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Precise and stable edge orientation signaling by human first-order tactile neurons
Fast-adapting type 1 (FA-1) and slow-adapting type 1 (SA-1) first-order neurons in the human tactile system have distal axons that branch in the skin and form many transduction sites, yielding receptive fields with many highly sensitive zones or ‘subfields.’ We previously demonstrated that this arra...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9642991/ https://www.ncbi.nlm.nih.gov/pubmed/36314774 http://dx.doi.org/10.7554/eLife.81476 |
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author | Sukumar, Vaishnavi Johansson, Roland S Pruszynski, J Andrew |
author_facet | Sukumar, Vaishnavi Johansson, Roland S Pruszynski, J Andrew |
author_sort | Sukumar, Vaishnavi |
collection | PubMed |
description | Fast-adapting type 1 (FA-1) and slow-adapting type 1 (SA-1) first-order neurons in the human tactile system have distal axons that branch in the skin and form many transduction sites, yielding receptive fields with many highly sensitive zones or ‘subfields.’ We previously demonstrated that this arrangement allows FA-1 and SA-1 neurons to signal the geometric features of touched objects, specifically the orientation of raised edges scanned with the fingertips. Here, we show that such signaling operates for fine edge orientation differences (5–20°) and is stable across a broad range of scanning speeds (15–180 mm/s); that is, under conditions relevant for real-world hand use. We found that both FA-1 and SA-1 neurons weakly signal fine edge orientation differences via the intensity of their spiking responses and only when considering a single scanning speed. Both neuron types showed much stronger edge orientation signaling in the sequential structure of the evoked spike trains, and FA-1 neurons performed better than SA-1 neurons. Represented in the spatial domain, the sequential structure was strikingly invariant across scanning speeds, especially those naturally used in tactile spatial discrimination tasks. This speed invariance suggests that neurons’ responses are structured via sequential stimulation of their subfields and thus links this capacity to their terminal organization in the skin. Indeed, the spatial precision of elicited action potentials rationally matched spatial acuity of subfield arrangements, which corresponds to a spatial period similar to the dimensions of individual fingertip ridges. |
format | Online Article Text |
id | pubmed-9642991 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
spelling | pubmed-96429912022-11-15 Precise and stable edge orientation signaling by human first-order tactile neurons Sukumar, Vaishnavi Johansson, Roland S Pruszynski, J Andrew eLife Neuroscience Fast-adapting type 1 (FA-1) and slow-adapting type 1 (SA-1) first-order neurons in the human tactile system have distal axons that branch in the skin and form many transduction sites, yielding receptive fields with many highly sensitive zones or ‘subfields.’ We previously demonstrated that this arrangement allows FA-1 and SA-1 neurons to signal the geometric features of touched objects, specifically the orientation of raised edges scanned with the fingertips. Here, we show that such signaling operates for fine edge orientation differences (5–20°) and is stable across a broad range of scanning speeds (15–180 mm/s); that is, under conditions relevant for real-world hand use. We found that both FA-1 and SA-1 neurons weakly signal fine edge orientation differences via the intensity of their spiking responses and only when considering a single scanning speed. Both neuron types showed much stronger edge orientation signaling in the sequential structure of the evoked spike trains, and FA-1 neurons performed better than SA-1 neurons. Represented in the spatial domain, the sequential structure was strikingly invariant across scanning speeds, especially those naturally used in tactile spatial discrimination tasks. This speed invariance suggests that neurons’ responses are structured via sequential stimulation of their subfields and thus links this capacity to their terminal organization in the skin. Indeed, the spatial precision of elicited action potentials rationally matched spatial acuity of subfield arrangements, which corresponds to a spatial period similar to the dimensions of individual fingertip ridges. eLife Sciences Publications, Ltd 2022-10-31 /pmc/articles/PMC9642991/ /pubmed/36314774 http://dx.doi.org/10.7554/eLife.81476 Text en © 2022, Sukumar et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited. |
spellingShingle | Neuroscience Sukumar, Vaishnavi Johansson, Roland S Pruszynski, J Andrew Precise and stable edge orientation signaling by human first-order tactile neurons |
title | Precise and stable edge orientation signaling by human first-order tactile neurons |
title_full | Precise and stable edge orientation signaling by human first-order tactile neurons |
title_fullStr | Precise and stable edge orientation signaling by human first-order tactile neurons |
title_full_unstemmed | Precise and stable edge orientation signaling by human first-order tactile neurons |
title_short | Precise and stable edge orientation signaling by human first-order tactile neurons |
title_sort | precise and stable edge orientation signaling by human first-order tactile neurons |
topic | Neuroscience |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9642991/ https://www.ncbi.nlm.nih.gov/pubmed/36314774 http://dx.doi.org/10.7554/eLife.81476 |
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