Neuronal correlates of grip coding in freely moving monkeys

The investigation of cortical mechanisms underlying the organization of manual actions has so far emphasized the distal components of hand shaping and finger control for grasping as a defining feature of the ventral premotor cortex. An untested assumption of this perspective is that the selectivity of ventral premotor neurons for specific grip types remains consistent when the same object is grasped from different spatial positions - and hence with different body postures - during unconstrained grasping actions. In this study, we tested this hypothesis by recording single-neuron activity from the ventral premotor cortex of two freely moving rhesus macaques, using chronically implanted floating multielectrode arrays and a 128-channel data logging system. During recordings, the monkeys grasped the same two objects - a large and a small sphere - using a Whole Hand (WH) grip and a Precision Grip (PG), respectively, while the objects were positioned in various locations within the home cage: on the ceiling, on a lower or upper part of the cage wall, or on a shelf. Each object location required different body postures to reach, grasp, and pull: standing and facing upward, sitting and facing forward, or sitting and facing downward with the back slightly bent or straight. We recorded a total of 288 neurons, of which 54 showed no modulation during grasping actions, while the remaining 234 neurons exhibited significant modulation during grasping in at least one position. The proportion of modulated neurons was consistent across positions, as was the fraction of grip-selective neurons. Some neurons (n=99) showed no grip selectivity in any of the four positions. Among grip-selective neurons, only 4 cells (3%) maintained the same grip selectivity across all tested positions, 9 neurons (7%) exhibited the same selectivity in three positions, 23 neurons (17%) in two positions, and the majority (n=79, 58%) encoded the grip type exclusively in one of the four positions. Notably, a substantial fraction of grip-selective neurons (n=20, 15%) displayed different grip tuning depending on the object’s location. We subsequently conducted a head-free intracortical microstimulation (ICMS) study, observing evoked axio-proximal movements involving the head, forelimb, and face/mouth. We found that stimulation at sites with grip-selective and grasp-related neurons predominantly evoked axio-proximal responses (43% at grip sites and 52.6% at grasp sites), while hand responses were observed less frequently (12.8% at grip sites and 12.3% at grasp sites). These results suggest a substantial dependence of distal grip selectivity in premotor neuron activity on the axio-proximal postural component that accompanies the execution of grasping actions.