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The Journal of Neurophysiology Vol. 79 No. 1 January 1998, pp. 478-482
Copyright ©1998 by the American Physiological Society
RAPID COMMUNICATION
Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, United Kingdom
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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Rushworth, M.F.S., H. Johansen-Berg, and S. A. Young. Parietal cortex and spatial-postural transformation during arm movements. J. Neurophysiol. 79: 478-482, 1998. Cells in the parietal motor areas 5, MIP, and 7b have spatially tuned activity during movements. Lesions, however, do not disrupt visual reaching or learned nonspatial movement selection. The role of such parietal cells in sensorimotor coordinate transformations is unclear. The present experiment investigates whether the parietal motor areas are concerned with the following: 1) the transformation between the desired position in space of the hand and the limb's postural configuration during movement and 2) interjoint coordination. Six macaque monkeys were trained to reach in the dark. Spatial-postural transformations assume a simple form in the absence of vision and so may be most easily studied when animals reach in the dark. A lesion was placed in the parietal cortex that included areas 5, MIP, and 7b of three macaques. The simple relation between hand position and limb postural configuration seen in controls was disrupted after the lesion. The intercoordination of movements of the hand with those of the rest of the arm was also affected. The lesion did not affect the range or velocity of joint movements or the curvature of the hand's trajectory. The cell activity in parietal areas 5, MIP, and 7b may not be essential for the transformation between retinocentric representation of the target and shoulder centered representations of the desired position of the hand, but it is essential for both the subsequent transformation between desired hand position and the postural configuration of the arm and for interjoint integration.
Cells in primary motor cortex (M1) have spatially tuned activity during visually guided movement (Georgopoulos 1995 Six male cynomolgus macaques (Macaca fascicularis) were used. Their ages ranged between 3 and 4 yr and their weights varied between 5 and 7 kg. Lesions were made in the parietal lobes of three of the animals after preoperative training. The performance of all the animals was similar preoperatively; all animals were given the same amount of training.
Surgery and histology
Details and figures of the surgery and histology have been published (Rushworth et al. 1997b Apparatus
The animals were tested in a standard transport cage in a completely darkened room. The front of the cage was an opaque screen with four doors (Rushworth et al. 1997b Procedure
All testing was conducted in the dark and the monkeys never saw the movement targets. The target and starting positions were kept constant during a day's testing but were varied from one day's session to the next. The experimenter opened one of the four doors on the screen to allow the monkey to search for the food reward. The door was closed between trials. The first five trials were regarded as practice trials while the animal learned the position of the unseen food reward. The animals then reached to the same target position from the same door for a further 15 trials.
Analysis
RELATION BETWEEN SPATIAL POSITION OF WRIST AND POSTURAL CONFIGURATION OF ARM.
The analysis was performed on two-dimensional (2-D) data. The small frame-to-frame variation in the measured length of limb segments confirmed that movement was mainly in the plane of the workspace and there was no difference between control and experimental groups in the small deviation from the plane. The spatial position of the wrist, in a body centered coordinate system, is described by two parameters (Fig. 1A): the distance (D) from the shoulder and the angle of elevation (W) with respect to the shoulder. In two dimensions, the postural configuration of the arm is described by the angle of elevation of the limb segments of the forearm (f) and the upper arm (s) and the relative angle of flexion (e) at the elbow between the upper and forearm segments. The present elevation angles, s and f, therefore correspond to the projection of the segmental elevation angles,
COORDINATION BETWEEN HAND AND ARM COMPONENTS OF THE MOVEMENT.
The monkeys usually moved their hands by flexing the wrist (angle h, Fig. 1) in anticipation of reaching the target position while the wrist was still moving toward the target. To assess the degree of coordination between the hand and arm movement we measured the tangential velocity of the wrist at the time that h decreased by 10° from its maximum value. The appropriateness of the measure was visually checked by graphing the changes in parameter h throughout the movement. Two measures were made as follows: 1) the absolute tangential velocity of the wrist at the time of wrist flexion and 2) the ratio of the tangential velocity of the wrist, at the time of wrist flexion, to the maximum tangential velocity of the wrist during the reach.
