any form reserved.

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recognition of one cookie-cutter pattern from another is greatly facilitated after continuous movement of the edges or the fingers (18). The term “spatiotemporal” has been adopted to characterize those stimuli which require movement for efficient perception. An earlier study from this laboratory utilized two sets of tasks-one whose discrimination emphasized the need for movement and one which needed no movement-and found that the primate dorsal funicul~ (DE) played a critical role in spatiotemporal discrimination. By contrast, discrimination of nonspatiotemporal tasks (i.e., requiring no exploratory movements) survived combined transections of the DF, spinothalamic, and spinocervical systems (1). The two types of tasks serve not only to differentiate the tactile role of the DF compared with the extra-DF systems, but may also serve as “tracers” for determining the cortical disposition of these two aBerent systems. In this report the suggested cortical distribution of DF and extra-DF tactile information is defined by whether or not these functions are afkcted by lesions in the respective zones. The question asked here was are the cytoarchitectonic regions of the primate somatosensory cortex specialized for decoding and processing of the spatiotemporal information transmitted by the DF on the one hand, and the nonspatiotemporal information carried by the extra-DF pathways on the other7 Brodmann areas 1 and 2 contain cells that are selectively responsive to direction of movement on the skin (4, 16); regions rich in such cells would be expected to be important for performance of the spatiotemporal tasks exemplifying DF function. The posterior parietal lobe, especially area 5, also contains direction-sensitive cells ( 16) and receives projections from area 2 (6, 7). The participation of areas 5 and 7 in tactile discrimination has been demonstrated mainly by total, bilateral ablation of these regions; unilateral or subtotal lesions result in only mild tactile deficits [( 12, 19); for recent review, see (lo)]. The different roles of the various subdivisions of the primate somatosensory cortex in tactile discrimination were studied by Randolph and Semmes (15), Semmes and Turner (19), and by Carlson (2). Most if not all the data are based on the use of large lesions, and there has been little attempt to relate cortical functions to the separate types of cutaneous a&rent input as mediated by the DF and extra-DF systems. The results reported here suggest a dissociation of these inputs at the cortical level as well as their relationship to the various cortical subdivisions. METHODS Twenty-one young stump-tailed macaques (Mucucu arc&ides) and two rhesus (iUucucu muluttu) of either gender were used. They weighed 2.2 to 3.8 kg at the start of the experiment, and were fed and watered ad Zibitum, except that solid food was restricted when necessary to motivate performance

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during testing. Some animals, especially the sham-operated controls, underwent more than one surgical procedure. The hand contralateral to the lesion (or sham-operation) was tested both before and after surgery. The apparatus and procedure for testing were adopted from our earlier studies; for further details see (1, 17). Briefly, the monkeys were contained in a cage with bars and a sliding opaque door. When the door was raised, the monkey could reach through the bars into a test box containing the tactile discriminanda. The latter consisted of two sets of materials: (i) pairs of rods whose tactile qualities could presumably be discriminated by immediate and static touch and did not require exploratory movements [termed the “rod” problems, see (l)]; and (ii) pairs of plastic disks into which geometric patterns were excavated so that active haptic exploration was required in order to discriminate between them (termed the “disk” problems). Two rod subtests consisted of differences in roughness (40 vs. 60 or 80 grade sandpaper), another consisted of a square- vs. a hexagonal-shape rod, and the fourth was vertical vs. horizontal grooves. The diameter of the sandpaper rods was 11 mm; each plane surface of the hexagon and square rods was 6 mm and 10 mm, respectively, and the diameter of the grooved rods was 12 mm. All were 32 mm long. Informal observations on human observers had indicated that the rod discriminations could be quickly learned after brief applications of the stimuli to the fingers, and without any exploratory movements. This includes the square-hexagon problem which, because of the difference in size of their surfaces, could be discriminated by motionless touch. The relevant point here is that the rod differences were readily perceived by monkeys with DF, or spinothalamic, or spinocervical, or combined transections of these afferent pathways (1, 17). The disk problems consisted of (i) a large triangle versus a small circle, (ii) large triangle vs. large circle, (iii) triangle vs. teardrop figure, and (iv) circle vs. oval. The patterns were excavated into plastic disks 40 mm in diameter. These disk problems revealed severe impairment after DF transection but not after spinothalamic or spinocervical lesions: the information necessary for discrimination of the disks is therefore presumed to be carried exclusively by the DF. For further details, see (1). The rods were mounted vertically on sliding blocks so that a pull on a rod activated a switch for the relevant reinforcer. The disks were attached to platforms which, when depressed, likewise activated the relevant reinforcer. The discriminanda in the test box were presented side-by-side, separated by a partition and visually isolated by screens and baffles. The left-right position of the stimuli were varied according to the Gellerman series. Criterion for discrimination was defined as 18 correct selections in two consecutive blocks of 10 trials each. If a monkey did not attain criterion of 90% correct after 1000 trials, the next problem was presented.

