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Hierarchical unimodal processing within the primary somatosensory cortex during a bimodal detection task

Do sensory cortices process more than one sensory modality? To answer these questions, scientists have generated a wide variety of studies at distinct space-time scales in different animal models, and often shown contradictory conclusions. Some conclude that this process occurs in early sensory cort...

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Autores principales: Parra, Sergio, Díaz, Héctor, Zainos, Antonio, Alvarez, Manuel, Zizumbo, Jerónimo, Rivera-Yoshida, Natsuko, Pujalte, Sebastián, Bayones, Lucas, Romo, Ranulfo, Rossi-Pool, Román
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9907144/
https://www.ncbi.nlm.nih.gov/pubmed/36534792
http://dx.doi.org/10.1073/pnas.2213847119
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author Parra, Sergio
Díaz, Héctor
Zainos, Antonio
Alvarez, Manuel
Zizumbo, Jerónimo
Rivera-Yoshida, Natsuko
Pujalte, Sebastián
Bayones, Lucas
Romo, Ranulfo
Rossi-Pool, Román
author_facet Parra, Sergio
Díaz, Héctor
Zainos, Antonio
Alvarez, Manuel
Zizumbo, Jerónimo
Rivera-Yoshida, Natsuko
Pujalte, Sebastián
Bayones, Lucas
Romo, Ranulfo
Rossi-Pool, Román
author_sort Parra, Sergio
collection PubMed
description Do sensory cortices process more than one sensory modality? To answer these questions, scientists have generated a wide variety of studies at distinct space-time scales in different animal models, and often shown contradictory conclusions. Some conclude that this process occurs in early sensory cortices, but others that this occurs in areas central to sensory cortices. Here, we sought to determine whether sensory neurons process and encode physical stimulus properties of different modalities (tactile and acoustic). For this, we designed a bimodal detection task where the senses of touch and hearing compete from trial to trial. Two Rhesus monkeys performed this novel task, while neural activity was recorded in areas 3b and 1 of the primary somatosensory cortex (S1). We analyzed neurons’ coding properties and variability, organizing them by their receptive field’s position relative to the stimulation zone. Our results indicate that neurons of areas 3b and 1 are unimodal, encoding only the tactile modality in both the firing rate and variability. Moreover, we found that neurons in area 3b carried more information about the periodic stimulus structure than those in area 1, possessed lower response and coding latencies, and had a lower intrinsic time scale. In sum, these differences reveal a hidden processing-based hierarchy. Finally, using a powerful nonlinear dimensionality reduction algorithm, we show that the activity from areas 3b and 1 can be separated, establishing a clear division in the functionality of these two subareas of S1.
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spelling pubmed-99071442023-06-19 Hierarchical unimodal processing within the primary somatosensory cortex during a bimodal detection task Parra, Sergio Díaz, Héctor Zainos, Antonio Alvarez, Manuel Zizumbo, Jerónimo Rivera-Yoshida, Natsuko Pujalte, Sebastián Bayones, Lucas Romo, Ranulfo Rossi-Pool, Román Proc Natl Acad Sci U S A Biological Sciences Do sensory cortices process more than one sensory modality? To answer these questions, scientists have generated a wide variety of studies at distinct space-time scales in different animal models, and often shown contradictory conclusions. Some conclude that this process occurs in early sensory cortices, but others that this occurs in areas central to sensory cortices. Here, we sought to determine whether sensory neurons process and encode physical stimulus properties of different modalities (tactile and acoustic). For this, we designed a bimodal detection task where the senses of touch and hearing compete from trial to trial. Two Rhesus monkeys performed this novel task, while neural activity was recorded in areas 3b and 1 of the primary somatosensory cortex (S1). We analyzed neurons’ coding properties and variability, organizing them by their receptive field’s position relative to the stimulation zone. Our results indicate that neurons of areas 3b and 1 are unimodal, encoding only the tactile modality in both the firing rate and variability. Moreover, we found that neurons in area 3b carried more information about the periodic stimulus structure than those in area 1, possessed lower response and coding latencies, and had a lower intrinsic time scale. In sum, these differences reveal a hidden processing-based hierarchy. Finally, using a powerful nonlinear dimensionality reduction algorithm, we show that the activity from areas 3b and 1 can be separated, establishing a clear division in the functionality of these two subareas of S1. National Academy of Sciences 2022-12-19 2022-12-27 /pmc/articles/PMC9907144/ /pubmed/36534792 http://dx.doi.org/10.1073/pnas.2213847119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Parra, Sergio
Díaz, Héctor
Zainos, Antonio
Alvarez, Manuel
Zizumbo, Jerónimo
Rivera-Yoshida, Natsuko
Pujalte, Sebastián
Bayones, Lucas
Romo, Ranulfo
Rossi-Pool, Román
Hierarchical unimodal processing within the primary somatosensory cortex during a bimodal detection task
title Hierarchical unimodal processing within the primary somatosensory cortex during a bimodal detection task
title_full Hierarchical unimodal processing within the primary somatosensory cortex during a bimodal detection task
title_fullStr Hierarchical unimodal processing within the primary somatosensory cortex during a bimodal detection task
title_full_unstemmed Hierarchical unimodal processing within the primary somatosensory cortex during a bimodal detection task
title_short Hierarchical unimodal processing within the primary somatosensory cortex during a bimodal detection task
title_sort hierarchical unimodal processing within the primary somatosensory cortex during a bimodal detection task
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9907144/
https://www.ncbi.nlm.nih.gov/pubmed/36534792
http://dx.doi.org/10.1073/pnas.2213847119
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