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The Effects of Unilateral or Bilateral Removals of the Second Somatosensory Cortex (Area SII): A Profound Tactile Disorder in Monkeys
THE EFFECTS OF UNILATERAL OR BILATERAL REMOVALS OF THE SECOND SOMATOSENSORY CORTEX (AREA SII): A PROFOUND TACTILE DISORDER IN MONKEYS H. S. Garcha and G. Ettlinger (Institute of Psychiatry, London)
INTRODUCTION
Ridley and Ettlinger (1976, 1978) have reported a severe and lasting disorder of tactile performance in monkeys with bilateral removals of the second somatosensory projection cortex (area SII). Those removals were to include cortex identified as SII both electrophysiologically (Woolsey, 1958) and anatomically (Jones and Powell, 1970) Subsequently, Burton and Jones (1976) have re-defined the position and extent of SII in the monkey by anatomical methods. We have therefore studied 2 further groups of animals, all with removals intended to involve only the smaller region of cortex recently designated as SII (Burton and Jones, 1976). Three animals were given unilateral and 3 animals bilateral removals. Unexpectedly, the animals with unilateral ablations of SII were massively impaired.
MATERIALS AND METHOD
Subjects
Nine previously untrained pre-pubertal rhesus monkeys, Macaca mulatta (2.2 3.1 kg) were divided into 3 comparable groups on the basis of their performance on a tactile task (stage 1). Three animals had the area newly designated as SII (Burton and Jones, 1976) removed bilaterally (animals BSII-1-3); 3 had this region removed unilaterally (animals USII-1-3); and 3 served as unoperated controls (C-1-3). Unilateral removals were made from the hemisphere contralateral to the pre-operatively preferred hand (stage 1). Histological verification of the actual extents of the removals is not available since all 9 animals will continue to be trained for another year. Training procedures
All procedures have remained exactly as already described (Ridley and Ettlinger, 1976, 1978). In brief, training was carried out in a WGTA for peanut reward, with 40 trials given daily, 4 or 5 days each week. Cortex (1978) 14, 319-326.
H. S. Garcha and G. Ettlinger
320
RESULTS
The sequence of training and the results are shown in Tables I-III. The one-tailed Mann-Whitney V-test was used for all comparisons. TABLE I
Performance by 3 Groups of Monkeys on Tasks Described in Text
Animals
Stage of training
With preferred hand
Cylinder and Sphere 1 Pre-operative New Learning
2 Post-operative 1st Retention
3 Concave and Convex New Learning
4 Pillar and Diabolo New Learning
USII-1 USII-2 USII-3
130 250 120
130 330 50
350 110 30
lOOOF lOOOF 270
BSII-1 BSII-2 BSII-3
230 100 130
170 60 140
80 80 500
lOOOF lOOOF lOOOF
C-1 C-2 C-3
130 180 200
0 0 0
90 90 70
220 100 190
Designation of animals as in text. Figures refer to the number of trials required to reach standard levels of performance: stage 1, 180 correct responses in 200 trials; stage 2, 90 correct responses in 100 trials; stages 3 and 4, 72 correct responses in 80 trials. F indicates that the animal failed to reach the required level of performance in the indicated number of trials. TABLE II
Performance by .3 Groups of Monkeys on Tasks Described in Text
Animals
Stage of training With non-preferred hand
6 T and L New Learning
Bimanual motor tasks
7 Cone and Pyramid New Learning
8 Push-Pull New Learning
9 Press-Rotate New Learning
USII-1 USII-2 USII-3
570 lOOOF 500F
210 50 OF 500F
670 400 920
320 450 240
BSII-l BSII-2 BSII-3
620 130 lOOOF
lOOOF 500F 500F
260 510 390
160 490 260
200 320 400
90 40 80
640 210 560
330 970 300
C-1 C-2 C-3
The designations of animals and the meaning of the letter F as in Table I. The figures refer to the number of trials required to reach standard levels of performance: stages 6 and 7, 72 correct responses in 80 trials; stages 8 and 9, 90 correct responses in 100 trials.