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An evaluation of motor function was obtained by three motor tasks: (i) the percentage of 4-mm food pellets retrieved from grooves in a turntable which moved past the monkey at three different speeds (rotary test); (ii) the time required to retrieve a pellet from a shallow and a deep notch with two fingers (digit control test); and (iii) the time to open a plastic puzzle box which required a t&d sequence of operations with one hand. The motor tests were usually administered before the block of disk problems, both before and after surgery, and were continued until the scores stabilized over a 3day period. Upon completion of the test battery the monkeys were anesthetized with sodium pentobarbital and underwent surgery for selective cortical ablation by subpial suction. A bone flap was turned and replaced when feasible. Cortical tissue was removed from various regions of the parietal cortex using the central, intraparietal, postcentral, and lateral sulci as landmarks. The animals were retested after a recovery and physical exercise period of from 1 to 3 weeks. At termination of the experiment they were perfused with Formalin under general anesthesia. The brains were photographed, and spec imens imbedded in pa&Tut, sectioned at 40 pm, and stained with thionin. The cytoarchitectonic maps of Jones et al. (6) were used in defining the boundaries of the lesions in areas 3b, 1, 2, 5, and 7. RESULTS

E&c& of Sham Lesions. A control group of eight animals was tested before and after sham operations. They learned the rod and disk problems in 304 and 870 mean trials, respectively. Despite this difference in initial leaming, postoperatively they scored about the same on the two types of problems (Fii. l), suggesting that the rods and disks were originally learned and could be recalled to a relatively equal level of proficiency. Eficts of Lesions in Area 3b. Five monkeys underwent ablation of the forelimb region of area 3b (group 3b). Their preoperative learning did not differ significantly from that of the control group (Fig. 1). Postoperatively, group 3b was significantly impaired in both problems (for rods, P < 0.02; for disks P < 0.001, Mann-Whitney U test, two-tailed). &cause a cut-off point of 1000 trials was arbitrarily set for each subproblem, the data in Fig. 1 do not completely reflect the relative di5culties in performing the two types of tasks by this group. The animals with the least damage to the hand area of area 3b (TAL, DGR, SPR, Fii. 2) showed some sparing of the rod discriminations, passing all the rod problems in from 190 to 1240 trials, while remaining at chance levels on 83% (or 10 of a total of 12 tests for the three animals) on the disks. The other two monkeys with the most extensive damage to area 3b (DAL, RHR) failed five of a total of

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4ooa RODS

1

Shams

GD

GD

Go

GD

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1000 l-

O--Sk 3b

-_tl, Gp 1

GP 2

Gp 5

Gp i

FIG. 1. Mean number of preoperative (horizontal lines) and postoperative trials (vertical bars) presented to each group on four rod tests and four disk tests. A test was ended if the monkey did not attain criterion for discrimination in 1000 trials; a score of 1000 was then assigned for that test.

eight rod subtests and all eight of the disks. (Both failed the 40-60 sandpaper and the horizontal-vertical tasks; RHR also failed the square-hexagon task.) These data suggest that disk discrimination suffered more impairment than rod discrimination. On the motor tasks, only one monkey in the group (DAL) was significantly impaired on any of the subtests (rotary task and digit control); damage to area 4 was also noted. The poor postoperative motor control of the digits could account for this animal’s poor performance on the rods (2650 trials, including failure on two tests) and on the disks (all problems failed). All of the other monkeys in group 3b showed motor scores well within their preoperative ranges, including the other three monkeys who also failed all the disks. There was no significant correlation between performance on the sensory and the motor problems for the group as a whole.

