Differential modulation of local field potentials in the primary and premotor cortices during ipsilateral and contralateral reach to grasp in macaque monkeys.

Abstract

Hand movements are associated with modulations of neuronal activity across several interconnected cortical areas, including the primary motor cortex (M1), and the dorsal and ventral premotor cortices (PMd and PMv). Local field potentials (LFPs) provide a link between neuronal discharges and synaptic inputs. Our current understanding of how LFPs vary in M1, PMd, and PMv during contralateral and ipsilateral movements is incomplete. To help reveal unique features in the pattern of modulations, we simultaneously recorded LFPs in these areas in two macaque monkeys performing reach and grasp movements with either the right or left hand. The greatest effector-dependent differences were seen in M1, at low (≤ 13 Hz) and gamma frequencies. In premotor areas, differences related to hand use were only present in low frequencies. PMv exhibited the greatest increase in low frequencies during instruction cues and the smallest effector-dependent modulation during movement execution. In PMd, delta oscillations were greater during contralateral reach and grasp, and beta activity increased during contralateral grasp. In contrast, beta oscillations decreased in M1 and PMv. These results suggest that while M1 primarily exhibits effector-specific LFP activity, premotor areas compute more effector-independent aspects of the task requirements, particularly during movement preparation for PMv and production for PMd. The generation of precise hand movements likely relies on the combination of complementary information contained in the unique pattern of neural modulations contained in each cortical area. Accordingly, integrating LFPs from premotor areas and M1 could enhance the performance and robustness of brain-machine interfaces.Significance Statement We compared local field potentials (LFPs) from the primary motor cortex (M1), the dorsal and ventral premotor cortices (PMd and PMv) while monkeys performed reach and grasp with the contralateral or ipsilateral hand. In general, hand-related differences were greater in M1 than in premotor areas. During both contralateral and ipsilateral trials, LFPs were more similar when comparing the two premotor areas than comparing M1 to PMd or PMv. However, the pattern of modulations in each area had unique features. The combination of these signals is likely essential to support the flexibility and complexity of unilateral hand movements. Our results help to understand the neural substrate that allows cortical areas to concurrently contribute to different aspects of movement planning and production.