What aspects of movement are represented in the primary motor cortex (M1): relatively low-level parameters like muscle force, or more abstract parameters like handpath? To examine this issue, the activity of neurons in M1 was recorded in a monkey trained to perform a task that dissociates three major variables of wrist movement: muscle activity, direction of movement at the wrist joint, and direction of movement in space. A substantial group of neurons in M1 (28 out of 88) displayed changes in activity that were muscle-like. Unexpectedly, an even larger group of neurons in M1 (44 out of 88) displayed changes in activity that were related to the direction of wrist movement in space independent of the pattern of muscle activity that generated the movement. Thus, both "muscles" and "movements" appear to be strongly represented in M1.There has been long-standing controversy over whether "muscles" or "movements" are represented in the primary motor cortex (M1) (1). From a contemporary perspective, this question can be recast: What aspects of movement are encoded in the activity of M1 neurons: relatively low-level movement parameters like muscle force, or more abstract movement parameters like handpath? Since the pioneering work of Evarts (2), this question has been examined by recording the activity of single neurons in awake trained primates [for example, (3-10)]. Early experiments examined M1 activity in relation to simple finger and wrist movements (3). The discharge of many M1 neurons in these studies covaried with movement parameters such as static and dynamic force. These results led to the view that M1 is concerned with the generation of movement in terms of an "intrinsic" parameter space related to one or more of a number of variables including aspects of joint kinematics, joint torques, and the detailed pattern of muscle activity at a single joint.A different perspective has come from studies of M1 activity during reaching movements (4). In some experiments, the activity of M1 neurons, as a population, covaried with the trajectory of hand movement and signaled its instantaneous movement direction and velocity. These and similar results led to the view that M1 is concerned with the generation of movement in terms of an "extrinsic" parameter space related to the motion of the hand, the location of the target in space, or both (4, 9, 10). However, the results of other experiments of M1 activity during reaching movements made under altered load conditions or with different arm postures produced evidence for coding in an intrinsic parameter space (5).To address this controversy, we developed a paradigm that dissociates three different coordinate frames related to wrist movements: extrinsic (related to the direction of movement in space), muscle (related to the activity of individual or groups of muscles), and joint (related to the angle of the wrist joint) (11-13). Our paradigm takes advantage of two features of the wrist joint. First, the wrist rotates along two axes: flexion-extension and radial-ulnar deviation...
The ventral premotor area (PMv) is a major source of input to the primary motor cortex (M1). To examine the potential hierarchical processing between these motor areas, we recorded the activity of PMv neurons in a monkey trained to perform wrist movements in different directions with the wrist in three different postures. The task dissociated three major variables of wrist movement: muscle activity, direction of joint movement and direction of movement in space. Many PMv neurons were directionally tuned. Nearly all of these neurons (61/65, 94%) were 'extrinsic-like'; they seemed to encode the direction of movement in space independent of forearm posture. These results are strikingly different from results from M1 of the same animal, and suggest that intracortical processing between PMv and M1 may contribute to a sensorimotor transformation between extrinsic and intrinsic coordinate frames.
1. A gamma aminobutyric acid (GABAA) receptor agonist, muscimol (Sigma, 5 micrograms/microliters solution), and a GABAB receptor agonist and antagonist, baclofen and phaclofen, respectively, were injected (1.0 microliter) into the dorsal and ventral aspects of the premotor cortex (PM) of two Japanese monkeys (Macaca fuscata), while they were performing a motor task that required wrist flexion or extension to a target. The correct movement was instructed by either 1) a conditional color cue [green or red light emitting diodes (LED)] equidistant from the targets or 2) a directional cue toward extension or flexion (right or left LED). When the green or right LED was illuminated, extension was to be performed. When the red or left LED was illuminated, flexion was required. The movement was triggered by a visual stimulus either simultaneously with the instruction stimulus or after a variable delay. 2. Before drug injection, single-unit recordings were made to select injection sites 1) in the dorsal aspect of the PM (PMd) around the superior precentral sulcus where typical set-related activity was frequently recorded and 2) in the ventral aspect of the PM (PMv) immediately caudal to the genu of the arcuate sulcus where movement-related neurons were densely located. 3. Behavioral deficits were observed primarily at the time muscimol, but not baclofen or phaclofen, was injected. Furthermore, muscimol effects were short-lasting: deficits were most frequently observed during the 10-min injection period but seldom after completion of injection. 4. When muscimol was injected into the PMd, there was an increase in the number of direction errors primarily when the conditional cues were presented. The initiated movements were similar in amplitude and velocity to the preinjection behavior. In contrast, when muscimol was injected into the PMv, many of the initiated movements showed smaller amplitudes and slower velocities, but few direction errors were made. 5. These results suggest that the PMd and PMv play differential roles in motor control: the PMd is more important than PMv in conditional motor behavior and plays a role in the preparation for forthcoming movements. In contrast, the PMv is more specialized for a role in the execution of visually guided movements.
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