Abstract
Hybrid kinetic and kinematic intracortical brain-computer interfaces (iBCIs) have the potential to restore functional grasping and object interaction capabilities in individuals with tetraplegia. This requires an understanding of how kinetic information is represented in neural activity, and how this representation is affected by non-motor parameters such as volitional state (VoS), namely, whether one observes, imagines, or attempts an action. To this end, this work investigates how motor cortical neural activity changes when three human participants with tetraplegia observe, imagine, and attempt to produce three discrete hand grasping forces with the dominant hand. We show that force representation follows the same VoS-related trends as previously shown for directional arm movements; namely, that attempted force production recruits more neural activity compared to observed or imagined force production. Additionally, VoS-modulated neural activity to a greater extent than grasping force. Neural representation of forces was lower than expected, possibly due to compromised somatosensory pathways in individuals with tetraplegia, which have been shown to influence motor cortical activity. Nevertheless, attempted forces (but not always observed or imagined forces) could be decoded significantly above chance, thereby potentially providing relevant information towards the development of a hybrid kinetic and kinematic iBCI.
Highlights
We characterize the topography of the neural space representing force and volitional state in three individuals with tetraplegia, both at the level of single neural features extracted from multiunit intracortical activity, and at the level of the neural population
A major goal of this study was to determine whether force-related tuning was present at the level of single neural features extracted from multiunit intracortical activity (Fig. 1A), and to assess the extent to which volitional state affected this tuning
Threshold crossing (TC) features, defined as the number of times the neural activity crossed a pre-defined, channel-specific noise threshold, are numbered from 1–192 according to the recording electrode from which they originate
Summary
Intracortical brain-computer interfaces (iBCIs) that command neuroprosthetics have the potential to restore lost or compromised function to individuals with tetraplegia. iBCIs typically detect neural activity from motor cortex, which encodes kinetic and kinematic information in rhesus macaques1–14. iBCIs that extract kinematic parameters have allowed individuals to command one- and two-dimensional computer cursors[15,16,17,18,19,20,21,22,23,24,25,26], prosthetics[27,28,29], and functional electrical stimulation of paralyzed muscles[30,31]. Additional work has characterized closed-loop kinetic control in nonhuman primates[32,33,34] and open-loop force modulation in human participants[35,36] These studies could potentially move iBCI technology towards restoring functional tasks requiring both kinetic and kinematic control. In individuals with tetraplegia, observed, imagined, and attempted arm reaches recruit shared neural populations, but yield unique patterns of activity[44] This supports the existence of a “core” network that modulates to all volitional states, and the recruitment of additional neural circuitry during the progression from passive observation to attempted movement[44,45,46,47,48]. We show that 1) volitional state affects how neural activity modulates to force; namely, that attempted forces generate stronger cortical modulation than observed and imagined forces; 2) grasping forces are reliably decoded when attempted, but not always when observed or imagined, and 3) volitional state is represented to a greater degree than grasping forces in the motor cortex
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