Exp Brain Res (1992) 90:229-232

Experimental BrainResearch 9 Springer-Verlag 1992

Research Note Control of arm movement after bilateral lesions of area 5 in the monkey (Macaca mulatta) P.D. Nixon, P. Burbaud*, and R.E. Passingham Department of Experimental Psychology, South Parks Road, Oxford OX1 3UD, UK Received April 30, 1991 / Accepted April 23, 1992

Summary. The effect of bilateral area 5 lesions on the analysis of proprioceptive information and the guidance of reaching movements was studied in three rhesus monkeys. In the first paradigm (Proprioceptive discrimination test) the monkeys were trained to discriminate between movements of a joystick to the right or left without visual control; they reported the direction of movement by touching or not touching a screen (go/no-go task). After area 5 had been removed, the monkeys were only mildly impaired on this test. It is concluded that such simple joint movement could be analysed in area 2, area 5 being concerned with more complex arm movements. In the second paradigm (Searching test) the monkey had to find a peanut on a board in the dark using proprioceptive information stored in memory during previous trials. After area 5 lesions, the number of correct reaches was not modified but the number of errors after an incorrect trial (correcting movement) was significantly increased. The data suggests that when visual input is not available, area 5 is involved in the guidance of arm movements on the basis of proprioceptive inputs.

Key words: Area 5 lesion - Monkey

Proprioceptive discrimination

Introduction

The parietal cortex is classically described as an associative cortex for somatic (area 5 and 7 b) and visuospatial (area 7 a) information. Its rich connections with sensory and motor areas allow this area to play a part in the analysis of somato-sensory input and in directing action on the basis of this information. Laboratoire de Neurophysiologie (CNRS URA 1200), Universit6 de Bordeaux II, 146 Rue L6o Saignat, F-33076 Bordeaux Cedex, France * Present address:

Correspondence to:

R.E. Passingham

Lesions of the posterior parietal cortex in man and monkeys induce various disorders, such as deficits in shape discrimination, under-use of the contralateral forelimb, visual hemineglect and clumsiness in reaching and grasping movements (for review, see Hyvarinen 1982). After unilateral lesions restricted to areas 5 and 7, monkeys make gross errors in the accuracy of reaching movements with or without visual guidance (Hfirtje et al. 1974; Lamotte et al. 1978). But whether this is due to " sensory impairment or to a disorder in the planning of movement remains unclear. The receptive fields of area 5 neurons are much larger and more complex than those of area 2 (for review see Hyvarinen 1982) and their properties suggest that area 5 is more likely to be involved in the integration of complex proprioceptive information than with precise tactile discrimination. Indeed, it was shown that monkeys with area 5 lesions were not impaired in tests of tactile discrimination, so long as the lesion did not include the hand region of SI (Murray and Mishkin 1984). That area 5 plays a role in the integration of proprioceptive input is supported by the high convergence of input from area 2 upon area 5 neurons (Pearson and Powell 1985). Behavioural studies suggest that area 5 could also intervene in the planning of arm movement. Indeed, a population of area 5 neurons without identifiable receptive fields activated during reaching or projection hand movements has been described (Mountcastle et al. 1975). These cells were still recorded in area 5 of deafferented monkeys suggesting that their activity had a central origin (Seal et al. 1982) and could play a role in the command of arm movement. Furthermore, it was shown that area 5 neurons could be involved in both spatial encoding of movement (Kalaska et al. 1983; Georgopoulos et al. 1984) and the initiation of movement triggered by sensory cues (Lamarre et al. 1983; Chapman et al. 1984; Seal et al. 1985; Crammond and Kalaska 1989). In the present study, we investigated the role of area 5 in the analysis of joint position during active wrist