KINEMATICS OF SPATIAL AND POSTURAL ASPECTS OF THE MOVEMENT.
We measured the following: 1) the amplitude range of upper arm elevation (s), forearm elevation (f), and elbow flexion (e); 2) the ratio of angle amplitudes s/f and s/e; 3) joint rotation (the angular displacement between the initial and final joint position as a ratio of the total angular distance traveled during the movement) at the elbow and shoulder angles s and e; 5) maximum velocities of s, e, and f; 6) the maximum velocity of the wrist; and 6) the curvature of the wrist trajectory.
Fig. 1C shows data collected from a control animal on two nonconsecutive days. Despite the fact that 2-D measurements were taken, the relation between f and W is both strong and consistent.
Relation between spatial position of the wrist and postural configuration of the limb
In the control animals there was a close relation between forearm elevation (f) and wrist elevation (W) throughout the movement (Fig. 2C). The relation, however, was not always linear; this may have been because of the constrained nature of the movements and the fact that we measured the relation throughout the movement and not just at the target. Adjusted R2 multiple correlation coefficients between W and a quadratic polynomial function of f showed that f accounted for 86% of the variation in W, on average, in the control animals. After the lesion, however, quadratic polynomial functions of f were only able to account for 57%, on average, of the variation in the spatial variable of W (Fig. 2D). There was a significant difference between the average performances of the two groups whether the linear or quadratic functions were considered (P < 0.05).
Coordination between and hand and arm components of the movement
In the control animals, hand movement relative to the rest of the arm occurred while the tangential velocity of the wrist was, on average, just under 6 cm/s. In the animals with lesions, the hand movement was initiated when the tangential velocity of the arm was just under 2 cm/s. Hand movements in the controls were initiated when the arm was moving significantly faster (P < 0.05). This significant difference remained even when the wrist velocity at the time of hand movement was expressed as a fraction of the maximum wrist velocity recorded during that movement (Fig. 3).
Kinematics of wrist trajectory and limb joints
There was no difference among the groups in terms of joint amplitudes, joint amplitude ratios, joint rotations, joint rotation ratios, maximum velocities of joint movement, or tangential velocity of the wrist. The trajectory of the wrist was curved in most animals (Fig. 2, A and B). The distance traveled by the wrist was ~1.5-2.5 times the direct distance between the initial and final wrist positions. This difference may reflect the constrained nature of the movement and the complete lack of visual guidance. The degree of curvature, however, did not differ between the groups.
During movement made by both humans (Flanders et al. 1992 Conclusions
The cell activity in areas 5, MIP, and 7b is not essential for learned, nonspatial sensorimotor transformations (defined by Passingham 1993
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
). Hoffman and Strick (1995) recently reported misdirected hand movements in a macaque with an M1 lesion. They demonstrated that M1's role in directing movements may be the selection of appropriate muscle activation patterns; these were disrupted in the monkey with the lesion. Cells in parietal areas 5, medial intraparietal sulcus (MIP), and 7b are also active during visually guided reaching (Hyvarinen and Shelepin 1979; Johnson et al. 1996) but their distinct contribution to the sensorimotor transformations involved in reaching remains unclear.
). There is an increase in blood flow in a human homologue of the 7a/7ab/LIP region, but not the homologues of areas 5, MIP, or 7b, when subjects wearing prisms learn a new pattern of coordination for visual reaching (Clower et al. 1996). Such results suggest that although cells in areas 5, MIP, and 7b are involved in reaching, they are not essential for the initial coordinate transformation in reaching between retinocentric and body centered representations of the target (Flanders et al. 1992).
