Modulation of Neural Variability in Premotor, Motor, and Posterior Parietal Cortex during Change of Motor Intention.

ABSTRACT

The time course of neural variability was studied in three nodes of the parieto-frontal system the dorsal premotor cortex (PMd, area 6), primary motor cortex (MI, area 4), and posterior parietal cortex (PPC, area 5) while monkeys made either direct reaches to visual targets or changed reach direction in response to an unexpected change of target location. These areas are crucial nodes in the distributed control of reaching and their lesion impairs trajectory formation and correction under different circumstances. During unperturbed reaches, neural variability declined before the onset of hand movement in both frontal and parietal cortex. When the original motor intention suddenly changed, neural variability displayed a complex and area-specific modulation because the perturbation of the motor state was signaled earlier in PMd than in MI and PPC. The comparison of perturbed versus unperturbed reaches revealed that, in the time between the onset of correction signal and trajectory change, identical hand movements were associated with different, therefore context-dependent, patterns of neural variability induced by the instruction to change hand movement direction. In PMd, neural variability was higher before the initiation of hand reach than before its correction, thus providing a neural underpinning to the phenomenon that it takes less time to correct than to initiate hand movement. Furthermore, neural variability was an excellent predictor of slow and fast reach corrections because it was lower during the latter than the former. We conclude that the analysis of neural variability can be an important tool for the study of complex forms of motor cognition. SIGNIFICANCE STATEMENT No single study has been performed on neural variability during update of motor intention across monkey premotor, motor, and posterior parietal cortex. In perturbed reaches, target location changed unexpectedly during reaction time and the correction of hand trajectory required updating the original motor plan. Comparing unperturbed versus perturbed reaches revealed that neural variability displayed a complex context- and area-dependent pattern of modulation because, before trajectory correction, similar initial hand movements were associated with different patterns of variability depending on the instruction signal, and therefore on the future hand path and final destination. Furthermore, neural variability predicted both slow and fast hand movement corrections, also offering a neural underpinning to the phenomenon that it takes less time to correct than to initiate hand movement.