230 movements (Proprioceptive discrimination test) and in the control of reaching movements on the basis of proprioceptive information (Searching test). A comparison was made o f the monkeys performance before and after the bilateral removal of area 5. Methods Three rhesus monkeys (Macaea mulatta) were used. They weighed between 5 and 7 kg. In the Proprioceptive discrimination test the monkeys were trained to move a joystick to the right or left. The joystick could be locked so that it could only move in one direction, left or right. The lock was controlled by computer, which determined for each trial the direction in which the joystick could be moved according to a r a n d o m sequence. At the beginning of a trial, the monkey pushed its forearm through a tube (which ensured that the movements were restricted to wrist movements) and grasped the joystick which was placed in an opaque box, preventing the animal seeing its arm or hand. The monkey moved the joystick in the permitted direction and on completion of the movement a white square appeared on the video screen. The monkey removed its hand from the box and if the joystick had moved to the left, he then had to touch the square within three seconds to obtain a reward. If the joystick had moved to the right, he had to refrain from touching the square to obtain the reward. Thus the task can be classified as a go/no-go task with symmetrical reward. To be certain that the animals were not able to use any visual information about their movements, the house light was automatically turned off as the monkey put its arm in the tube. The monkeys were trained until they reached a criterion of 90% correct @ials Over two sessions of 100 trials each. They were left without training for three weeks and were then retested one week before surgery. After a two week post-operative recovery period, they were again retested until they reached the criterion level of performance. In the Searching test, the monkeys were trained to find a peanut on a board containing 21 holes (diameter 4.5 cms, depth 4.5 cms, 7 cms centre to centre, Figure 1). To reach the board the animal had to put its left arm through a hole in an opaque screen; thus it could not see its arm as it searched. During each session, the peanut was placed in the same hole on each trial. The location of the holes tested were chosen so as to test reaching memory over as large a range of arm positions as possible i.e. full extension to half flexion of forearm and five different reaching distances. On each trial the monkey explored the holes for the peanut until he found i[. He then withdrew his arm and the aperture was closed. The peanut was placed in different holes from session to session. Five trials were given for the animal to locate the peanut in its new position, and then a further 65 trials were given. The animals performance was filmed with an infrared camera. Analysis of the tape provided information on the holes the animal tried and on the timing of the session. The analysis was performed on the last 65 trials. Before surgery the animals were given five pretraining sessions. They were then given test sessions on the target holes. Three weeks after surgery they were given a further five test sessions on the same holes. Surgery was performed under general anaesthesia and aseptic conditions. The cortex was removed bilaterally from area 5 using a fine gauge sucker under the guidance of a binocular operating microscope. In the intraparietal sulcus we tried to remove the whole of the arm area of area 5 (Pearson and Powell 1985) and in doing so probably invaded a small part of area 2. At the completion of the experiment, each animal was perfused intracardially with formal-saline. The brain was removed and placed in 30% sucrose formalin till it sank. It was then blocked in the vertical stereotaxic plane. The brains were cut coronaUy on a freezing microtome at 50-Ix intervals. A one in ten series

Investigator

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Fig. 1. Testing board for the Searching test. The letters indicate the holes that were baited, and the order of testing was retained throughout the lesion. Figure 2 shows sections taken at AP-2.5, 0.5, 3.5 and 6.5. It will be seen that the lesion was largest in animal 102. Some tissue deep in the intraparietal sulcus was spared in all three animals. Results and discussion Proprioceptive discrimination test Figure 3 shows the errors in relearning after surgery for the Proprioceptive discrimination Test. All three monkeys relearned the task to criterion, but two o f the monkeys (102 and 103) were mildly impaired. They took 57 and 155 trials to relearn the task. Thus it appears that after the removal of area 5, the monkeys were only mildly impaired in a simple test of proprioceptive discrimination. The lack of a severe defect might be explained by the simplicity of the movement, the pronation or supination of the wrist. It is possible that such proprioceptive information can be adequately analysed in area 2, which has a direct projection to the m o t o r cortex (Jones and Powell 1969). Unit recording studies have shown that at least 50% of the joint neurons in area 2 have a reciprocal organization during wrist or elbow movement (Bioulac and Lamarre 1979) but very few neurons have this property in area 5 (Mountcastle et al. 1975; Seal et al. 1982; Lamarre etal. 1983; Chapman etal. 1984). Therefore a short cortical loop might be involved in the analysis of simple joint displacements without the intervention of parietal area 5. The latter may be involved with the integration of more complex polyarticular input during whole arm movement. This is in agreement with the characteristics of the receptive fields of area 5 neurons (Hyvarinen 1982).

Searching test Figure 4 gives the performance of the monkeys before and after surgery on this test.

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Fig. 2. Histology of area 5 lesions. This figure shows coronal sections of the brains of monkeys S 101, S 102, and S 103 taken AP-2.5, 0.5, 3.5 and 6.5. Dashed lines indicate the localization of cortex

removed. Some tissue in the depth of the intraparietal cortex was spared in all three animals

The histograms on the left show the number of trials in which the animals reached to the correct well first time. There was no significant change in the proportion of these trials after surgery. This indicates that the reaching component of the movement was not impaired by the area 5 lesion.

The histograms on the right show the total number of errors, that is the number of holes which the animals explored incorrectly. A significant increase in the number of errors was found in lesioned monkeys (p < 0.001). These results mean that on those trials on which the animals first explored an incorrect hole, they then made more errors after surgery before finding the correct hole. We take this to mean that the impairment was not in reaching but in searching once they had inserted their arm and failed to find the hole immediately. When the animals missed the baited hole, one may think that, in the absence of visual control, area 5 is needed to provide the feed-back necessary to adjust the arm position in order to reach the correct hole. This suggests that this structure is involved in the guiding of arm movements on the basis of proprioceptive information alone. To search accurately without seeing his arm, the monkey must use information about proprioceptive input memorised from previous trials. The monkeys might perform poorly because of a memory defect for proprioceptive information or inattention to their own movements. Unit recording studies have indeed shown that area 5 neurons could play a role in the temporary retention of proprioceptive information (Koch and Fuster 1989) but that attentional factors also influence their response to somaesthetic stimuli (Mountcastle et al. 1975; Chapman et al. 1984). An impairment in searching may also be due to an impairment in the integration of sensory and motor information. It is possible that area 5 neurons, on which

