Hai Sun1, Timothy M Blakely2, Felix Darvas3, Jeremiah D Wander2, Lise A Johnson4, David K Su5, Kai J Miller6, Eberhard E Fetz7, Jeffery G Ojemann8. 1. Department of Neurological Surgery, Oregon Health & Science University, Portland, OR, USA; Department of Neurological Surgery, University of Washington, Seattle, WA, USA. Electronic address: hai.sun@bnaneuro.net. 2. Department of Bioengineering, University of Washington, Seattle, WA, USA. 3. Department of Neurological Surgery, University of Washington, Seattle, WA, USA; Department of Bioengineering, University of Washington, Seattle, WA, USA. 4. Department of Neurological Surgery, University of Washington, Seattle, WA, USA; The Center for Sensorimotor Neural Engineering, Seattle, WA, USA. 5. Department of Neurological Surgery, University of Washington, Seattle, WA, USA. 6. Neurobiology and Behavior Degree Program, University of Washington, Seattle, WA, USA. 7. The Center for Sensorimotor Neural Engineering, Seattle, WA, USA; Neurobiology and Behavior Degree Program, University of Washington, Seattle, WA, USA; Department of Physiology and Biophysics, University of Washington, Seattle, WA, USA. 8. Department of Neurological Surgery, University of Washington, Seattle, WA, USA; Department of Bioengineering, University of Washington, Seattle, WA, USA; The Center for Sensorimotor Neural Engineering, Seattle, WA, USA; Seattle Children's Hospital, Seattle, WA, USA.
Abstract
OBJECTIVE: Human 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. METHODS: Electrocorticography (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 (70-150Hz). 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. RESULTS: In all 5 subjects, HG activation in PM preceded S1 by an average of 53±13ms (P=0.03), PM preceded M1 by 180±40ms (P=0.001) and S1 activation preceded M1 by 136±40ms (P=0.04). CONCLUSIONS: Sequential 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. SIGNIFICANCE: First electrophysiological evidence of efference copy in humans.
OBJECTIVE:Humanvoluntary 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. METHODS: Electrocorticography (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 (70-150Hz). 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. RESULTS: In all 5 subjects, HG activation in PM preceded S1 by an average of 53±13ms (P=0.03), PM preceded M1 by 180±40ms (P=0.001) and S1 activation preceded M1 by 136±40ms (P=0.04). CONCLUSIONS: Sequential 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. SIGNIFICANCE: First electrophysiological evidence of efference copy in humans.
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