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FIG. 2. Representation of lesions of monkeys in group 3b. The anterior and posterior banks of the central sulcus are indicated by the areas between the heavy dotted lines. Deep lesions extending into the white matter are shown in black superficial ablations involving only surface gray matter are shown by stippling. In this and following &ures, the extent of sulcal lesions was determined from sections across the sulcal axis, and the extent of surface lesions reconstructed by tracing photographs of each brain.

E&et of Lesions in Area 1. Lesionswere placed in area 1 of three monkeys (group 1, Fig. 3). Two of these showed no deficit on any test. The third monkey (NRR), also sustained slight damage to area 3b and failed one disk problem (large circle-triangle). A Mann-Whitney U test revealed no significant difference between group 1 and the controls in rod or disk performance; a further analysis revealed that the apparent impairment on the disks (Fig. 1) was entirely due to the results by NRR with area 3b involvement. On the motor tasks, the efficiency of NIW was marginally worse than preoperative performance on the digit test; all the other tests were performe4I as well or

FIG. 3. Representation of lesions in group 1. Areas of cortical tissue damaged or missing are shown in black.

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better than preoperatively. In summary, the results in group 1 suggest that relatively small lesions in area 1 have only a mild, if any, effect on rod and disk discrimination. Effects of Lesions in Area 2. Partial ablations of area 2 were undertaken in nine monkeys (group 2, Fig. 4). Preoperative learning of the rod and disk problems did not differ significantly from the controls or group 3b. Postoperatively two animals (CZR and PNR) failed one rod subtest (the horizontal-vertical); all the other rod tests were completed by group 2 at about the same rate as the controls. By contrast, 44% (16/36) of the disk tests were failed and the number of trials to complete postoperative testing on the disks was significantly greater than required by controls (P < 0.02). The extent of deficit on the disks tended to be related to the extent and locus of the lesion. The lesions in the three monkeys (HEL, NDL, PEL) with the least damage to area 2 involved primarily the surface gray matter between the central sulcus and the intraparietal sulcus (IPS) without invading the anterior bank of the latter or the white matter underneath (Fig. 4). These three animals showed normal postoperative savings scores on both the rods and disks (55% and 33%, respectively). Three of the four monkeys with the most damage to area 2 (CAL, ESL, KYR) averaged 290 trials to learn all four rod problems preoperatively and 213 trials postoperatively, and they averaged 320 trials on the disks preoperatively but failed 75% (9/12) of the disk problems postoperatively (mean score, 3420). These three lesions, which effectively impaired disk discrimination while leaving the rods intact, typically included the region near the lateral end of the IPS, penetrating the white matter underlying the posterior surface of area 2 or invading the anterior bank of the sulcus. The fourth animal with a large lesion (PNR) sustained similar damage to area 2 and also to area 7; PNR scored 110 (preoperative) and 1220 (postoperative) on the rods, and 530 preoperative on the disks but failed all the disks postoperative. The lesions in the remaining two monkeys (CZR, LVR) in group 2 were slightly less extensive than in the subgroup above, but more importantly showed some sparing of the region in area 2 near the lateral end of the IPS. On the rods, postoperatively CZR failed one test as noted earlier, and completed the rest in normal time. LVR had some transient difficulty with the same horizontal-vertical (rod) problem, and also finished the remainder of the rods in normal time. On the disks, postoperatively CZR and LVR failed two (small circle-large triangle; large circle-triangle) and one (large circle-triangle) problem respectively, while completing the rest in normal time. Comparing the four monkeys in group 2 whose ablations included the region near the lateral tip of the IPS (CAL, ESL, KYR, PNR) with the five monkeys (CZR, HEL, LVR, NDL, PEL) whose lesion spared much of this region, the results indicate impairment on one rod subtest by CZR and PNR; all the other rod problems were easily

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FIG. 4. Representation of lesions in group 2. The anterior and posterior banks of the intraparietal suleus are indicated by the areas between the heavy dotted lines. Deep leaions penetrating to the white matter are shown in black, superticial lesions with incomplete removal of gray matter are shown by stippling.

discriminated. On the disks, however, 8 1% ( 13/ 16) were failed by the former as compared with 15% (3/20) by the latter animals. In summary, the results of group 2 show (a) no effect on rod or disk discrimination after subtotal, supe&ial lesions in area 2; (b) mild impairment on the rods with large area 2 ablations; and (c) severe and selective impairment on the disks when the area 2 ablation included the region near the lateral tip of the IPS.