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b total number of holes that the animals explored in error across all trials before and after surgery; [] PRE-OP; [] POST-OP

b o t h peripheral and central inputs converge, m a y c o m pare the intended m o v e m e n t with the effective m o v e m e n t (Kalaska et al. 1983) and thus influence the accuracy o f searching m o v e m e n t s by peripheral feed-back. By well defined c o n n e c t i o n s (Strick et al. 1978; Petrides and Pandya 1984; Caminiti et al. 1985), area 5 m a y receive i n f o r m a t i o n f r o m p r e m o t o r areas prior to m o v e m e n t onset and after integration o f proprioceptive feed-back during the o n g o i n g m o v e m e n t , influence in turn their activity by w a y o f a cortico-cortical loop. M o r e experiments are needed to segregate the influence o f peripheral and central i n f o r m a t i o n on area 5 neurons but one m a y think that it is the high convergence o f sensory and m o t o r input which probably explains the role o f this cortical area in the planning o f arm m o v e m e n t s .

Hyvarinen J (1982) The parietal cortex of monkey and man. Springer, Berlin Heidelberg New York Jones EG, Powell TPS (1969) Connexions of the somatic sensory cortex of the rhesus monkey-I-ipsilateral cortical connexions. Brain 92 :477-502 Kalaska JF, Caminiti R, Georgopoulos AP (1983) Cortical mechanisms related to the direction of two dimensional arm movements: relations in parietal area 5 and comparison with motor cortex. Exp Brain Res 51:247-260 Koch KW, Fuster JM (1989) Unit activity in monkey parietal cortex related to haptic perception and tempory memory. Exp Brain Res 76: 292-306 Lamarre Y, Spidalieri G, Chapman CE (1983) A comparison of neuronal discharge recorded in the sensory motor cortex, parietal cortex and dentate nucleus of the monkey during arm movements triggered by light, sound or somesthetic stimuli. Exp Brain Res 7:140-156 Lamotte RH, Acuna C (1978) Defects in accuracy of reaching after removal of posterior parietal cortex in monkeys. Brain Res 139 : 309-326 Mountcastle VB, Lynch JC, Georgopoulos A, Sakata H, Acuna C (1975) Posterior parietal association cortex of the monkey: command functions for operations within extra-personal space. J Neurophysiol 3 : 871-908 Murray EA, Mishkin M (1984) Relative contributions of SII and area 5 to tactile discrimination in monkeys. Behav Brain Res 11:67-83 Pearson RCA, Powell TPS (1985) The projections of the primary sensory cortex upon area 5 in the monkey. Brain Res Rev 9 : 89107 Petrides M, Pandya DN (1984) Projections of the frontal cortex from the posterior parietal region in the rhesus monkey. J Comp Neurol 228:105-116 Seal J, Gross Ch, Bioulac B (1982) Activity of neurons in area 5 during a simple arm movement in monkeys before and after deafferentation of the trained limb. Brain Res 250: 229-243 Seal J, Commenges D (1985) A quantitative analysis of stimulus and movement-related responses in the posterior parietal cortex of the monkey. Exp Brain Res 5 : 144-153 Strick PL, Kim CC (1978) Input to primate motor cortex from posterior parietal cortex (area 5). I. Demonstration by retrograde transport. Brain Res 157: 325-330

Acknowledgement. This project was supported by a Fyssen Foundation grant. References Bioulac B, Lamarre Y (1979) Activity of post-central cortical neurons of the monkey during conditioned movements of a deafferented limb. Brain Res 172:427-437 Caminiti R, Zeger S, Johnson PB, Urbano A, Georgopoulos AP (1985) Cortico-cortical efferent systems in the monkey: a quantitative spatial analysis of the tangential distribution of cells of origin. J Comp Neurol 241:405419 Chapman CE, Spidalieri G, Lamarre Y (1984) Discharge properties of area 5 neurons during arm movements triggered by sensory stimuli in the monkey. Brain Res 309: 63-77 Crammond PJ, Kalaska JF (1989) Neuronal activity in primate parietal cortex area 5 varies with intended movement direction dering an instructed delay period. Exp Brain Res 76:458-462 Georgopoulos AP, Caminiti R, Kalaska JF (1984) Static spatial effects in motor cortex and area 5: quantitative relations in a two-dimensional space. Exp Brain Res 54:446-454 Hartje N, Ettlinger G (1974) Reaching in light and dark after unilateral posterior parietal ablations in the monkey. Cortex 9 : 346-354

Control of arm movement after bilateral lesions of area 5 in the monkey (Macaca mulatta).

The effect of bilateral area 5 lesions on the analysis of proprioceptive information and the guidance of reaching movements was studied in three rhesu...
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