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Invasive brain-machine interfaces can help restore function through the control of external devices while the addition of intracortical microstimulation (ICMS) can elicit sensations of touch and help provide further benefits for individuals living with sensorimotor deficits. However, the extent of tactile information that can be conveyed through ICMS has not been fully explored. In a human participant with spinal cord injury and chronically implanted microelectrode arrays, we used ICMS to the somatosensory cortex to provide grip force feedback in the hands during grasping of objects with varying stiffness with a robotic arm. Using only ICMS-evoked touch sensations, the participant was able to identify between two and three objects with an accuracy of 92% and 67%, respectively. In a compliant grasping task with the goal of grasping a delicate object without crushing it, objects were deformed on average only 2.8 mm with ICMS-based touch feedback compared to 8.7 mm without. These results demonstrate that ICMS-evoked touch sensations to the hands can be used to provide force-based feedback for perceiving object properties and enable more precise grasping during closed-loop control of a robotic limb through a cortical interface.

Advances in intelligent robotic systems and brain-machine interfaces (BMI) have helped restore functionality and independence to individuals living with sensorimotor deficits; however, tasks requiring bimanual coordination and fine manipulation continue to remain unsolved given the technical complexity of controlling multiple degrees of freedom (DOF) across multiple limbs in a coordinated way through a user input. To address this challenge, we implemented a collaborative shared control strategy to manipulate and coordinate two Modular Prosthetic Limbs (MPL) for performing a bimanual self-feeding task. A human participant with microelectrode arrays in sensorimotor brain regions provided commands to both MPLs to perform the self-feeding task, which included bimanual cutting. Motor commands were decoded from bilateral neural signals to control up to two DOFs on each MPL at a time. The shared control strategy enabled the participant to map his four-DOF control inputs, two per hand, to as many as 12 DOFs for specifying robot end effector position and orientation. Using neurally-driven shared control, the participant successfully and simultaneously controlled movements of both robotic limbs to cut and eat food in a complex bimanual self-feeding task. This demonstration of bimanual robotic system control via a BMI in collaboration with intelligent robot behavior has major implications for restoring complex movement behaviors for those living with sensorimotor deficits., Competing Interests: DH is inventor on intellectual property pertaining to robotic manipulation. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest., (Copyright © 2022 Handelman, Osborn, Thomas, Badger, Thompson, Nickl, Anaya, Wormley, Cantarero, McMullen, Crone, Wester, Celnik, Fifer and Tenore.)

Understanding the cortical representations of movements and their stability can shed light on improved brain-machine interface (BMI) approaches to decode these representations without frequent recalibration. Here, we characterize the spatial organization (somatotopy) and stability of the bilateral sensorimotor map of forearm muscles in an incomplete-high spinal-cord injury study participant implanted bilaterally in the primary motor and sensory cortices with Utah microelectrode arrays (MEAs). We built representation maps by recording bilateral multiunit activity (MUA) and surface electromyography (EMG) as the participant executed voluntary contractions of the extensor carpi radialis (ECR), and attempted motions in the flexor carpi radialis (FCR), which was paralytic. To assess stability, we repeatedly mapped and compared left- and right-wrist-extensor-related activity throughout several sessions, comparing somatotopy of active electrodes, as well as neural signals both at the within-electrode (multiunit) and cross-electrode (network) levels. Wrist motions showed significant activation in motor and sensory cortical electrodes. Within electrodes, firing strength stability diminished as the time increased between consecutive measurements (hours within a session, or days across sessions), with higher stability observed in sensory cortex than in motor, and in the contralateral hemisphere than in the ipsilateral. However, we observed no differences at network level, and no evidence of decoding instabilities for wrist EMG, either across timespans of hours or days, or across recording area. While map stability differs between brain area and hemisphere at multiunit/electrode level, these differences are nullified at ensemble level., (© 2022. The Author(s).)

Background and Objectives: The restoration of touch to fingers and fingertips is critical to achieving dexterous neuroprosthetic control for individuals with sensorimotor dysfunction. However, localized fingertip sensations have not been evoked via intracortical microstimulation (ICMS)., Methods: Using a novel intraoperative mapping approach, we implanted electrode arrays in the finger areas of left and right somatosensory cortex and delivered ICMS over a 2-year period in a human participant with spinal cord injury., Results: Stimulation evoked tactile sensations in 8 fingers, including fingertips, spanning both hands. Evoked percepts followed expected somatotopic arrangements. The subject was able to reliably identify up to 7 finger-specific sites spanning both hands in a finger discrimination task. The size of the evoked percepts was on average 33% larger than a finger pad, as assessed via manual markings of a hand image. The size of the evoked percepts increased modestly with increased stimulation intensity, growing 21% as pulse amplitude increased from 20 to 80 µA. Detection thresholds were estimated on a subset of electrodes, with estimates of 9.2 to 35 µA observed, roughly consistent with prior studies., Discussion: These results suggest that ICMS can enable the delivery of consistent and localized fingertip sensations during object manipulation by neuroprostheses for individuals with somatosensory deficits., Clinicaltrialsgov Identifier: NCT03161067., (© 2021 American Academy of Neurology.)