; Helms Tillery et al. 1995). This coordinate transformation follows the one from retinocentric representation to body centered representation described in the previous paragraph. We trained animals to reach in the dark; the relation between desired hand position and posture is based on a simple linear approximation when movements are made without visual guidance (Flanders et al. 1992). We also tested whether the areas are important for interjoint coordination. Again, this was done during reaching in the dark; interjoint coordination might otherwise be corrected by vision (Ghez et al. 1995). Interjoint coordination is a prerequisite for spatial-postural transformation. Bilateral lesions were made in areas 7b, 5, and most of adjacent MIP in three of the six animals trained on the task.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
). The present data set was collected after the completion of the previously reported procedures.
). The surgery was performed by Dr. R. E. Passingham. Surgery was carried out under sterile conditions with pentobarbital sodium anesthesia. At the end of the experiment the animals were anesthetized with pentobarbital and perfused with 90% saline and 10% formalin.
; Gallese et al. 1994), which were not verified in the present study. The location of the lesion was confirmed histologically. The absence of degeneration in nucleus ventralis posterolateral (VPLc) of the thalamus indicated that the lesions had not intruded into area 2 of the primary somatosensory cortex. The removal of the superior parietal convexity included its most caudal part where it extended over the crown onto the most dorsal part of the medial surface to include PEc and adjacent mediodorsal parietal area (MDP) (Colby and Duhamel 1991; Pandya and Seltzer 1982). There was some damage to area 7m (Cavada and Goldman-Rakic 1989) in each case, but this was always unilateral and limited to its most dorsal aspect.
). Items of food reward were put on a 1-cm2 shelf that could be placed anywhere on a 12- × 20-cm grid in front of the screen. The monkey in the cage behind the screen could reach arm's length through the doors to find the food reward at the target. The work space in which movements were recorded was therefore vertical and in the frontal plane. The work space was illuminated by an infrared light so that the monkeys' movements could be recorded in the two dimensions of the arm's workspace with an infrared camera, placed directly in front of the screen, for later analysis.
and 
(Soechting and Ross 1984), onto the planar surface of the workspace. Figure 1B shows a typical example of the type of movement measured.
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FIG. 1.
A: in 2 dimensions the position of the arm with respect to the shoulder can be described in terms of its distance (D) and elevation (W). Posture of the arm can be described by elevation of the upper arm (s) and elevation of the forearm (f). e, angle of flexion at the elbow; h, angle of flexion at the wrist. B: example of movements studied in the vertical, frontal plane. Top left: shoulder; hand to the right. Numbering indicates order of arm positions recorded during the movement. Movements of control and lesion animals were of a similar size and extent. C: strong relation between f and W in the control animals. 
, 
, 
, and 
: data for movements made on 2 nonconsecutive days by the same animal from the same starting position but to different target positions.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
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FIG. 2.
Trajectory in frontal plane taken by the wrist during 15 movements for a control (A) and a lesion animal (B). Broad hatching, starting position; fine hatching, target grid on which the actual target position for the session recorded is indicated ( 
). Relation between forearm elevation f and wrist elevation W in a control (C) and experimental animal (D). C and D: relation between velocity of forearm elevation f and tangential velocity of the arm at the wrist.
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FIG. 3.
After the lesion, hand movement relative to the arm occurred when limb was moving more slowly. Average tangential velocity of the wrist for each animal is shown at the time when the wrist flexion h decreased by 10° from its maximal value. Tangential velocity is expressed as a fraction of the maximum tangential velocity recorded during each movement.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
) and monkeys (Helms Tillery et al. 1995) there is a simple relation between the desired position of the hand in a shoulder centered space and the arm's postural configuration. When movements are made in the dark, the transformation is particularly simple (Flanders et al. 1992) and is therefore amenable to study. Our monkeys were trained to find a target position in the absence of vision at the start of each session. The transformation between desired hand position and limb posture was expected to be very direct because it was not preceded by any transformation from a remembered visual position (Flanders et al. 1992). In confirmation of this expectation in the controls, we found that ~86% of the variance in the elevation of the wrist W was accounted for by a function of forearm elevation f (Fig. 2C). This relation held for positions and postures throughout the recorded movements and was not just based on measurements when the hand was at the target (Flanders et al. 1992; Helms Tillery et al. 1995). The distance of the wrist from the shoulder, the other parameter that describes hand position in shoulder centered space, is necessarily determined by the postural parameter of angle of flexion at the elbow (D and e; Fig. 1).