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321
TABLE III
Performance by 3 Groups of Monkeys on Tasks Described in Text Animals
Stage of training
With preferred hand 10 Latch Box Problems New Learning I II III IV
11 Alternation New Learning
non-preferred Cylinder and Sphere 12 2nd Retention
13 Retention
USII-1 USII-2 USII-3
50 10 40
70 60 50
0 0 60
110 150F 150F
450 280 190
130 60 100
o(lOE) 20 500F
BSII-1 BSII-2 BSII-3
50 210 50
30 70 90
0 0 50
0 100 0
560 140 240
400 120 400
740 180 0(8E)
C-l C-2 C-3
120 30 260
70 80 10
60 50 0
30 30 10
340 520 320
0 40 0
o(3E) O(3E) o(2E)
The designations of animals and the meaning of the letter F as in Table 1. The figures refer to the number of trials required to reach standard levels of performance: stage 10, 18 correct responses in 20 trials; stages 11-13, 90 correct responses in 100 trials. Figures in brackets at stage 13 represent errors in initial 100 trials.
Stages 1 and 2 Animals were trained to discriminate with their preferred hand in the dark between a cylinder (2.5 cm diameter, 5.5 cm high) and a sphere (5.5 cm diameter) to 180 correct responses in 200 consecutive trials. The groups did not differ significantly on this task pre-operatively (stage 1). When, starting 13 days after surgery, they were retrained on the same task to 90 correct responses in 100 trials (stage 2), the bilateral animals (p < .05) and the unilateral animals (p < 0.5) were significantly impaired relative to the control animals. Already at this stage the mean score of the unilateral group, namely 170 trials, was somewhat greater than that of the bilateral group, namely 123 trials; whereas pre-operatively the difference between group means was only 14 trials. Both groups were somewhat less impaired than were the earlier (Ridley and Ettlinger, 1976) animals with presumably larger bilateral removals on the same task. (In the case of animals USII-l and USII-3 the lesser degree of impairment may be due to only these 2 animals being given 20 additional training trials before surgery, so that the interval between pre- and post-operative training would be exactly 13 days for all animals). Three animals reversed their hand preference as a result of surgery: BSII-3, USII-2 and USII-3.
322
H. S. Garcha and G. Ettlinger
Stages 3 and 4 After stage 2, animals were trained in the dark to 72 correct responses in 80 trials on 2 further tactile discrimination tasks, using their preferred hand: concave (0.8 cm high from 1.0 cm high) and convex (4.1 cm high from 3.0 cm high) blocks (3.0 cm X 3.0 cm) (stage 3); and pillar (3.0 cm X 3.0 cm X 1.0 cm at top and base; 1.0 cm X 1.0 cm stalk) and diabolo (3.0 cm diameter at top and base; 1.0 cm diameter at waist) with overall heights of 4.0 cm (stage 4). Stage 3 was easier (mean of 83 trials) than stage 4 (mean 170 trials) for the control animals, and the groups did not differ significantly at stage 3 (but at least one animal in each operated group seemed to be severely impaired). However, at stage 4 both operated groups were significantly (p < .05) impaired at learning in comparison with the control group. It is noteworthy that animal USII-l continued to prefer to use the hand contralateral to the unilateral removal until stage 11, and performed poorly at stages 2, 3 and 4. Animal USII-2 changed its preferred hand but performed poorly at stages 2, 3 and 4 with the hand ipsilateral to the removal. Animal USII-3 also changed its hand preference and performed within control limits at stage 3, and not far beyond at stages 2 and 4, with the ipsilateral hand. Stage 5 In order to evaluate tactile learning with their non-preferred hands, all animals were next adapted to restriction of the use of the preferred hand. A weighted rubber ball was attached by a chain and bracelet to one wrist. First, all animals were trained, while the non-preferred hand was restricted, to discriminate in the dark between a block (3.35 cm deep X 5.05 cm wide X 3.25 cm high) and spikes 0.2 cm nails set into hemisphere of 4.9 cm diameter) to 45 correct responses in 50 trials. No differences between the groups emerged and the data are not presented. Then they were trained to the same level of performance with the preferred hand restricted. (These learning scores with the second hand might be viewed as a measure of intermanual transfer.) All bilateral and control animals learnt in 0 or 10 trials. The unilateral animals required 20, 110 and 1000 + trials respectively (where + indicates failure to meet the required criterion). Each of these unilateral animals, unlike any control or bilateral animals, required more trials to learn with the second hand than with the first. The performance of the unilateral animals differed significantly (p < .05) from that of the other 2 groups.
