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Deep brain stimulation creates informational lesion through membrane depolarization in mouse hippocampus
Deep brain stimulation (DBS) is a promising neuromodulation therapy, but the neurophysiological mechanisms of DBS remain unclear. In awake mice, we performed high-speed membrane voltage fluorescence imaging of individual hippocampal CA1 neurons during DBS delivered at 40 Hz or 140 Hz, free of electr...
Autores principales: | , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9748039/ https://www.ncbi.nlm.nih.gov/pubmed/36513664 http://dx.doi.org/10.1038/s41467-022-35314-1 |
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author | Lowet, Eric Kondabolu, Krishnakanth Zhou, Samuel Mount, Rebecca A. Wang, Yangyang Ravasio, Cara R. Han, Xue |
author_facet | Lowet, Eric Kondabolu, Krishnakanth Zhou, Samuel Mount, Rebecca A. Wang, Yangyang Ravasio, Cara R. Han, Xue |
author_sort | Lowet, Eric |
collection | PubMed |
description | Deep brain stimulation (DBS) is a promising neuromodulation therapy, but the neurophysiological mechanisms of DBS remain unclear. In awake mice, we performed high-speed membrane voltage fluorescence imaging of individual hippocampal CA1 neurons during DBS delivered at 40 Hz or 140 Hz, free of electrical interference. DBS powerfully depolarized somatic membrane potentials without suppressing spike rate, especially at 140 Hz. Further, DBS paced membrane voltage and spike timing at the stimulation frequency and reduced timed spiking output in response to hippocampal network theta-rhythmic (3–12 Hz) activity patterns. To determine whether DBS directly impacts cellular processing of inputs, we optogenetically evoked theta-rhythmic membrane depolarization at the soma. We found that DBS-evoked membrane depolarization was correlated with DBS-mediated suppression of neuronal responses to optogenetic inputs. These results demonstrate that DBS produces powerful membrane depolarization that interferes with the ability of individual neurons to respond to inputs, creating an informational lesion. |
format | Online Article Text |
id | pubmed-9748039 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-97480392022-12-15 Deep brain stimulation creates informational lesion through membrane depolarization in mouse hippocampus Lowet, Eric Kondabolu, Krishnakanth Zhou, Samuel Mount, Rebecca A. Wang, Yangyang Ravasio, Cara R. Han, Xue Nat Commun Article Deep brain stimulation (DBS) is a promising neuromodulation therapy, but the neurophysiological mechanisms of DBS remain unclear. In awake mice, we performed high-speed membrane voltage fluorescence imaging of individual hippocampal CA1 neurons during DBS delivered at 40 Hz or 140 Hz, free of electrical interference. DBS powerfully depolarized somatic membrane potentials without suppressing spike rate, especially at 140 Hz. Further, DBS paced membrane voltage and spike timing at the stimulation frequency and reduced timed spiking output in response to hippocampal network theta-rhythmic (3–12 Hz) activity patterns. To determine whether DBS directly impacts cellular processing of inputs, we optogenetically evoked theta-rhythmic membrane depolarization at the soma. We found that DBS-evoked membrane depolarization was correlated with DBS-mediated suppression of neuronal responses to optogenetic inputs. These results demonstrate that DBS produces powerful membrane depolarization that interferes with the ability of individual neurons to respond to inputs, creating an informational lesion. Nature Publishing Group UK 2022-12-13 /pmc/articles/PMC9748039/ /pubmed/36513664 http://dx.doi.org/10.1038/s41467-022-35314-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Lowet, Eric Kondabolu, Krishnakanth Zhou, Samuel Mount, Rebecca A. Wang, Yangyang Ravasio, Cara R. Han, Xue Deep brain stimulation creates informational lesion through membrane depolarization in mouse hippocampus |
title | Deep brain stimulation creates informational lesion through membrane depolarization in mouse hippocampus |
title_full | Deep brain stimulation creates informational lesion through membrane depolarization in mouse hippocampus |
title_fullStr | Deep brain stimulation creates informational lesion through membrane depolarization in mouse hippocampus |
title_full_unstemmed | Deep brain stimulation creates informational lesion through membrane depolarization in mouse hippocampus |
title_short | Deep brain stimulation creates informational lesion through membrane depolarization in mouse hippocampus |
title_sort | deep brain stimulation creates informational lesion through membrane depolarization in mouse hippocampus |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9748039/ https://www.ncbi.nlm.nih.gov/pubmed/36513664 http://dx.doi.org/10.1038/s41467-022-35314-1 |
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