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Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions

Anterior cingulate cortex (ACC) and striatum (STR) contain neurons encoding not only the expected values of actions, but also the value of stimulus features irrespective of actions. Values about stimulus features in ACC or STR might contribute to adaptive behavior by guiding fixational information s...

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Autores principales: Banaie Boroujeni, Kianoush, Sigona, Michelle K., Treuting, Robert Louie, Manuel, Thomas J., Caskey, Charles F., Womelsdorf, Thilo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9481162/
https://www.ncbi.nlm.nih.gov/pubmed/36067198
http://dx.doi.org/10.1371/journal.pbio.3001785
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author Banaie Boroujeni, Kianoush
Sigona, Michelle K.
Treuting, Robert Louie
Manuel, Thomas J.
Caskey, Charles F.
Womelsdorf, Thilo
author_facet Banaie Boroujeni, Kianoush
Sigona, Michelle K.
Treuting, Robert Louie
Manuel, Thomas J.
Caskey, Charles F.
Womelsdorf, Thilo
author_sort Banaie Boroujeni, Kianoush
collection PubMed
description Anterior cingulate cortex (ACC) and striatum (STR) contain neurons encoding not only the expected values of actions, but also the value of stimulus features irrespective of actions. Values about stimulus features in ACC or STR might contribute to adaptive behavior by guiding fixational information sampling and biasing choices toward relevant objects, but they might also have indirect motivational functions by enabling subjects to estimate the value of putting effort into choosing objects. Here, we tested these possibilities by modulating neuronal activity in ACC and STR of nonhuman primates using transcranial ultrasound stimulation while subjects learned the relevance of objects in situations with varying motivational and cognitive demands. Motivational demand was indexed by varying gains and losses during learning, while cognitive demand was varied by increasing the uncertainty about which object features could be relevant during learning. We found that ultrasound stimulation of the ACC, but not the STR, reduced learning efficiency and prolonged information sampling when the task required averting losses and motivational demands were high. Reduced learning efficiency was particularly evident at higher cognitive demands and when subjects experienced loss of already attained tokens. These results suggest that the ACC supports flexible learning of feature values when loss experiences impose a motivational challenge and when uncertainty about the relevance of objects is high. Taken together, these findings provide causal evidence that the ACC facilitates resource allocation and improves visual information sampling during adaptive behavior.
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spelling pubmed-94811622022-09-17 Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions Banaie Boroujeni, Kianoush Sigona, Michelle K. Treuting, Robert Louie Manuel, Thomas J. Caskey, Charles F. Womelsdorf, Thilo PLoS Biol Research Article Anterior cingulate cortex (ACC) and striatum (STR) contain neurons encoding not only the expected values of actions, but also the value of stimulus features irrespective of actions. Values about stimulus features in ACC or STR might contribute to adaptive behavior by guiding fixational information sampling and biasing choices toward relevant objects, but they might also have indirect motivational functions by enabling subjects to estimate the value of putting effort into choosing objects. Here, we tested these possibilities by modulating neuronal activity in ACC and STR of nonhuman primates using transcranial ultrasound stimulation while subjects learned the relevance of objects in situations with varying motivational and cognitive demands. Motivational demand was indexed by varying gains and losses during learning, while cognitive demand was varied by increasing the uncertainty about which object features could be relevant during learning. We found that ultrasound stimulation of the ACC, but not the STR, reduced learning efficiency and prolonged information sampling when the task required averting losses and motivational demands were high. Reduced learning efficiency was particularly evident at higher cognitive demands and when subjects experienced loss of already attained tokens. These results suggest that the ACC supports flexible learning of feature values when loss experiences impose a motivational challenge and when uncertainty about the relevance of objects is high. Taken together, these findings provide causal evidence that the ACC facilitates resource allocation and improves visual information sampling during adaptive behavior. Public Library of Science 2022-09-06 /pmc/articles/PMC9481162/ /pubmed/36067198 http://dx.doi.org/10.1371/journal.pbio.3001785 Text en © 2022 Banaie Boroujeni et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Banaie Boroujeni, Kianoush
Sigona, Michelle K.
Treuting, Robert Louie
Manuel, Thomas J.
Caskey, Charles F.
Womelsdorf, Thilo
Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions
title Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions
title_full Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions
title_fullStr Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions
title_full_unstemmed Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions
title_short Anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions
title_sort anterior cingulate cortex causally supports flexible learning under motivationally challenging and cognitively demanding conditions
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9481162/
https://www.ncbi.nlm.nih.gov/pubmed/36067198
http://dx.doi.org/10.1371/journal.pbio.3001785
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