Stages 6 and 7 Animals were next trained in the dark to 72 correct responses in 80 trials on 2 further tactile discrimination tasks, using their non-preferred
Tactile disorder in monkeys
323
hands. First,. they were required to discriminate between T (3.9 em deep, 4.0 em wide, bar width 0.6 em, bar height 1.0 em) and L (4.0 em deep, 1.9 em wide, bar dimensions as for T) (stage 6); and then between cone (3.0 em diameter at base, 4.2 em high) and pyramid (3.1 em sides at base, 4.2 em high) (stage 7). Stage 6 was more difficult (mean of 307 trials) than stage 7 (mean of 70 trials) for the control group. If task difficulty were a relevant factor then greater impairment would be expected at stage 6 than at stage 7. Nonetheless, only the unilateral group was significantly impaired (p < .05) in comparison with the control animals at stage 6, although 2 of the bilateral animals also performed poorly. At stage 7 the bilateral and unilateral groups differed significantly (p < .05) from the control group. However, in partial explanation for the greater impairment at stage 7 it must be noted that the results for performance at stages 5, 6 and 7 are not entirely independent. Thus animal USII-3 failed to learn within 1000 trials at stage 5 with the non-preferred hand, and subsequently failed with that hand at stages 6 and 7; likewise animals BSII-3 and USlf2 failed to learn at stage 6 and also failed at stage 7. (However, animals BSII-1 and 2 learnt at stages 5 and 6 but failed with the same hand at stage 7.) Steges 8 and .9 The animals of Ridley and Ettlinger (1976, 1978) were not required to learn any motor task. In the post-operative training of the present animals it was noted that movement of the fingers seemed "clumsy", both in palpating the objects and in opening the lids and retrieving rewards. Therefore all animals were required to learn 2 bi-manual motor skills previously described (Elliott, Ettlinger, Maccabe and Richardson, 1976): "push-pull" where the monkey is required to push a handle with one hand, and simultaneously pull another with the other hand to obtain a peanut reward (stage 8); and "press-rotate" where the monkey has to rotate a knob with one hand and simultaneously depress a lever with the other for peanut reward (stage 9). At stage 8 training was entirely in the light, but at stage 9 in the dark once the animals had partially learnt the component responses. There were no significant differences at either stage. Stage 10
The skill required at stages 8 and 9 was bi-manual coordination, but the movements were relatively coarse. Therefore, at stage 10 fine movements of at least one hand were required to solve the 5 graded latch-box problems described and illustrated in Elliott (1976). The problems were given exactly as in Elliott (1976), with a time limit of 30 sec per trial and in the light. There were no group differences on problems 1-3 but on
324
H. S. Garcha and G. Ettlinger
problem 4 the unilateral group was significantly (p < .05) impaired. Only 1 animal (C-3) learnt problem 5 so the data are not presented.
Stage 11 Next, the monkeys were trained on spatial alternation in the dark: a doubly-baited zero trial started each day's session of 40 trials; errors were corrected by delayed re-run trials which were included in the learning scores; intertrial interval was 6-7 sec. The 2 operated groups performed better than the control group.
Stages 12 and 13 The tactile discrimination task (cylinder and sphere) already trained pre-operatively (stage 1) and again first after surgery (stage 2) was retrained to 90 correct responses in 100 trials first with the preferred hand (stage 12), then after a replication of stage 5 with the non-preferred hand (stage 13). Both operated groups were significantly (p < .05) impaired at stages 12 and 13.
Summary of results There were no consistent impairments at motor learning or spatial performance; but there was significant defect, especially in the unilateral animals and then in both hands, on tasks requiring tactile learning and tactile retention. DISCUSSION
The lesio12S Detailed discussion must await histological verification at the conclusion of further training. However, it would seem likely prima facie that removals of the newly defined (Burton and Jones, 1976) second somatosensory projection area, although intended to be less extensive than the earlier removals (Ridley and Ettlinger, 1976, 1978) are sufficient to produce massive and lasting deficit. The surrounding tissue may also be partly involved in tactile performance, because the earlier (Ridley and Ettlinger, 1976) bilaterally lesioned animals were more impaired at their stage 2 (the same task) than the present bilateral animals at stage 2. The effect of destruction of underlying fibre tracts is uncertain: it is difficult to ensure total removal of the relevant SII cortex within the lateral fissure without damaging some non-cortical structures. The degree of defect in the unilateral group was unexpected. Again, caution is advisable in case, on histological verification, these lesions are
Tactile disorder in monkeys
325
toO large or too deep. However, it is already certain that only a single hemisphere was involved. All 3 unilateral animals were impaired with their preferred hand at stages 2 and 4, and 2 animals also at stage 3. The preferred hand in one of the animals was contralateral to the removal (Le. still the pre-operatively preferred hand); but in 2 other animals it was ipsilateral to the removal. So it would seem that unilateral removals of SII impair performance with both hands (since the one animal which did not change its hand preference was also impaired at stages 6 and 7 with the non-preferred, Le. ipsilateral, hand).
