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

Abstract

Hand movements are controlled by neuronal networks in primary motor cortex (M1). The organising principle 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. Both electrophysiological recordings in primates and human imaging data suggest that M1 encodes kinematic features of movements, such as joint position and velocity. 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? Moreover, to what extent is information related to muscle activity encoded in motor cortex? Here we provide evidence for spatially and temporally distinct encoding of kinematic and muscle information in human M1 during the production of a wide variety of naturalistic hand movements. Using a powerful combination of high-field fMRI and MEG, a spatial and temporal multivariate representational similarity analysis revealed encoding of kinematic information from data glove recordings in more caudal regions of M1, over 200ms before movement onset. In contrast, patterns of muscle activity from EMG were encoded in more rostral motor regions later in the cycle of movement. Our spatial and temporal analysis provide compelling evidence that top-down control of dexterous movement engages kinematic representations in caudal regions of M1 prior to movement production; an area with direct cortico-motorneuronal connections. Muscle information encoded more rostrally in M1 was engaged later, suggestive of involvement in bottom-up signalling.