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Sequence Learning Induces Selectivity to Multiple Task Parameters in Mouse Somatosensory Cortex
Sequential temporal ordering and patterning are key features of natural signals, used by the brain to decode stimuli and perceive them as sensory objects. To explore how cortical neuronal activity underpins sequence discrimination, we developed a task in which mice distinguished between tactile “wor...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Cell Press
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7883307/ https://www.ncbi.nlm.nih.gov/pubmed/33186553 http://dx.doi.org/10.1016/j.cub.2020.10.059 |
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author | Bale, Michael R. Bitzidou, Malamati Giusto, Elena Kinghorn, Paul Maravall, Miguel |
author_facet | Bale, Michael R. Bitzidou, Malamati Giusto, Elena Kinghorn, Paul Maravall, Miguel |
author_sort | Bale, Michael R. |
collection | PubMed |
description | Sequential temporal ordering and patterning are key features of natural signals, used by the brain to decode stimuli and perceive them as sensory objects. To explore how cortical neuronal activity underpins sequence discrimination, we developed a task in which mice distinguished between tactile “word” sequences constructed from distinct vibrations delivered to the whiskers, assembled in different orders. Animals licked to report the presence of the target sequence. Mice could respond to the earliest possible cues allowing discrimination, effectively solving the task as a “detection of change” problem, but enhanced their performance when responding later. Optogenetic inactivation showed that the somatosensory cortex was necessary for sequence discrimination. Two-photon imaging in layer 2/3 of the primary somatosensory “barrel” cortex (S1bf) revealed that, in well-trained animals, neurons had heterogeneous selectivity to multiple task variables including not just sensory input but also the animal’s action decision and the trial outcome (presence or absence of the predicted reward). Many neurons were activated preceding goal-directed licking, thus reflecting the animal’s learned action in response to the target sequence; these neurons were found as soon as mice learned to associate the rewarded sequence with licking. In contrast, learning evoked smaller changes in sensory response tuning: neurons responding to stimulus features were found in naive mice, and training did not generate neurons with enhanced temporal integration or categorical responses. Therefore, in S1bf, sequence learning results in neurons whose activity reflects the learned association between target sequence and licking rather than a refined representation of sensory features. |
format | Online Article Text |
id | pubmed-7883307 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Cell Press |
record_format | MEDLINE/PubMed |
spelling | pubmed-78833072021-02-19 Sequence Learning Induces Selectivity to Multiple Task Parameters in Mouse Somatosensory Cortex Bale, Michael R. Bitzidou, Malamati Giusto, Elena Kinghorn, Paul Maravall, Miguel Curr Biol Article Sequential temporal ordering and patterning are key features of natural signals, used by the brain to decode stimuli and perceive them as sensory objects. To explore how cortical neuronal activity underpins sequence discrimination, we developed a task in which mice distinguished between tactile “word” sequences constructed from distinct vibrations delivered to the whiskers, assembled in different orders. Animals licked to report the presence of the target sequence. Mice could respond to the earliest possible cues allowing discrimination, effectively solving the task as a “detection of change” problem, but enhanced their performance when responding later. Optogenetic inactivation showed that the somatosensory cortex was necessary for sequence discrimination. Two-photon imaging in layer 2/3 of the primary somatosensory “barrel” cortex (S1bf) revealed that, in well-trained animals, neurons had heterogeneous selectivity to multiple task variables including not just sensory input but also the animal’s action decision and the trial outcome (presence or absence of the predicted reward). Many neurons were activated preceding goal-directed licking, thus reflecting the animal’s learned action in response to the target sequence; these neurons were found as soon as mice learned to associate the rewarded sequence with licking. In contrast, learning evoked smaller changes in sensory response tuning: neurons responding to stimulus features were found in naive mice, and training did not generate neurons with enhanced temporal integration or categorical responses. Therefore, in S1bf, sequence learning results in neurons whose activity reflects the learned association between target sequence and licking rather than a refined representation of sensory features. Cell Press 2021-02-08 /pmc/articles/PMC7883307/ /pubmed/33186553 http://dx.doi.org/10.1016/j.cub.2020.10.059 Text en © 2020 The Author(s) http://creativecommons.org/licenses/by/4.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). |
spellingShingle | Article Bale, Michael R. Bitzidou, Malamati Giusto, Elena Kinghorn, Paul Maravall, Miguel Sequence Learning Induces Selectivity to Multiple Task Parameters in Mouse Somatosensory Cortex |
title | Sequence Learning Induces Selectivity to Multiple Task Parameters in Mouse Somatosensory Cortex |
title_full | Sequence Learning Induces Selectivity to Multiple Task Parameters in Mouse Somatosensory Cortex |
title_fullStr | Sequence Learning Induces Selectivity to Multiple Task Parameters in Mouse Somatosensory Cortex |
title_full_unstemmed | Sequence Learning Induces Selectivity to Multiple Task Parameters in Mouse Somatosensory Cortex |
title_short | Sequence Learning Induces Selectivity to Multiple Task Parameters in Mouse Somatosensory Cortex |
title_sort | sequence learning induces selectivity to multiple task parameters in mouse somatosensory cortex |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7883307/ https://www.ncbi.nlm.nih.gov/pubmed/33186553 http://dx.doi.org/10.1016/j.cub.2020.10.059 |
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