The behavioural alterations It was perhaps surprising that the bilateral removals of Ridley and Ettlinger (1976, 1978) would be followed by such severe and persisting disturbances. For, although more extensive than in this study, those lesions were small relative to most other lesions that produce behavioural defect in the monkey. Nonetheless, those behavioural alterations could have reflected damage to neural systems which, when intact, were themselves involved in the mediation of tactile learning and memory. This may still be a possible explanation for the present findings; but it would be necessary to suppose that each individual (i.e. left- or right-sided) SII region contributed to the tactile performance of both hands and yet could not function adequately in the absence of the opposite SII region. It seems more plausible to suppose that SII cortex (in addition to its other functions) sustains the adequate functioning of another somatosensory system; and that after a unilateral SII removal the neural system concerned with tactile learning and memory is functionally disrupted by an abnormal output from the remaining SII cortex which is no longer "in balance". On this view impairment after bilateral SII removals is due to the absence of normal sustaining inputs from the two SII regions to another system; impairment after unilateral SII removals (which may be more severe than after bilateral removals) is due to an abnormal input from the intact SII cortex to another system. This view of the origin of the defects after SII removals can be readily reconciled with the detailed behavioural findings. Performance on visual, motor and spatial tasks is intact, even in the dark. Tactile sensory capacities and weight discriminations were not impaired (Ridley and Ettlinger, 1976, 1978). The defect seems, on the available evidence, to involve only tactile learning, tactile retention and intermanual transfer (Ridley and Ettlinger, 1978). Such a disorder of learning and memory is likely to be a consequence of dysfunction of a system functionally separate and perhaps (but not necessarily) also anatomically separate from SII, rather than to ensue from loss of a system within SII cortex which in the intact monkey would itself
H. S. Garcha and G. Ettlinger
326
mediate tactile learning and memory. However, it remains unknown what kind of sustaining functions SII cortex possibly provides for tactile learning, just as it remains unknown how, for example, the mamillary bodies sustain verbal learning and memory in man.
SUMMARY
Three groups of monkeys were studied: one with bilateral removals of the second somatosensory projection cortex (SII); another with similar unilateral removals; and an unoperated control group. Both lesion groups were significantly impaired on tasks of tactile learning and tactile retention. However, there were no differences between groups on the great majority of tasks of motor learning, nor on spatial alternation in the dark. The animals with unilateral removals were generally impaired whether using the hand contralateral to or ispilateral to the removal. Acknowledgments. We are grateful to the MRC who supported this work; and to Dr. R. M. Ridley for comments on this paper.
REFERENCES BURTON, H., and JONES, E. G. (1976) The posterior thalamic region and its cortical projection in New World and Old World monkeys, ]. Camp. Neurol., 168, 249-301. ELLIOTT, R. C. (1976) Problem solving in cebus and rhesus monkeys, Bull. Psychonom. Soc., 7, 319-320. - , ETTLINGER, G., MACCABE, J. J., and RICHARDSON, N. (1976) Bi-manual motor performance in the monkey; Successive division of the forebrain and of the cerebellum, Exp. Neurol.,
50, 48-59.
JONES, E. G., and POWELL, T. P. S. (1970) An anatomical study of converging sensory pathways within the cerebral cortex of the monkey, Brain, 93, 793-820. RIDLEY, R. M., and ETTLINGER, G. (1976) Impaired tactile learning and retention after removals of the second somatic sensory projecion cortex (SIl) in the monkey, Brain Res., 109, 656-660. - , - (1978) Further evidence of impaired tactile learning after removals of the second somatic sensory projection cortex (SIl) in the monkey, Exper. Brain Res., 31, 475-488. WOOLSEY, C. N. (1958) Organization of somatic sensory and motor areas of the cerebral cortex, in Biological and Biochemical Bases of Behavior, ed. by H. F. Harlow and C. N. Woolsey, Univ. Wisconsin Press, Madison.
