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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...

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Autores principales: Bale, Michael R., Bitzidou, Malamati, Giusto, Elena, Kinghorn, Paul, Maravall, Miguel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2021
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.
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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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