Advances in brain-machine interfaces have helped restore function and independence for individuals with sensorimotor deficits; however, providing efficient and effective sensory feedback remains challenging. Intracortical microstimulation (ICMS) of sensorimotor brain regions is a promising technique for providing bioinspired sensory feedback. In a human participant with chronically-implanted microelectrode arrays, we provided ICMS to the primary somatosensory cortex to generate tactile percepts in his hand. In a 3-choice object identification task, the participant identified virtual objects using tactile sensory feedback and no visual information. We evaluated three different stimulation paradigms, each with a different weighting of the grip force and its derivative, to explore the potential benefits of a more bioinspired stimulation strategy. In all paradigms, the participant's ability to identify the objects was above-chance, with object identification accuracy reaching 80% correct when using only sustained grip force feedback and 76.7% when using equal weighting of both sustained grip force and its derivative. These results demonstrate that bioinspired ICMS can provide sensory feedback that is functionally beneficial in sensorimotor tasks. Designing more efficient stimulation paradigms is important because it will allow us to 1) provide safer stimulation delivery methods that reduce overall injected charge without sacrificing function and 2) more effectively transmit sensory information to promote intuitive integration and usage by the human body.

Defining eloquent cortex intraoperatively, traditionally performed by neurosurgeons to preserve patient function, can now help target electrode implantation for restoring function. Brain-machine interfaces (BMIs) have the potential to restore upper-limb motor control to paralyzed patients but require accurate placement of recording and stimulating electrodes to enable functional control of a prosthetic limb. Beyond motor decoding from recording arrays, precise placement of stimulating electrodes in cortical areas associated with finger and fingertip sensations allows for the delivery of sensory feedback that could improve dexterous control of prosthetic hands. In this study, the authors demonstrated the use of a novel intraoperative online functional mapping (OFM) technique with high-density electrocorticography to localize finger representations in human primary somatosensory cortex. In conjunction with traditional pre- and intraoperative targeting approaches, this technique enabled accurate implantation of stimulating microelectrodes, which was confirmed by postimplantation intracortical stimulation of finger and fingertip sensations. This work demonstrates the utility of intraoperative OFM and will inform future studies of closed-loop BMIs in humans.

Volitional rhythmic motor behaviors such as limb cycling and locomotion exhibit spatial and timing regularity. Such rhythmic movements are executed in the presence of exogenous visual and nonvisual cues, and previous studies have shown the pivotal role that vision plays in guiding spatial and temporal regulation. However, the influence of nonvisual information conveyed through auditory or touch sensory pathways, and its effect on control, remains poorly understood. To characterize the function of nonvisual feedback in rhythmic arm control, we designed a paddle juggling task in which volunteers bounced a ball off a rigid elastic surface to a target height in virtual reality by moving a physical handle with the right hand. Feedback was delivered at two key phases of movement: visual feedback at ball peaks only and simultaneous audio and haptic feedback at ball-paddle collisions. In contrast to previous work, we limited visual feedback to the minimum required for jugglers to assess spatial accuracy, and we independently perturbed the spatial dimensions and the timing of feedback. By separately perturbing this information, we evoked dissociable effects on spatial accuracy and timing, confirming that juggling, and potentially other rhythmic tasks, involves two complementary processes with distinct dynamics: spatial error correction and feedback timing synchronization. Moreover, we show evidence that audio and haptic feedback provide sufficient information for the brain to control the timing synchronization process by acting as a metronome-like cue that triggers hand movement. NEW & NOTEWORTHY Vision contains rich information for control of rhythmic arm movements; less is known, however, about the role of nonvisual feedback (touch and sound). Using a virtual ball bouncing task allowing independent real-time manipulation of spatial location and timing of cues, we show their dissociable roles in regulating motor behavior. We confirm that visual feedback is used to correct spatial error and provide new evidence that nonvisual event cues act to reset the timing of arm movements.