Mr. H. S. Garcha, Institute of Psychiatry, De Crespigny Park, London SE5 SAF, UK. Prof. G. Ettlinger, Institute of Psychiatry, De Crespigny Park, London SE5 SAF, UK.
INTRODUCTION
Ridley and Ettlinger (1976, 1978) have reported a severe and lasting disorder of tactile performance in monkeys with bilateral removals of the second somatosensory projection cortex (area SII). Those removals were to include cortex identified as SII both electrophysiologically (Woolsey, 1958) and anatomically (Jones and Powell, 1970) Subsequently, Burton and Jones (1976) have re-defined the position and extent of SII in the monkey by anatomical methods. We have therefore studied 2 further groups of animals, all with removals intended to involve only the smaller region of cortex recently designated as SII (Burton and Jones, 1976). Three animals were given unilateral and 3 animals bilateral removals. Unexpectedly, the animals with unilateral ablations of SII were massively impaired.
MATERIALS AND METHOD
Subjects
Nine previously untrained pre-pubertal rhesus monkeys, Macaca mulatta (2.2 3.1 kg) were divided into 3 comparable groups on the basis of their performance on a tactile task (stage 1). Three animals had the area newly designated as SII (Burton and Jones, 1976) removed bilaterally (animals BSII-1-3); 3 had this region removed unilaterally (animals USII-1-3); and 3 served as unoperated controls (C-1-3). Unilateral removals were made from the hemisphere contralateral to the pre-operatively preferred hand (stage 1). Histological verification of the actual extents of the removals is not available since all 9 animals will continue to be trained for another year. Training procedures
All procedures have remained exactly as already described (Ridley and Ettlinger, 1976, 1978). In brief, training was carried out in a WGTA for peanut reward, with 40 trials given daily, 4 or 5 days each week. Cortex (1978) 14, 319-326.
H. S. Garcha and G. Ettlinger
320
RESULTS
The sequence of training and the results are shown in Tables I-III. The one-tailed Mann-Whitney V-test was used for all comparisons. TABLE I
Performance by 3 Groups of Monkeys on Tasks Described in Text
Animals
Stage of training
With preferred hand
Cylinder and Sphere 1 Pre-operative New Learning
2 Post-operative 1st Retention
3 Concave and Convex New Learning
4 Pillar and Diabolo New Learning
USII-1 USII-2 USII-3
130 250 120
130 330 50
350 110 30
lOOOF lOOOF 270
BSII-1 BSII-2 BSII-3
230 100 130
170 60 140
80 80 500
lOOOF lOOOF lOOOF
C-1 C-2 C-3
130 180 200
0 0 0
90 90 70
220 100 190
Designation of animals as in text. Figures refer to the number of trials required to reach standard levels of performance: stage 1, 180 correct responses in 200 trials; stage 2, 90 correct responses in 100 trials; stages 3 and 4, 72 correct responses in 80 trials. F indicates that the animal failed to reach the required level of performance in the indicated number of trials. TABLE II
Performance by .3 Groups of Monkeys on Tasks Described in Text
Animals
Stage of training With non-preferred hand
6 T and L New Learning
Bimanual motor tasks
7 Cone and Pyramid New Learning
8 Push-Pull New Learning
9 Press-Rotate New Learning
USII-1 USII-2 USII-3
570 lOOOF 500F
210 50 OF 500F
670 400 920
320 450 240
BSII-l BSII-2 BSII-3
620 130 lOOOF
lOOOF 500F 500F
260 510 390
160 490 260
200 320 400
90 40 80
640 210 560
330 970 300
C-1 C-2 C-3
The designations of animals and the meaning of the letter F as in Table I. The figures refer to the number of trials required to reach standard levels of performance: stages 6 and 7, 72 correct responses in 80 trials; stages 8 and 9, 90 correct responses in 100 trials.
