Do bimanual motor actions involve the dorsal premotor (PMd), cingulate (CMA) and posterior parietal (PPC) cortices? Comparison with primary and supplementary motor cortical areas

Single neuronal activity was recorded from the dorsal premotor cortex (PMd), the cingulate motor area (CMA) and the posterior parietal cortex (PPC) in two Macaca fascicularis trained to perform a delayed conditional sequence of coordinated pull and grasp movements. The monkey had to perform three types of trials instructed in a random manner: (i) bimanually, using the two hands in a coordinated sequence of movements; (ii) unimanually, using the left hand only; (iii) unimanually, using the right hand only. The aim of this study was first to assess the bilateral relationships of the three cortical areas for unimanual motor control. Second, to establish whether the three cortical areas contain units reflecting bimanual synergy. A total of 255 task-related neurons were recorded from the PMd, CMA and PPC, where most neurons exhibited a significant modulation of activity in both contralateral and ipsilateral unimanual trials (bilateral neurons: 85, 77 and 61%, respectively). Lower proportions of neurons in PMd (7%), CMA (16%) and PPC (6%) were active in unimanual contralateral trials, but not in unimanual ipsilateral trials. The reverse (modulation of activity in ipsilateral but not contralateral unimanual trials) represented 5% of neurons in PMd, 7% in CMA and 3% in PPC. When comparing unimanual and bimanual trials to search evidence for bimanual coordination, 57% of PMd task-related neurons were classified as bimanual, defined as units in which the activity observed in bimanual trials could not be predicted from that associated with unimanual trials when comparing the same events related to the same arm. The proportion of bimanual neurons in CMA (56%) was comparable to that found in PMd (55%), whereas PPC exhibited a higher proportion of bimanual neurons (74%). Furthermore, comparison of the present data with our previous results regarding the supplementary (SMA) and primary (M1) motor cortical areas shows that there is no statistically significant difference between PMd, CMA, SMA and M1 with respect to the proportions of bimanual neurons. Altogether, these results suggest that the five cortical areas PMd, CMA, PPC, SMA and M1 are participating to the control of sequential bimanually coordinated movements. Inter-limb coordination may thus be controlled by a widely distributed network including several cortical and sub-cortical areas.