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The cellular coding of temperature in the mammalian cortex

Temperature is a fundamental sensory modality separate from touch, with dedicated receptor channels and primary afferent neurons for cool and warm(1–3). Unlike for other modalities, however, the cortical encoding of temperature remains unknown, with very few cortical neurons reported that respond to...

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Autores principales: Vestergaard, M., Carta, M., Güney, G., Poulet, J. F. A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9946826/
https://www.ncbi.nlm.nih.gov/pubmed/36755097
http://dx.doi.org/10.1038/s41586-023-05705-5
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author Vestergaard, M.
Carta, M.
Güney, G.
Poulet, J. F. A.
author_facet Vestergaard, M.
Carta, M.
Güney, G.
Poulet, J. F. A.
author_sort Vestergaard, M.
collection PubMed
description Temperature is a fundamental sensory modality separate from touch, with dedicated receptor channels and primary afferent neurons for cool and warm(1–3). Unlike for other modalities, however, the cortical encoding of temperature remains unknown, with very few cortical neurons reported that respond to non-painful temperature, and the presence of a ‘thermal cortex’ is debated(4–8). Here, using widefield and two-photon calcium imaging in the mouse forepaw system, we identify cortical neurons that respond to cooling and/or warming with distinct spatial and temporal response properties. We observed a representation of cool, but not warm, in the primary somatosensory cortex, but cool and warm in the posterior insular cortex (pIC). The representation of thermal information in pIC is robust and somatotopically arranged, and reversible manipulations show a profound impact on thermal perception. Despite being positioned along the same one-dimensional sensory axis, the encoding of cool and that of warm are distinct, both in highly and broadly tuned neurons. Together, our results show that pIC contains the primary cortical representation of skin temperature and may help explain how the thermal system generates sensations of cool and warm.
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spelling pubmed-99468262023-02-24 The cellular coding of temperature in the mammalian cortex Vestergaard, M. Carta, M. Güney, G. Poulet, J. F. A. Nature Article Temperature is a fundamental sensory modality separate from touch, with dedicated receptor channels and primary afferent neurons for cool and warm(1–3). Unlike for other modalities, however, the cortical encoding of temperature remains unknown, with very few cortical neurons reported that respond to non-painful temperature, and the presence of a ‘thermal cortex’ is debated(4–8). Here, using widefield and two-photon calcium imaging in the mouse forepaw system, we identify cortical neurons that respond to cooling and/or warming with distinct spatial and temporal response properties. We observed a representation of cool, but not warm, in the primary somatosensory cortex, but cool and warm in the posterior insular cortex (pIC). The representation of thermal information in pIC is robust and somatotopically arranged, and reversible manipulations show a profound impact on thermal perception. Despite being positioned along the same one-dimensional sensory axis, the encoding of cool and that of warm are distinct, both in highly and broadly tuned neurons. Together, our results show that pIC contains the primary cortical representation of skin temperature and may help explain how the thermal system generates sensations of cool and warm. Nature Publishing Group UK 2023-02-08 2023 /pmc/articles/PMC9946826/ /pubmed/36755097 http://dx.doi.org/10.1038/s41586-023-05705-5 Text en © The Author(s) 2023 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Vestergaard, M.
Carta, M.
Güney, G.
Poulet, J. F. A.
The cellular coding of temperature in the mammalian cortex
title The cellular coding of temperature in the mammalian cortex
title_full The cellular coding of temperature in the mammalian cortex
title_fullStr The cellular coding of temperature in the mammalian cortex
title_full_unstemmed The cellular coding of temperature in the mammalian cortex
title_short The cellular coding of temperature in the mammalian cortex
title_sort cellular coding of temperature in the mammalian cortex
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9946826/
https://www.ncbi.nlm.nih.gov/pubmed/36755097
http://dx.doi.org/10.1038/s41586-023-05705-5
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