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321
TABLE III
Performance by 3 Groups of Monkeys on Tasks Described in Text Animals
Stage of training
With preferred hand 10 Latch Box Problems New Learning I II III IV
11 Alternation New Learning
non-preferred Cylinder and Sphere 12 2nd Retention
13 Retention
USII-1 USII-2 USII-3
50 10 40
70 60 50
0 0 60
110 150F 150F
450 280 190
130 60 100
o(lOE) 20 500F
BSII-1 BSII-2 BSII-3
50 210 50
30 70 90
0 0 50
0 100 0
560 140 240
400 120 400
740 180 0(8E)
C-l C-2 C-3
120 30 260
70 80 10
60 50 0
30 30 10
340 520 320
0 40 0
o(3E) O(3E) o(2E)
The designations of animals and the meaning of the letter F as in Table 1. The figures refer to the number of trials required to reach standard levels of performance: stage 10, 18 correct responses in 20 trials; stages 11-13, 90 correct responses in 100 trials. Figures in brackets at stage 13 represent errors in initial 100 trials.
Stages 1 and 2 Animals were trained to discriminate with their preferred hand in the dark between a cylinder (2.5 cm diameter, 5.5 cm high) and a sphere (5.5 cm diameter) to 180 correct responses in 200 consecutive trials. The groups did not differ significantly on this task pre-operatively (stage 1). When, starting 13 days after surgery, they were retrained on the same task to 90 correct responses in 100 trials (stage 2), the bilateral animals (p < .05) and the unilateral animals (p < 0.5) were significantly impaired relative to the control animals. Already at this stage the mean score of the unilateral group, namely 170 trials, was somewhat greater than that of the bilateral group, namely 123 trials; whereas pre-operatively the difference between group means was only 14 trials. Both groups were somewhat less impaired than were the earlier (Ridley and Ettlinger, 1976) animals with presumably larger bilateral removals on the same task. (In the case of animals USII-l and USII-3 the lesser degree of impairment may be due to only these 2 animals being given 20 additional training trials before surgery, so that the interval between pre- and post-operative training would be exactly 13 days for all animals). Three animals reversed their hand preference as a result of surgery: BSII-3, USII-2 and USII-3.
322
H. S. Garcha and G. Ettlinger
Stages 3 and 4 After stage 2, animals were trained in the dark to 72 correct responses in 80 trials on 2 further tactile discrimination tasks, using their preferred hand: concave (0.8 cm high from 1.0 cm high) and convex (4.1 cm high from 3.0 cm high) blocks (3.0 cm X 3.0 cm) (stage 3); and pillar (3.0 cm X 3.0 cm X 1.0 cm at top and base; 1.0 cm X 1.0 cm stalk) and diabolo (3.0 cm diameter at top and base; 1.0 cm diameter at waist) with overall heights of 4.0 cm (stage 4). Stage 3 was easier (mean of 83 trials) than stage 4 (mean 170 trials) for the control animals, and the groups did not differ significantly at stage 3 (but at least one animal in each operated group seemed to be severely impaired). However, at stage 4 both operated groups were significantly (p < .05) impaired at learning in comparison with the control group. It is noteworthy that animal USII-l continued to prefer to use the hand contralateral to the unilateral removal until stage 11, and performed poorly at stages 2, 3 and 4. Animal USII-2 changed its preferred hand but performed poorly at stages 2, 3 and 4 with the hand ipsilateral to the removal. Animal USII-3 also changed its hand preference and performed within control limits at stage 3, and not far beyond at stages 2 and 4, with the ipsilateral hand. Stage 5 In order to evaluate tactile learning with their non-preferred hands, all animals were next adapted to restriction of the use of the preferred hand. A weighted rubber ball was attached by a chain and bracelet to one wrist. First, all animals were trained, while the non-preferred hand was restricted, to discriminate in the dark between a block (3.35 cm deep X 5.05 cm wide X 3.25 cm high) and spikes 0.2 cm nails set into hemisphere of 4.9 cm diameter) to 45 correct responses in 50 trials. No differences between the groups emerged and the data are not presented. Then they were trained to the same level of performance with the preferred hand restricted. (These learning scores with the second hand might be viewed as a measure of intermanual transfer.) All bilateral and control animals learnt in 0 or 10 trials. The unilateral animals required 20, 110 and 1000 + trials respectively (where + indicates failure to meet the required criterion). Each of these unilateral animals, unlike any control or bilateral animals, required more trials to learn with the second hand than with the first. The performance of the unilateral animals differed significantly (p < .05) from that of the other 2 groups.