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On the motor tests only PNR was significantly impaired (P < 0.05). A rank order correlation between group 2’s performance on the rods and the various motor tasks yielded a barely significant correlation (P < 0.05) with the puzzle box only; otherwise, there was no relationship between the rod and disk scores on the one hand and motor scores on the other. Furthermore, monkey CZR which failed one rod problem and two disk problems, and monkeys ESL and KYR which had failed all four disk problems, showed no change whatever on any of the motor tasks. E’cts of Lesions in Area 5. Four monkeys (CRL, JAL, HNR, NDL, group 5) received lesions in the zone of area 5 which receives projections from the forelimb representation in area 2 (6). The lesions in group 5 variably extended into area 2, but none came near the lateral part of the IPS (Fig. 5). The lesion in JAL barely invaded area 5. Monkey NDL had previously undergone surgery for removal of anterior area 2 and had shown no behavioral deficits (see Fig. 4); a second lesion was placed in area 5 which included the upper halves of both banks of the IPS and extended into area 7. All four monkeys

FIG.

5. Representation of lesions in groups 5 and 7. See Fig. 4 for explanation.

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showed normal postoperative savings on both the rods and disks (Fig 1). Initially motor control was clearly af&cted, but after the usual physical therapy and retmining th6y were performing the motor tests at their preoperative levels before starting the disks. Eficts of Subtotal and Combined Lesions in Area 7. Four monkeys, including two in group 5 (HNR, NDL) sustained damage to the inferior parietal lobule (Fig. 5). Only one animal @AL) failed one of the disk subtests (triangle-teardrop); all the other tasks; both rods and disks, were relearned with normal retention. On the motor tests all four monkeys soon performed at their preoperative levels. Thus, other than the failure by LAL on one disk test, lesions in areas 5 and 7 had no effect on rod or disk discrimination (Fig. 1). DISCUSSION Area 3b is generally considered to be the main cortical entry point for ail tactile signals from the skin. This concept is derived in part from the fact that area 3b receives a heavy projection from the ventroposterior thalamic nucleus in contrast to the more posteriorly situated areas 1 and 2 which receive only sparse projections (5, 8). The concept entirely predicts the findings reported here and by others (15, 19)-extensive damage to area 3b produces severe deficits in a wide variety of tactile tasks. A significant amount of extra-DF information, in contrast to DF information, however, apparently escapes destruction by lesions in area 3b. This partial dissociation is implied by the relative sparing of 75% of the rod tests but only 10% of the disks in group 3b. A differential role for area 1 in processing DF and extra-DF information may also be proposed alter a consideration of the present results in combination with those of Randolph and Semmes (15), Semmes and Turner ( 19), and Carlson (2). Those authors utilized two tasks which constitute rodtype problems (sandpaper differences, horizontal versus vertical grooves) and two which, according to our previous analysis (l), may constitute disk or spatiotemporal discriminations (square-diamond, concave-convex). The qualifications of the latter as spatiotemporal tasks incorporating movement is suggested by the observation of Semmes and Turner (19) that their monkeys could discriminate these objects by stroking certain edges of the stimuli. The lesions in area 1 imposed by the Semmes group and by Carbon resulted in significant impairment of rod-type discriminations but had no effect on disk-type discriminations. Except for the most difficult sandpaper problem presented by Carlson to her two monkeys, however, all lesion studies, including the present one, show that the rod discriminations were eventually performed successfully. In the animals studied here, area 1 lesions produced

