Abstract
The organizing principle of human motor cortex 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 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? 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 functional magnetic resonance imaging and magnetoencephalography, a spatial and temporal multivariate representational similarity analysis revealed encoding of kinematic information in more caudal regions of M1, over 200 ms before movement onset. In contrast, patterns of muscle activity were encoded in more rostral motor regions much later after movements began. We provide compelling evidence that top-down control of dexterous movement engages kinematic representations in caudal regions of M1 prior to movement production.
Highlights
Mounting evidence supports the encoding of movements in M1 based on kinematics and synergistic muscle activation, rather than the anatomy of the peripheral musculature (Overduin et al 2012, 2015)
We addressed this question using a spatiotemporal multivariate representational similarity analysis (RSA) to ask where in the human brain and when during movement production are the kinematics of human hand movements encoded? This approach combined high-field functional magnetic resonance imaging (fMRI) and magnetoencephalography (MEG) data with kinematic data glove recordings made during a broad repertoire of prehensile and nonprehensile hand movements
Spearman’s ρ surface maps for each model were subject to an omnibus threshold (α = 0.01) and used to construct a cross-participant heatmap. This analysis assessed where the relative dissimilarities in the kinematic, muscle and ethological actions across the different hand movements were mirrored by the relative differences in the pattern of fMRI activity elicited by performing the same movements
Summary
Mounting evidence supports the encoding of movements in M1 based on kinematics and synergistic muscle activation, rather than the anatomy of the peripheral musculature (Overduin et al 2012, 2015). Evidence of neuronal tuning to multiple kinematic features has been reported during the production of intended movements from M1 microelectrode recordings. The functional relevance of kinematic encoding in M1 to human motor control remains a fundamental unknown. As well as their role in motor output, M1 neurons exhibit rapid and integrative responses to somatosensory signals (Hatsopoulos and Suminski 2011; Pruszynski et al 2011). Are kinematic motor representations reported in human M1 functionally relevant in the process of top-down motor control, or an epiphenomenon generated by bottom-up sensory feedback during human movement production?
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