Stages 6 and 7 Animals were next trained in the dark to 72 correct responses in 80 trials on 2 further tactile discrimination tasks, using their non-preferred
Tactile disorder in monkeys
323
hands. First,. they were required to discriminate between T (3.9 em deep, 4.0 em wide, bar width 0.6 em, bar height 1.0 em) and L (4.0 em deep, 1.9 em wide, bar dimensions as for T) (stage 6); and then between cone (3.0 em diameter at base, 4.2 em high) and pyramid (3.1 em sides at base, 4.2 em high) (stage 7). Stage 6 was more difficult (mean of 307 trials) than stage 7 (mean of 70 trials) for the control group. If task difficulty were a relevant factor then greater impairment would be expected at stage 6 than at stage 7. Nonetheless, only the unilateral group was significantly impaired (p < .05) in comparison with the control animals at stage 6, although 2 of the bilateral animals also performed poorly. At stage 7 the bilateral and unilateral groups differed significantly (p < .05) from the control group. However, in partial explanation for the greater impairment at stage 7 it must be noted that the results for performance at stages 5, 6 and 7 are not entirely independent. Thus animal USII-3 failed to learn within 1000 trials at stage 5 with the non-preferred hand, and subsequently failed with that hand at stages 6 and 7; likewise animals BSII-3 and USlf2 failed to learn at stage 6 and also failed at stage 7. (However, animals BSII-1 and 2 learnt at stages 5 and 6 but failed with the same hand at stage 7.) Steges 8 and .9 The animals of Ridley and Ettlinger (1976, 1978) were not required to learn any motor task. In the post-operative training of the present animals it was noted that movement of the fingers seemed "clumsy", both in palpating the objects and in opening the lids and retrieving rewards. Therefore all animals were required to learn 2 bi-manual motor skills previously described (Elliott, Ettlinger, Maccabe and Richardson, 1976): "push-pull" where the monkey is required to push a handle with one hand, and simultaneously pull another with the other hand to obtain a peanut reward (stage 8); and "press-rotate" where the monkey has to rotate a knob with one hand and simultaneously depress a lever with the other for peanut reward (stage 9). At stage 8 training was entirely in the light, but at stage 9 in the dark once the animals had partially learnt the component responses. There were no significant differences at either stage. Stage 10
The skill required at stages 8 and 9 was bi-manual coordination, but the movements were relatively coarse. Therefore, at stage 10 fine movements of at least one hand were required to solve the 5 graded latch-box problems described and illustrated in Elliott (1976). The problems were given exactly as in Elliott (1976), with a time limit of 30 sec per trial and in the light. There were no group differences on problems 1-3 but on
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problem 4 the unilateral group was significantly (p < .05) impaired. Only 1 animal (C-3) learnt problem 5 so the data are not presented.
Stage 11 Next, the monkeys were trained on spatial alternation in the dark: a doubly-baited zero trial started each day's session of 40 trials; errors were corrected by delayed re-run trials which were included in the learning scores; intertrial interval was 6-7 sec. The 2 operated groups performed better than the control group.
Stages 12 and 13 The tactile discrimination task (cylinder and sphere) already trained pre-operatively (stage 1) and again first after surgery (stage 2) was retrained to 90 correct responses in 100 trials first with the preferred hand (stage 12), then after a replication of stage 5 with the non-preferred hand (stage 13). Both operated groups were significantly (p < .05) impaired at stages 12 and 13.
Summary of results There were no consistent impairments at motor learning or spatial performance; but there was significant defect, especially in the unilateral animals and then in both hands, on tasks requiring tactile learning and tactile retention. DISCUSSION
The lesio12S Detailed discussion must await histological verification at the conclusion of further training. However, it would seem likely prima facie that removals of the newly defined (Burton and Jones, 1976) second somatosensory projection area, although intended to be less extensive than the earlier removals (Ridley and Ettlinger, 1976, 1978) are sufficient to produce massive and lasting deficit. The surrounding tissue may also be partly involved in tactile performance, because the earlier (Ridley and Ettlinger, 1976) bilaterally lesioned animals were more impaired at their stage 2 (the same task) than the present bilateral animals at stage 2. The effect of destruction of underlying fibre tracts is uncertain: it is difficult to ensure total removal of the relevant SII cortex within the lateral fissure without damaging some non-cortical structures. The degree of defect in the unilateral group was unexpected. Again, caution is advisable in case, on histological verification, these lesions are
Tactile disorder in monkeys
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toO large or too deep. However, it is already certain that only a single hemisphere was involved. All 3 unilateral animals were impaired with their preferred hand at stages 2 and 4, and 2 animals also at stage 3. The preferred hand in one of the animals was contralateral to the removal (Le. still the pre-operatively preferred hand); but in 2 other animals it was ipsilateral to the removal. So it would seem that unilateral removals of SII impair performance with both hands (since the one animal which did not change its hand preference was also impaired at stages 6 and 7 with the non-preferred, Le. ipsilateral, hand).
