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Recurrent pattern completion drives the neocortical representation of sensory inference

When sensory information is incomplete or ambiguous, the brain relies on prior expectations to infer perceptual objects. Despite the centrality of this process to perception, the neural mechanism of sensory inference is not known. Illusory contours (ICs) are key tools to study sensory inference beca...

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Autores principales: Shin, Hyeyoung, Ogando, Mora B., Abdeladim, Lamiae, Durand, Severine, Belski, Hannah, Cabasco, Hannah, Loefler, Henry, Bawany, Ahad, Hardcastle, Ben, Wilkes, Josh, Nguyen, Katrina, Suarez, Lucas, Johnson, Tye, Han, Warren, Ouellette, Ben, Grasso, Conor, Swapp, Jackie, Ha, Vivian, Young, Ahrial, Caldejon, Shiella, Williford, Ali, Groblewski, Peter, Olsen, Shawn, Kiselycznyk, Carly, Lecoq, Jerome, Adesnik, Hillel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10274729/
https://www.ncbi.nlm.nih.gov/pubmed/37333175
http://dx.doi.org/10.1101/2023.06.05.543698
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author Shin, Hyeyoung
Ogando, Mora B.
Abdeladim, Lamiae
Durand, Severine
Belski, Hannah
Cabasco, Hannah
Loefler, Henry
Bawany, Ahad
Hardcastle, Ben
Wilkes, Josh
Nguyen, Katrina
Suarez, Lucas
Johnson, Tye
Han, Warren
Ouellette, Ben
Grasso, Conor
Swapp, Jackie
Ha, Vivian
Young, Ahrial
Caldejon, Shiella
Williford, Ali
Groblewski, Peter
Olsen, Shawn
Kiselycznyk, Carly
Lecoq, Jerome
Adesnik, Hillel
author_facet Shin, Hyeyoung
Ogando, Mora B.
Abdeladim, Lamiae
Durand, Severine
Belski, Hannah
Cabasco, Hannah
Loefler, Henry
Bawany, Ahad
Hardcastle, Ben
Wilkes, Josh
Nguyen, Katrina
Suarez, Lucas
Johnson, Tye
Han, Warren
Ouellette, Ben
Grasso, Conor
Swapp, Jackie
Ha, Vivian
Young, Ahrial
Caldejon, Shiella
Williford, Ali
Groblewski, Peter
Olsen, Shawn
Kiselycznyk, Carly
Lecoq, Jerome
Adesnik, Hillel
author_sort Shin, Hyeyoung
collection PubMed
description When sensory information is incomplete or ambiguous, the brain relies on prior expectations to infer perceptual objects. Despite the centrality of this process to perception, the neural mechanism of sensory inference is not known. Illusory contours (ICs) are key tools to study sensory inference because they contain edges or objects that are implied only by their spatial context. Using cellular resolution, mesoscale two-photon calcium imaging and multi-Neuropixels recordings in the mouse visual cortex, we identified a sparse subset of neurons in the primary visual cortex (V1) and higher visual areas that respond emergently to ICs. We found that these highly selective ‘IC-encoders’ mediate the neural representation of IC inference. Strikingly, selective activation of these neurons using two-photon holographic optogenetics was sufficient to recreate IC representation in the rest of the V1 network, in the absence of any visual stimulus. This outlines a model in which primary sensory cortex facilitates sensory inference by selectively strengthening input patterns that match prior expectations through local, recurrent circuitry. Our data thus suggest a clear computational purpose for recurrence in the generation of holistic percepts under sensory ambiguity. More generally, selective reinforcement of top-down predictions by pattern-completing recurrent circuits in lower sensory cortices may constitute a key step in sensory inference.
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spelling pubmed-102747292023-06-17 Recurrent pattern completion drives the neocortical representation of sensory inference Shin, Hyeyoung Ogando, Mora B. Abdeladim, Lamiae Durand, Severine Belski, Hannah Cabasco, Hannah Loefler, Henry Bawany, Ahad Hardcastle, Ben Wilkes, Josh Nguyen, Katrina Suarez, Lucas Johnson, Tye Han, Warren Ouellette, Ben Grasso, Conor Swapp, Jackie Ha, Vivian Young, Ahrial Caldejon, Shiella Williford, Ali Groblewski, Peter Olsen, Shawn Kiselycznyk, Carly Lecoq, Jerome Adesnik, Hillel bioRxiv Article When sensory information is incomplete or ambiguous, the brain relies on prior expectations to infer perceptual objects. Despite the centrality of this process to perception, the neural mechanism of sensory inference is not known. Illusory contours (ICs) are key tools to study sensory inference because they contain edges or objects that are implied only by their spatial context. Using cellular resolution, mesoscale two-photon calcium imaging and multi-Neuropixels recordings in the mouse visual cortex, we identified a sparse subset of neurons in the primary visual cortex (V1) and higher visual areas that respond emergently to ICs. We found that these highly selective ‘IC-encoders’ mediate the neural representation of IC inference. Strikingly, selective activation of these neurons using two-photon holographic optogenetics was sufficient to recreate IC representation in the rest of the V1 network, in the absence of any visual stimulus. This outlines a model in which primary sensory cortex facilitates sensory inference by selectively strengthening input patterns that match prior expectations through local, recurrent circuitry. Our data thus suggest a clear computational purpose for recurrence in the generation of holistic percepts under sensory ambiguity. More generally, selective reinforcement of top-down predictions by pattern-completing recurrent circuits in lower sensory cortices may constitute a key step in sensory inference. Cold Spring Harbor Laboratory 2023-06-07 /pmc/articles/PMC10274729/ /pubmed/37333175 http://dx.doi.org/10.1101/2023.06.05.543698 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Shin, Hyeyoung
Ogando, Mora B.
Abdeladim, Lamiae
Durand, Severine
Belski, Hannah
Cabasco, Hannah
Loefler, Henry
Bawany, Ahad
Hardcastle, Ben
Wilkes, Josh
Nguyen, Katrina
Suarez, Lucas
Johnson, Tye
Han, Warren
Ouellette, Ben
Grasso, Conor
Swapp, Jackie
Ha, Vivian
Young, Ahrial
Caldejon, Shiella
Williford, Ali
Groblewski, Peter
Olsen, Shawn
Kiselycznyk, Carly
Lecoq, Jerome
Adesnik, Hillel
Recurrent pattern completion drives the neocortical representation of sensory inference
title Recurrent pattern completion drives the neocortical representation of sensory inference
title_full Recurrent pattern completion drives the neocortical representation of sensory inference
title_fullStr Recurrent pattern completion drives the neocortical representation of sensory inference
title_full_unstemmed Recurrent pattern completion drives the neocortical representation of sensory inference
title_short Recurrent pattern completion drives the neocortical representation of sensory inference
title_sort recurrent pattern completion drives the neocortical representation of sensory inference
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10274729/
https://www.ncbi.nlm.nih.gov/pubmed/37333175
http://dx.doi.org/10.1101/2023.06.05.543698
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