Noninvasively recorded high-gamma signals improve synchrony of force feedback in a novel neurorehabilitation brain–machine interface for brain injury

Abstract

Abstract Objective. Brain injury is the leading cause of long-term disability worldwide, often resulting in impaired hand function. Brain–machine interfaces (BMIs) offer a potential way to improve hand function. BMIs often target replacing lost function, but may also be employed in neurorehabilitation (nrBMI) by facilitating neural plasticity and functional recovery. Here, we report a novel nrBMI capable of acquiring high-γ (70–115 Hz) information through a unique post-traumatic brain injury (TBI) hemicraniectomy window model, and delivering sensory feedback that is synchronized with, and proportional to, intended grasp force. Approach. We developed the nrBMI to use electroencephalogram recorded over a hemicraniectomy (hEEG) in individuals with TBI. The nrBMI empowered users to exert continuous, proportional control of applied force, and provided continuous force feedback. We report the results of an initial testing group of three human participants with TBI, along with a control group of three skull- and motor-intact volunteers. Main results. All participants controlled the nrBMI successfully, with high initial success rates (2 of 6 participants) or performance that improved over time (4 of 6 participants). We observed high-γ modulation with force intent in hEEG but not skull-intact EEG. Most significantly, we found that high-γ control significantly improved the timing synchronization between neural modulation onset and nrBMI output/haptic feedback (compared to low-frequency nrBMI control). Significance. These proof-of-concept results show that high-γ nrBMIs can be used by individuals with impaired ability to control force (without immediately resorting to invasive signals like electrocorticography). Of note, the nrBMI includes a parameter to change the fraction of control shared between decoded intent and volitional force, to adjust for recovery progress. The improved synchrony between neural modulations and force control for high-γ signals is potentially important for maximizing the ability of nrBMIs to induce plasticity in neural circuits. Inducing plasticity is critical to functional recovery after brain injury.