Neural activity in monkey dorsal and ventral cingulate motor areas: comparison with the supplementary motor area.

Abstract

The cingulate motor areas are a recently discovered group of discrete cortical regions located in the cingulate sulcus with direct connections to the primary motor cortex and spinal cord. Although much is known about their anatomical relationship with other motor areas, relatively little is known about their functional neurophysiology. We investigated neural mechanisms of motor processing in the dorsal and ventral cingulate motor areas (CMAd and CMAv) during two-dimensional visually guided arm movements. Single-neuron activity in CMAd and CMAv was recorded during an instructed delay task requiring combined elbow and shoulder movements. Neural activity associated with the onset of a visual cue (signal activity), delay (set activity), and motor response (movement activity) were assessed, and their onset time, duration, magnitude, and parameters of directional specificity were calculated. To determine how CMAd and CMAv compared with other premotor areas, we also analyzed the activity of neurons in the supplementary motor area (SMA) during the same task in the same monkeys. Comparison of CMAd, CMAv, and SMA revealed remarkably similar response properties. All three areas contained signal, set, and movement activity in similar proportions and in all possible combinations within single neurons. The average onset time of signal and set activity and the duration of signal activity were not significantly different across areas. The directional tuning of activities in all three areas were uniformly distributed and highly correlated within the same neuron. There were, however, some notable differences in movement activity between motor areas. Neurons with only movement activity were more numerous in CMAd and CMAv, whereas neurons with both set and movement activity were more prevalent in SMA. Furthermore, movement activity in SMA began earlier and had a shorter duration than movement activity in CMAd and CMAv, although there was substantial overlap in their distributions. These results indicate that CMAd and CMAv participate in the visual guidance of limb movements using similar neurophysiological mechanisms as SMA. The earlier average onset and shorter duration of movement activity in SMA suggest a more prominent role for this area in movement initiation, whereas the later onset and longer duration of movement activity in CMAd and CMAv suggest a more influential role in movement execution. Notwithstanding these differences, however, the remarkable similarities in response types and their combinatorial organization within single neurons across all cortical areas attests to the parallel organization and distributed nature of information processing in these three motor areas.