Sequential activation of premotor, primary somatosensory and primary motor areas in humans during cued finger movements

•Using onset of high gamma activities in human electrocorticography, the authors capture sequential activation of premotor, somatosensory and primary motor regions in preparation for voluntary movements.•The fact that sensory neurons led motor neurons in activation in movement planning supports the notion of the efference copy.•Premotor neurons, rather motor neurons, modulate the activities of sensory neurons in preparation for human voluntary movements.

ObjectiveHuman voluntary movements are a final product of complex interactions between multiple sensory, cognitive and motor areas of central nervous system. The objective was to investigate temporal sequence of activation of premotor (PM), primary motor (M1) and somatosensory (S1) areas during cued finger movements.MethodsElectrocorticography (ECoG) was used to measure activation timing in human PM, S1, and M1 neurons in preparation for finger movements in 5 subjects with subdural grids for seizure localization. Cortical activation was determined by the onset of high gamma (HG) oscillation (70–150 Hz). The three cortical regions were mapped anatomically using a common brain atlas and confirmed independently with direct electrical cortical stimulation, somatosensory evoked potentials and detection of HG response to tactile stimulation. Subjects were given visual cues to flex each finger or pinch the thumb and index finger. Movements were captured with a dataglove and time-locked with ECoG. A windowed covariance metric was used to identify the rising slope of HG power between two electrodes and compute time lag. Statistical constraints were applied to the time estimates to combat the noise. Rank sum testing was used to verify the sequential activation of cortical regions across 5 subjects.ResultsIn all 5 subjects, HG activation in PM preceded S1 by an average of 53 ± 13 ms (P = 0.03), PM preceded M1 by 180 ± 40 ms (P = 0.001) and S1 activation preceded M1 by 136 ± 40 ms (P = 0.04).ConclusionsSequential HG activation of PM, S1 and M1 regions in preparation for movements is reported. Activity in S1 prior to any overt body movements supports the notion that these neurons may encode sensory information in anticipation of movements, i.e., an efference copy. Our analysis suggests that S1 modulation likely originates from PM.SignificanceFirst electrophysiological evidence of efference copy in humans.