Motor-related brain activity during action observation: a neural substrate for electrocorticographic brain-computer interfaces after spinal cord injury

After spinal cord injury (SCI), motor commands from the brain are unable to reach peripheral nerves and muscles below the level of the lesion. Action observation (AO), in which a person observes someone else performing an action, has been used to augment traditional rehabilitation paradigms. Similarly, AO can be used to derive the relationship between brain activity and movement kinematics for a motor-based brain-computer interface (BCI) even when the user cannot generate overt movements. BCIs use brain signals to control external devices to replace functions that have been lost due to SCI or other motor impairment. Previous studies have reported congruent motor cortical activity during observed and overt movements using magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI). Recent single-unit studies using intracortical microelectrodes also demonstrated that a large number of motor cortical neurons had similar firing rate patterns between overt and observed movements. Given the increasing interest in electrocorticography (ECoG)-based BCIs, our goal was to identify whether action observation-related cortical activity could be recorded using ECoG during grasping tasks. Specifically, we aimed to identify congruent neural activity during observed and executed movements in both the sensorimotor rhythm (10-40 Hz) and the high-gamma band (65-115 Hz) which contains significant movement-related information. We observed significant motor-related high-gamma band activity during AO in both able-bodied individuals and one participant with a complete C4 SCI. Furthermore, in able-bodied participants, both the low and high frequency bands demonstrated congruent activity between action execution and observation. Our results suggest that AO could be an effective and critical procedure for deriving the mapping from ECoG signals to intended movement for an ECoG-based BCI system for individuals with paralysis.