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Dorsal root ganglia control nociceptive input to the central nervous system
Accumulating observations suggest that peripheral somatosensory ganglia may regulate nociceptive transmission, yet direct evidence is sparse. Here, in experiments on rats and mice, we show that the peripheral afferent nociceptive information undergoes dynamic filtering within the dorsal root ganglio...
Autores principales: | , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9847955/ https://www.ncbi.nlm.nih.gov/pubmed/36603052 http://dx.doi.org/10.1371/journal.pbio.3001958 |
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author | Hao, Han Ramli, Rosmaliza Wang, Caixue Liu, Chao Shah, Shihab Mullen, Pierce Lall, Varinder Jones, Frederick Shao, Jicheng Zhang, Hailin Jaffe, David B. Gamper, Nikita Du, Xiaona |
author_facet | Hao, Han Ramli, Rosmaliza Wang, Caixue Liu, Chao Shah, Shihab Mullen, Pierce Lall, Varinder Jones, Frederick Shao, Jicheng Zhang, Hailin Jaffe, David B. Gamper, Nikita Du, Xiaona |
author_sort | Hao, Han |
collection | PubMed |
description | Accumulating observations suggest that peripheral somatosensory ganglia may regulate nociceptive transmission, yet direct evidence is sparse. Here, in experiments on rats and mice, we show that the peripheral afferent nociceptive information undergoes dynamic filtering within the dorsal root ganglion (DRG) and suggest that this filtering occurs at the axonal bifurcations (t-junctions). Using synchronous in vivo electrophysiological recordings from the peripheral and central processes of sensory neurons (in the spinal nerve and dorsal root), ganglionic transplantation of GABAergic progenitor cells, and optogenetics, we demonstrate existence of tonic and dynamic filtering of action potentials traveling through the DRG. Filtering induced by focal application of GABA or optogenetic GABA release from the DRG-transplanted GABAergic progenitor cells was specific to nociceptive fibers. Light-sheet imaging and computer modeling demonstrated that, compared to other somatosensory fiber types, nociceptors have shorter stem axons, making somatic control over t-junctional filtering more efficient. Optogenetically induced GABA release within DRG from the transplanted GABAergic cells enhanced filtering and alleviated hypersensitivity to noxious stimulation produced by chronic inflammation and neuropathic injury in vivo. These findings support “gating” of pain information by DRGs and suggest new therapeutic approaches for pain relief. |
format | Online Article Text |
id | pubmed-9847955 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-98479552023-01-19 Dorsal root ganglia control nociceptive input to the central nervous system Hao, Han Ramli, Rosmaliza Wang, Caixue Liu, Chao Shah, Shihab Mullen, Pierce Lall, Varinder Jones, Frederick Shao, Jicheng Zhang, Hailin Jaffe, David B. Gamper, Nikita Du, Xiaona PLoS Biol Research Article Accumulating observations suggest that peripheral somatosensory ganglia may regulate nociceptive transmission, yet direct evidence is sparse. Here, in experiments on rats and mice, we show that the peripheral afferent nociceptive information undergoes dynamic filtering within the dorsal root ganglion (DRG) and suggest that this filtering occurs at the axonal bifurcations (t-junctions). Using synchronous in vivo electrophysiological recordings from the peripheral and central processes of sensory neurons (in the spinal nerve and dorsal root), ganglionic transplantation of GABAergic progenitor cells, and optogenetics, we demonstrate existence of tonic and dynamic filtering of action potentials traveling through the DRG. Filtering induced by focal application of GABA or optogenetic GABA release from the DRG-transplanted GABAergic progenitor cells was specific to nociceptive fibers. Light-sheet imaging and computer modeling demonstrated that, compared to other somatosensory fiber types, nociceptors have shorter stem axons, making somatic control over t-junctional filtering more efficient. Optogenetically induced GABA release within DRG from the transplanted GABAergic cells enhanced filtering and alleviated hypersensitivity to noxious stimulation produced by chronic inflammation and neuropathic injury in vivo. These findings support “gating” of pain information by DRGs and suggest new therapeutic approaches for pain relief. Public Library of Science 2023-01-05 /pmc/articles/PMC9847955/ /pubmed/36603052 http://dx.doi.org/10.1371/journal.pbio.3001958 Text en © 2023 Hao et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Hao, Han Ramli, Rosmaliza Wang, Caixue Liu, Chao Shah, Shihab Mullen, Pierce Lall, Varinder Jones, Frederick Shao, Jicheng Zhang, Hailin Jaffe, David B. Gamper, Nikita Du, Xiaona Dorsal root ganglia control nociceptive input to the central nervous system |
title | Dorsal root ganglia control nociceptive input to the central nervous system |
title_full | Dorsal root ganglia control nociceptive input to the central nervous system |
title_fullStr | Dorsal root ganglia control nociceptive input to the central nervous system |
title_full_unstemmed | Dorsal root ganglia control nociceptive input to the central nervous system |
title_short | Dorsal root ganglia control nociceptive input to the central nervous system |
title_sort | dorsal root ganglia control nociceptive input to the central nervous system |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9847955/ https://www.ncbi.nlm.nih.gov/pubmed/36603052 http://dx.doi.org/10.1371/journal.pbio.3001958 |
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