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no deficit on the rods, agreeing with Carlson’s “easy” and “moderate” roughness (rod problems) results. The proficiency of group 1 on the rods, in contrast to the preparations studied by Semmes and her colleagues, may be due in part to the smaller lesions used here. In summary, there is evidence that area 1 participates in extra-DF tactile functions, especially when fine discriminations are involved, but its integrity is not crucial because such functions can still be performed after area 1 ablation. Tactile functions of the DF type, on the other hand, are unaffected by lesions restricted to area 1. Ablation of the hand region in area 2 selectively destroyed disk discrimination while leaving rod discrimination intact. These results agree with the findings of the Semmes group and Carlson when one presumes that their concave-convex and square-diamond problems may represent spatiotemporal tasks. A comparison of the effects of cortical lesions in areas 1 and 2 on the two types of tactile function suggest that the representation for disk discrimination is focal and restricted to the hand region of area 2 near the lateral end of the IPS, as indicated by the fact that only the ablations of this region were effective, and that the disk deficit was severe and long-lasting if not permanent. By contrast, the various studies show survival of most rod discriminations after area 1 lesions, which suggests that rod discrimination is widely represented in the cortex and not confined to area 1. Further support for this view was provided by Semmes and Turner (19); they reported almost twice as much difficulty with roughness discrimination after combined lesions of areas 1 and 2 as after lesions to each area alone. In addition, normal rod discrimination in our earlier monkeys after combined section of the DF, spinothalamic, and spinocervical pathways (1, 17) implied that the relevant tactile information was mediated by extra-lemniscal systems. The diffuse cerebral projections of the extra-lemniscal system (11) may well account for the survival of rod discrimination after extensive cortical lesions. No deficit on either the rods or disks was observed after subtotal ablation of areas 5 or 7. Several authors have assigned an important role in tactile discrimination to areas 5 and 7 [for recent reviews, see (3, 10, 13)]. Most, if not all, studies which show tactile impairment of rod-type tasks have involved large lesions in the posterior parietal lobe and encompassed both areas 5 and 7. A comparison between the disk problems and the various tactile tests used by earlier authors is difficult because it is not known which of the latter would be affected by DF section. The disk-type tests (square-diamond, concave-convex) used by Semmes and Turner, however, were not significantly affected by ablation of areas 5 and 7 combined, whereas roughness discrimination (i.e., rod test) was markedly impaired (19). Those results agree with the concept that only the extra-DF information is distributed over a widespread cortical region. The lack of any clear effect on spatiotemporal (disk) discrimination by

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area 5 lesions might have been predicted alter consideration of certain relevant data. Area 5 has few cells sensitive to movement on the skin, compared with area 2, but is rich in cells responsive to contralateral and/or ipsilateral stimulation of joint receptors (4, 13, 16). We have shown elsewhere in the human that participation by the deep receptors is not necessary in tactile perception of spatiotemporal features (18). Possibly one may have expected some gross deficit on the motor tests in group 5. Indeed, acute focal cooling of area 5 (20) may impair grasping (but not reaching). The extensive postoperative physical therapy and retraining regimen may explain the normal performance on the motor tests by group 5. The data discussed here suggest a dissociation in the cortical distribution of DF and extra-DF tactile information, reflecting a segregation of tactile information at the spinal level (1). It is proposed that both systems project primarily to area 3b where the DF function is compactly represented and severely impaired by a given lesion, whereas the extra-DF function suffers less damage, possibly because of diffuse projections to other cortical areas. The proposed dissociation also pertains to area 1 which, like area 3b, contains a complete and separate representation of the hand (9, 14). The frequent survival of rod discrimination after area 3b ablation and the moderate impairment on these tasks after area 1 ablation (2, 15, 19) suggests that area 1 constitutes at least one zone for extra-DF projection and processing; DF information, on the other hand, apparently bypasses area 1 and projects to area 2. There is no indication that, apart from area 3b, DF tactile information as represented by the disks is processed in any cortical area other than area 2, whereas extra-DF information may be transmitted to area 2 but this region is not important for rod discrimination. The present data do not elucidate the precise roles, if any, of areas 5 or 7 in tactile discrimination. Finally, it is proposed that the detection of the direction of movement on the skin, for which the DF is essential (21) and which is well represented in area 2 (4, 16), may be a most critical component in tactile perception of such forms as the disks. REFERENCES 1. AWLAY, A., AND A. S. SCHWARIZ. 1975. The role of the dorsal tkniculus of the primate in tactile discrimination. Exp. Neural. 46: 315-332. 2. CARLWN, M. 1980. Characteristics of sensory deficits following lesions of Brodmann’s Areas 1 and 2 in the postcentral gyms of Mucucu mulatta. Brain Res. 204: 424-430. 3. DARIAN-SMITH, I., K. 0. JOHNSON,AND A. M. GOODWIN. 1979. Posterior parietal cortex: relations of unit activity to sensorimotor function. Ann. Rev. Physiof. 41: 141-157. 4. HW&RINEN, J., AND A. POIUNEN. 1978. Movement-sensitive and direction and orientation selective cutaneous receptive fields in the hand area of the post-central gyrus in monkeys. J. Physiol. (London) 283: 523-537. 5. JONES, E. G., AND H. BURTON. 1976. Areal dilfkrences in the laminar distribution of tha-