The behavioural alterations It was perhaps surprising that the bilateral removals of Ridley and Ettlinger (1976, 1978) would be followed by such severe and persisting disturbances. For, although more extensive than in this study, those lesions were small relative to most other lesions that produce behavioural defect in the monkey. Nonetheless, those behavioural alterations could have reflected damage to neural systems which, when intact, were themselves involved in the mediation of tactile learning and memory. This may still be a possible explanation for the present findings; but it would be necessary to suppose that each individual (i.e. left- or right-sided) SII region contributed to the tactile performance of both hands and yet could not function adequately in the absence of the opposite SII region. It seems more plausible to suppose that SII cortex (in addition to its other functions) sustains the adequate functioning of another somatosensory system; and that after a unilateral SII removal the neural system concerned with tactile learning and memory is functionally disrupted by an abnormal output from the remaining SII cortex which is no longer "in balance". On this view impairment after bilateral SII removals is due to the absence of normal sustaining inputs from the two SII regions to another system; impairment after unilateral SII removals (which may be more severe than after bilateral removals) is due to an abnormal input from the intact SII cortex to another system. This view of the origin of the defects after SII removals can be readily reconciled with the detailed behavioural findings. Performance on visual, motor and spatial tasks is intact, even in the dark. Tactile sensory capacities and weight discriminations were not impaired (Ridley and Ettlinger, 1976, 1978). The defect seems, on the available evidence, to involve only tactile learning, tactile retention and intermanual transfer (Ridley and Ettlinger, 1978). Such a disorder of learning and memory is likely to be a consequence of dysfunction of a system functionally separate and perhaps (but not necessarily) also anatomically separate from SII, rather than to ensue from loss of a system within SII cortex which in the intact monkey would itself
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mediate tactile learning and memory. However, it remains unknown what kind of sustaining functions SII cortex possibly provides for tactile learning, just as it remains unknown how, for example, the mamillary bodies sustain verbal learning and memory in man.
SUMMARY
Three groups of monkeys were studied: one with bilateral removals of the second somatosensory projection cortex (SII); another with similar unilateral removals; and an unoperated control group. Both lesion groups were significantly impaired on tasks of tactile learning and tactile retention. However, there were no differences between groups on the great majority of tasks of motor learning, nor on spatial alternation in the dark. The animals with unilateral removals were generally impaired whether using the hand contralateral to or ispilateral to the removal. Acknowledgments. We are grateful to the MRC who supported this work; and to Dr. R. M. Ridley for comments on this paper.
REFERENCES BURTON, H., and JONES, E. G. (1976) The posterior thalamic region and its cortical projection in New World and Old World monkeys, ]. Camp. Neurol., 168, 249-301. ELLIOTT, R. C. (1976) Problem solving in cebus and rhesus monkeys, Bull. Psychonom. Soc., 7, 319-320. - , ETTLINGER, G., MACCABE, J. J., and RICHARDSON, N. (1976) Bi-manual motor performance in the monkey; Successive division of the forebrain and of the cerebellum, Exp. Neurol.,
50, 48-59.
JONES, E. G., and POWELL, T. P. S. (1970) An anatomical study of converging sensory pathways within the cerebral cortex of the monkey, Brain, 93, 793-820. RIDLEY, R. M., and ETTLINGER, G. (1976) Impaired tactile learning and retention after removals of the second somatic sensory projecion cortex (SIl) in the monkey, Brain Res., 109, 656-660. - , - (1978) Further evidence of impaired tactile learning after removals of the second somatic sensory projection cortex (SIl) in the monkey, Exper. Brain Res., 31, 475-488. WOOLSEY, C. N. (1958) Organization of somatic sensory and motor areas of the cerebral cortex, in Biological and Biochemical Bases of Behavior, ed. by H. F. Harlow and C. N. Woolsey, Univ. Wisconsin Press, Madison.
Mr. H. S. Garcha, Institute of Psychiatry, De Crespigny Park, London SE5 SAF, UK. Prof. G. Ettlinger, Institute of Psychiatry, De Crespigny Park, London SE5 SAF, UK.