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Dynamic peripheral nerve stimulation can produce cortical activation similar to punctate mechanical stimuli

During contact, phasic and tonic responses provide feedback that is used for task performance and perceptual processes. These disparate temporal dynamics are carried in peripheral nerves, and produce overlapping signals in cortex. Using longitudinal intrafascicular electrodes inserted into the media...

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Autores principales: Tanner, Justin, Keefer, Edward, Cheng, Jonathan, Helms Tillery, Stephen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10079952/
https://www.ncbi.nlm.nih.gov/pubmed/37033904
http://dx.doi.org/10.3389/fnhum.2023.1083307
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author Tanner, Justin
Keefer, Edward
Cheng, Jonathan
Helms Tillery, Stephen
author_facet Tanner, Justin
Keefer, Edward
Cheng, Jonathan
Helms Tillery, Stephen
author_sort Tanner, Justin
collection PubMed
description During contact, phasic and tonic responses provide feedback that is used for task performance and perceptual processes. These disparate temporal dynamics are carried in peripheral nerves, and produce overlapping signals in cortex. Using longitudinal intrafascicular electrodes inserted into the median nerve of a nonhuman primate, we delivered composite stimulation consisting of onset and release bursts to capture rapidly adapting responses and sustained stochastic stimulation to capture the ongoing response of slowly adapting receptors. To measure the stimulation’s effectiveness in producing natural responses, we monitored the local field potential in somatosensory cortex. We compared the cortical responses to peripheral nerve stimulation and vibrotactile/punctate stimulation of the fingertip, with particular focus on gamma band (30–65 Hz) responses. We found that vibrotactile stimulation produces consistently phase locked gamma throughout the duration of the stimulation. By contrast, punctate stimulation responses were phase locked at the onset and release of stimulation, but activity maintained through the stimulation was not phase locked. Using these responses as guideposts for assessing the response to the peripheral nerve stimulation, we found that constant frequency stimulation produced continual phase locking, whereas composite stimulation produced gamma enhancement throughout the stimulus, phase locked only at the onset and release of the stimulus. We describe this response as an “Appropriate Response in the gamma band” (ARγ), a trend seen in other sensory systems. Our demonstration is the first shown for intracortical somatosensory local field potentials. We argue that this stimulation paradigm produces a more biomimetic response in somatosensory cortex and is more likely to produce naturalistic sensations for readily usable neuroprosthetic feedback.
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spelling pubmed-100799522023-04-08 Dynamic peripheral nerve stimulation can produce cortical activation similar to punctate mechanical stimuli Tanner, Justin Keefer, Edward Cheng, Jonathan Helms Tillery, Stephen Front Hum Neurosci Neuroscience During contact, phasic and tonic responses provide feedback that is used for task performance and perceptual processes. These disparate temporal dynamics are carried in peripheral nerves, and produce overlapping signals in cortex. Using longitudinal intrafascicular electrodes inserted into the median nerve of a nonhuman primate, we delivered composite stimulation consisting of onset and release bursts to capture rapidly adapting responses and sustained stochastic stimulation to capture the ongoing response of slowly adapting receptors. To measure the stimulation’s effectiveness in producing natural responses, we monitored the local field potential in somatosensory cortex. We compared the cortical responses to peripheral nerve stimulation and vibrotactile/punctate stimulation of the fingertip, with particular focus on gamma band (30–65 Hz) responses. We found that vibrotactile stimulation produces consistently phase locked gamma throughout the duration of the stimulation. By contrast, punctate stimulation responses were phase locked at the onset and release of stimulation, but activity maintained through the stimulation was not phase locked. Using these responses as guideposts for assessing the response to the peripheral nerve stimulation, we found that constant frequency stimulation produced continual phase locking, whereas composite stimulation produced gamma enhancement throughout the stimulus, phase locked only at the onset and release of the stimulus. We describe this response as an “Appropriate Response in the gamma band” (ARγ), a trend seen in other sensory systems. Our demonstration is the first shown for intracortical somatosensory local field potentials. We argue that this stimulation paradigm produces a more biomimetic response in somatosensory cortex and is more likely to produce naturalistic sensations for readily usable neuroprosthetic feedback. Frontiers Media S.A. 2023-03-24 /pmc/articles/PMC10079952/ /pubmed/37033904 http://dx.doi.org/10.3389/fnhum.2023.1083307 Text en Copyright © 2023 Tanner, Keefer, Cheng and Helms Tillery. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Tanner, Justin
Keefer, Edward
Cheng, Jonathan
Helms Tillery, Stephen
Dynamic peripheral nerve stimulation can produce cortical activation similar to punctate mechanical stimuli
title Dynamic peripheral nerve stimulation can produce cortical activation similar to punctate mechanical stimuli
title_full Dynamic peripheral nerve stimulation can produce cortical activation similar to punctate mechanical stimuli
title_fullStr Dynamic peripheral nerve stimulation can produce cortical activation similar to punctate mechanical stimuli
title_full_unstemmed Dynamic peripheral nerve stimulation can produce cortical activation similar to punctate mechanical stimuli
title_short Dynamic peripheral nerve stimulation can produce cortical activation similar to punctate mechanical stimuli
title_sort dynamic peripheral nerve stimulation can produce cortical activation similar to punctate mechanical stimuli
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10079952/
https://www.ncbi.nlm.nih.gov/pubmed/37033904
http://dx.doi.org/10.3389/fnhum.2023.1083307
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