Action kinematics as an organising principle in the cortical control of human hand movement

Hand movements are controlled by neuronal networks in primary motor cortex (M1). The organising principle encoding hand movements in M1 does not follow an anatomical body map, but rather a distributed representational structure in which motor primitives are combined to produce motor outputs. Electrophysiological recordings in primates suggest that M1 neurons encode kinematic features of movements, such as joint position and velocity. Human imaging data concur: relative differences in movement kinematics are mirrored by differences in the associated patterns of M1 activity. However, M1 exhibits well-documented sensory responses to cutaneous and proprioceptive stimuli, raising questions regarding the origins of kinematic motor representations: are they relevant in top-down motor control, or are they an epiphenomenon of bottom-up sensory feedback during movement? Here we show that the kinematic signature of a wide variety of naturalistic hand movements is encoded in human M1 prior to the point of movement initiation. Using a powerful combination of high-field fMRI and MEG, a spatial and temporal multivariate representational similarity analysis revealed that patterns of M1 activity mirrored kinematic, but not muscle-based features of naturalistic hand movements prior to movement onset. Comparable M1 activity was not observed for an ethological action model based functional mappings proposed in M1. Our spatial and temporal analyses provide firm evidence that the top-down control of dexterous movements activates cortical networks in M1 encoding hand kinematics.