| Labeling corticospinal neurons with retrograde tracers injected in the cervical segments of the spinal cord of macaque rhesus, has revealed multiple corticospinal output zones in both the lateral and the medial aspect of the hemisphere of the frontal lobe. Seven distinct forelimb motor representations have been identified including the primary motor cortex (M1) and six secondary motor areas. These include, the supplementary motor area (SMA), the dorsal, ventral and rostral cingulate motor areas (CMAd, CMAv, and CMAr), and the dorsal and the ventral premotor areas (PMd and PMv). Extensive data on the properties of M1 have already been published, and the direct linkage of its corticospinal neurons on motoneurons has been demonstrated. While the location and distribution of the corticospinal neurons from the secondary motor areas have been described in great detail, their specific roles in limb movement and the extent of their linkage on motoneurons remain much less understood. The broad objective of this study was to characterize the motor output properties of SMA, CMAd, PMd and PMv and to compare their roles in the control of forelimb movements to those from M1. Stimulus-triggered-averaging (StTA) of electromyography (EMG) activity was used to map and characterize their output properties in terms of sign (excitatory or inhibitory), latency, strength, and distribution of effects. Our results demonstrate that effects from SMA, CMAd, PMd and PMV have longer latencies and are markedly weaker than those from M1, suggesting additional synapses in the anatomical pathway for their actions on motoneurons. Moreover, facilitation effects from SMA, CMAd, PMd and PMv did not follow the pattern of increased magnitudes of effects from proximal to distal muscles characteristic of M1. In terms of their organization, no clear segregated representations of proximal versus distal muscles were found in the secondary motor areas compared to M1, in which the existence of segregated proximal and distal muscle representations was demonstrated. Our results raise doubts about the role of the corticospinal neurons from SMA, CMAd, PMd and PMv in the direct control of forelimb motoneurons and suggest that their effects on muscular activity are most likely achieved indirectly through projections to M1 and/or to the intermediate zone of the spinal cord. |
