Neural activity of supplementary and primary motor areas in monkeys and its relation to bimanual and unimanual movement sequences

Abstract

A chronic single-unit study of motor cortical activity was undertaken in two monkeys trained to perform a bimanually coordinated task. The hypothesis was tested that the supplementary motor area plays a specific role in coordinating the two hands for common goal-oriented actions. With this objective, a special search was made for neurons that might exhibit properties exclusively related to bimanual task performance. Monkeys learned to reach for and to pull open a spring-loaded drawer with one hand, while the other hand reached out to grasp food from the drawer recess. The two hands were precisely coordinated for achievement of this goal. Monkeys also performed, in separate blocks of trials, only the pulling or grasping movements, using the same hands as in the bimanual task. Task-related activity of 348 neurons from the supplementary motor area and 341 neurons from the primary motor area, each examined in the bimanual and in both unimanual tasks, was recorded in the two hemispheres. Most neurons from the supplementary motor area were recorded within its caudal microexcitable portion. Contrary to expectation, the proportion of neurons with activity patterns related exclusively to the bimanual task was small, but somewhat higher in the supplementary motor area (5%) than in the primary motor cortex (2%). Another group of neurons that were equally modulated during the bimanual as well as to both unimanual task components might also contribute in controlling bimanual actions. Such “task-dependent” rather than “effector-dependent” activity patterns were more common in neurons of the supplementary motor area (19%) than of the primary motor cortex (5%). Bilateral receptive fields were also more numerous among the supplementary motor area neurons. However, a large majority of neurons from primary and supplementary motor areas had activity profiles clearly related only to contralateral hand movements (65% in the primary motor and 51% in the supplementary motor area). A similar group of neurons showed an additional slight modulation with ipsilateral movements; they were equally common in the two areas (14% and 16%, respectively) and their significance for bimanual coordination is questionable. Summed activity profiles of all neurons recorded in the primary and supplementary motor areas of the same hemisphere were compared. The modulations of the three histograms, corresponding to the two unimanual and the bimanual tasks, were similar for the two motor areas, i.e. prominent with bimanual and contralateral movements and weak with ipsilateral movements. It is concluded that the supplementary motor area is likely to contribute to bimanual coordination, perhaps more than the primary motor cortex, but that it is not a defining function for the former cortical area. Instead, it is suggested that the supplementary motor area is part of a callosally interconnected and distributed network of frontal and parietal cortical areas that together orchestrate bimanual coordination.