jneJNEOBHJournal of Neural EngineeringJNEJ. Neural Eng.1741-25601741-2552IOP Publishingjneac63e810.1088/1741-2552/ac63e8ac63e8JNE-105022.R1PaperCharacterizing the short-latency evoked response to intracortical microstimulation across a multi-electrode array0000-0001-5108-8901SombeckJoseph T10000-0002-4896-7603HeyeJuliet20000-0002-7619-322XKumaraveluKarthik50000-0002-1944-0714GoetzStefan M68910110000-0002-4385-065XPeterchevAngel V5689100000-0001-5240-6588GrillWarren M5678100000-0003-4039-9135BensmaiaSliman1213140000-0001-8675-7140MillerLee E1234*lm@northwestern.edu Department of Biomedical Engineering, Northwestern University, Evanston, IL, United States of America Department of Neuroscience, Northwestern University, Chicago, IL, United States of America Department of Physical Medicine and Rehabilitation, Northwestern University, Chicago, IL, United States of America Shirley Ryan AbilityLab, Chicago, IL, United States of America Department of Biomedical Engineering, Duke University, Durham, NC, United States of America Department of Electrical and Computer Engineering, Duke University, Durham, NC, United States of America Department of Neurobiology, Duke University, Durham, NC, United States of America Department of Neurosurgery, Duke University, Durham, NC, United States of America Department of Psychiatry and Behavioral Sciences, Duke University, Durham, NC, United States of America Duke Institute for Brain Sciences, Duke University, Durham, NC, United States of America Department of Engineering, University of Cambridge, Cambridge, United Kingdom Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL, United States of America Committee on Computational Neuroscience, University of Chicago, Chicago, IL, United States of America Neuroscience Institute, University of Chicago, Chicago, IL, United States of America

Author to whom any correspondence should be addressed.

014202220420222042022192026044121120218220224420221522022© 2022 The Author(s). Published by IOP Publishing Ltd2022 Original content from this work may be used under the terms of the Creative Commons Attribution 4.0 license. Any further distribution of this work must maintain attribution to the author(s) and the title of the work, journal citation and DOI.Abstract

Objective. Persons with tetraplegia can use brain-machine interfaces to make visually guided reaches with robotic arms. Without somatosensory feedback, these movements will likely be slow and imprecise, like those of persons who retain movement but have lost proprioception. Intracortical microstimulation (ICMS) has promise for providing artificial somatosensory feedback. ICMS that mimics naturally occurring neural activity, may allow afferent interfaces that are more informative and easier to learn than stimulation evoking unnaturalistic activity. To develop such biomimetic stimulation patterns, it is important to characterize the responses of neurons to ICMS. Approach. Using a Utah multi-electrode array, we recorded activity evoked by both single pulses and trains of ICMS at a wide range of amplitudes and frequencies in two rhesus macaques. As the electrical artifact caused by ICMS typically prevents recording for many milliseconds, we deployed a custom rapid-recovery amplifier with nonlinear gain to limit signal saturation on the stimulated electrode. Across all electrodes after stimulation, we removed the remaining slow return to baseline with acausal high-pass filtering of time-reversed recordings. Main results. After single pulses of stimulation, we recorded what was likely transsynaptically-evoked activity even on the stimulated electrode as early as ∼0.7 ms. This was immediately followed by suppressed neural activity lasting 10–150 ms. After trains, this long-lasting inhibition was replaced by increased firing rates for ∼100 ms. During long trains, the evoked response on the stimulated electrode decayed rapidly while the response was maintained on non-stimulated channels. Significance. The detailed description of the spatial and temporal response to ICMS can be used to better interpret results from experiments that probe circuit connectivity or function of cortical areas. These results can also contribute to the design of stimulation patterns to improve afferent interfaces for artificial sensory feedback.

intracortical microstimulationsomatosensorymonkeybrain computer interfaceNational Institute of Neurological Disorders and Strokehttp://dx.doi.org/10.13039/100000065 F31NS115478NS095251National Institute of HealthT32HD07418ccc1741-2552/22/026044+17$33.00printedPrinted in the UKcrossmarkyes