). Second, the curvature of movements was not affected by the lesion (Fig. 2, A and B). Third, no other basic aspect of the measured kinematics differed between the groups. These similarities also ensure that differences in spatial-postural correlations are not simply due to range restriction effects in the data. Fourth, the movements were recorded until the hand stayed in the same place for two frames and no corrective movements were recorded.
) but that the lesioned parietal areas play a role in comparing intended and actual postures. This conclusion would be consistent with demonstrations that both proprioceptive and efference copy signals reach area 5 (Sakata et al. 1973; Seal et al. 1982).
); reaches made to the same target from different starting positions require different arm postures. We have previously used the same animals to compare reaches made in the dark to a target either from constant or from shifting starting positions (Rushworth et al. 1997b). Lesions that include 5, MIP, and 7b disproportionately affect reaches made from different starting positions; they are less direct and take longer to reach the target. The activity of single cells in area 5 depends on both the starting position and the target position of a reach (Lacquaniti et al. 1995). The cells' responses in this study were interpreted as representing the limb in a body centered coordinate framework. The movements were very stereotyped and each target position was associated with certain arm postures. It is possible that some of the cells may also have been encoding postural configurations of the limb. The maintenance of posture has a greater effect on the tonic activity of area 5 cells than it does on that of premotor and M1 cells (Georgopoulos et al. 1984). Despite these differences, M1 may also have a role in spatial postural transformation; M1 activity does not just depend on the direction of movement but on the arm posture used (Scott and Kalaska 1997).
) and imaging studies (Faillenot et al. 1997) have shown that some parietal regions are important for the visually guided coordination of reaching and grasping movements. The present results concerning reaching in the dark must be interpreted differently; they suggest that some areas have a wider role in using proprioception and efference copy to guide the coordination of multicomponent movements. Deafferentation in large fiber neuropathies also causes deficits in interjoint coordination (Sainburg et al. 1993) and multijoint movement, especially in the absence of vision (Gentilluci et al. 1994; Ghez et al. 1995). The parietal motor areas may play a special role integrating information about the relative positions of several joints into motor behavior; cells in areas 5 (Sakata et al. 1973) and 7b (Robinson and Burton 1980) have receptive fields that are distinguished by their responsiveness to both skin and joint stimulation and the manner in which they integrate information from several parts of the body. This should be contrasted with M1 receptive fields where, despite variation in size, there is a tendency for them to be smaller and there is also greater segregation of proprioceptive and cutaneous modalities (Strick and Preston 1982). The effects of deafferentation and parietal lesions should be distinguishable. Deafferentation additionally prevents proprioceptive guidance at the level of the spine and primary somatosensory and motor cortices. Parietal lesions may additionally disrupt corollary discharge signals (Seal et al. 1982).
).
; Wise et al. 1996) or spatial transformation between retinocentric and body centered representations of the target (Rushworth et al. 1997a). This cell activity is distinct from that seen in posterior parietal area PEG (Clower et al. 1996). Instead the cell activity in these parietal areas is required for interjoint integration and the transformation between the desired position of the hand and the postural configuration of the arm.
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ACKNOWLEDGEMENTS |
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We are grateful to M. Brown for technical assistance, C. Healey-Yorke for histological processing, Dr. R. Baddeley for helpful discussions, and Dr. R. E. Passingham for surgery and support and advice throughout the study.
This work was supported by Wellcome Trust Program Grant 038041/Z/93.
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FOOTNOTES |
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Address for reprint requests: M. Rushworth, Dept. of Experimental Psychology, University of Oxford, South Parks Rd., Oxford OX1 3UD, United Kingdom.
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REFERENCES |
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Abstract
Introduction
Methods
Results
Discussion
References
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