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lamic atIerents in cortical fields of the insular, parietal and temporal regions of primates. J. Comp. Neural. 168, 197-248. 6. JONES,E. G., J. D. COULTER, AND S. H. C. HENDRY. 1978. Intracortical connectivity of architectonic fields in the somatic sensory, motor and parietal cortex of monkeys. J. Comp. Neurol. 181: 291-348. 7. JONES, E. G., AND T. P. S. POWELL. 1969. Connections of the somatic sensory cortex of the rhesus monkey. I. Ipsilateral cortical connections. Bruin 92: 477-502. 8. JONES, E. G., AND T. P. S. POWELL. 1970. Connections of the somatic sensory cortex of the rhesus monkey. III. Thalamic connections. Brain 93: 37-56. 9. RAAS, J. H., R. J. NELSON, M. SUR, C. S. LIN, AND M. M. MERZENICH. 1979. Multiple representations of the body within the primary somatosensory cortex of primates. Science 204: 521-523. IO. LYNCH, J. C. 1980. The functional organization of posterior parietal association cortex. Behav. Brain Sci. 3: 485-534. 11. MEHLER, W. R., E. FEFIXMAN, ANLI W. J. H. NAUTA. 1960. Ascending axon degeneration following anterolateral cordotomy. Brain 83: 7 18-750. 12. MOFFETT, A. M., AND G. ETTLINGER. 1970. Tactile discrimination performance in the monkey: the effect of unilateral posterior parietal ablations. Cortex 6: 47-67. 13. MOUNTCASTLE, V. B., J. C. LYNCH, A. GEORCWOULOS, H. SAKATA, AND C. ACUNA. 1975. Posterior parietal association cortex of the monkey: command function for operations within extrapersonal space. J. Neurophysiol. 38: 871-908. 14. NELSON, R. J., M. SUR, D. J. FELLEMAN, AND J. H. KAAS. 1980. Representations of the body surface in postcentral parietal cortex of Macaca jkwicularis. J. Comp. Neurol. 192: 61 l-643. 15. RANDOLPH, M., AND J. SEMMES. 1974. Behavioral consequences of selective subtotal ablations in the postcentral gyrus of Macaw mulatta. Bruin Res. 70: 55-70. 16. SAKATA, H. 1975. Somatic sensory responses of neurons in the parietal association area (Area 5) of monkeys. Pages 350-361 in H. H. KORNHUBER, Ed., The Somatosensory System. Thieme, Stuttgart. 17. SCHWARTZ, A. S., E. EIDELBERG, P. MARCHOK, AND A. A~ULAY. 1972. Tactile discrimination in the monkey after section of the dorsal funiculus and lateral lemniscus. Exp. Neural. 37: 582-596. 18. SCHWARTZ,A. S., A. PEREY, AND A. A~ULAY. 1975. Further analysis of active and passive touch in pattern discrimination. Bull. Psychon. Sot. 6: 7-9. 19. SEMMES, J., AND B. TURNER. 1977. Effects of cortical lesions on somatosensory tasks. J. Invest. Dermatol. 69: 181-189. 20. STEIN, J. F. 1976. The effect of cooling parietal lobe areas 5 and 7 upon voluntary movement in awake rhesus monkeys. J. Physiol. (London) 258: 62P-63P. 2 I. VIERCK, C. J. 1974. Tactile movement detection and discrimination following dorsal column lesions in monkeys. Exp. Bruin Res. 20: 331-346.