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Reward uncertainty asymmetrically affects information transmission within the monkey fronto-parietal network

A central hypothesis in research on executive function is that controlled information processing is costly and is allocated according to the behavioral benefits it brings. However, while computational theories predict that the benefits of new information depend on prior uncertainty, the cellular eff...

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Autores principales: Taghizadeh, Bahareh, Foley, Nicholas C., Karimimehr, Saeed, Cohanpour, Michael, Semework, Mulugeta, Sheth, Sameer A., Lashgari, Reza, Gottlieb, Jacqueline
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7578031/
https://www.ncbi.nlm.nih.gov/pubmed/33087809
http://dx.doi.org/10.1038/s42003-020-01320-6
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author Taghizadeh, Bahareh
Foley, Nicholas C.
Karimimehr, Saeed
Cohanpour, Michael
Semework, Mulugeta
Sheth, Sameer A.
Lashgari, Reza
Gottlieb, Jacqueline
author_facet Taghizadeh, Bahareh
Foley, Nicholas C.
Karimimehr, Saeed
Cohanpour, Michael
Semework, Mulugeta
Sheth, Sameer A.
Lashgari, Reza
Gottlieb, Jacqueline
author_sort Taghizadeh, Bahareh
collection PubMed
description A central hypothesis in research on executive function is that controlled information processing is costly and is allocated according to the behavioral benefits it brings. However, while computational theories predict that the benefits of new information depend on prior uncertainty, the cellular effects of uncertainty on the executive network are incompletely understood. Using simultaneous recordings in monkeys, we describe several mechanisms by which the fronto-parietal network reacts to uncertainty. We show that the variance of expected rewards, independently of the value of the rewards, was encoded in single neuron and population spiking activity and local field potential (LFP) oscillations, and, importantly, asymmetrically affected fronto-parietal information transmission (measured through the coherence between spikes and LFPs). Higher uncertainty selectively enhanced information transmission from the parietal to the frontal lobe and suppressed it in the opposite direction, consistent with Bayesian principles that prioritize sensory information according to a decision maker’s prior uncertainty.
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spelling pubmed-75780312020-10-23 Reward uncertainty asymmetrically affects information transmission within the monkey fronto-parietal network Taghizadeh, Bahareh Foley, Nicholas C. Karimimehr, Saeed Cohanpour, Michael Semework, Mulugeta Sheth, Sameer A. Lashgari, Reza Gottlieb, Jacqueline Commun Biol Article A central hypothesis in research on executive function is that controlled information processing is costly and is allocated according to the behavioral benefits it brings. However, while computational theories predict that the benefits of new information depend on prior uncertainty, the cellular effects of uncertainty on the executive network are incompletely understood. Using simultaneous recordings in monkeys, we describe several mechanisms by which the fronto-parietal network reacts to uncertainty. We show that the variance of expected rewards, independently of the value of the rewards, was encoded in single neuron and population spiking activity and local field potential (LFP) oscillations, and, importantly, asymmetrically affected fronto-parietal information transmission (measured through the coherence between spikes and LFPs). Higher uncertainty selectively enhanced information transmission from the parietal to the frontal lobe and suppressed it in the opposite direction, consistent with Bayesian principles that prioritize sensory information according to a decision maker’s prior uncertainty. Nature Publishing Group UK 2020-10-21 /pmc/articles/PMC7578031/ /pubmed/33087809 http://dx.doi.org/10.1038/s42003-020-01320-6 Text en © The Author(s) 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Taghizadeh, Bahareh
Foley, Nicholas C.
Karimimehr, Saeed
Cohanpour, Michael
Semework, Mulugeta
Sheth, Sameer A.
Lashgari, Reza
Gottlieb, Jacqueline
Reward uncertainty asymmetrically affects information transmission within the monkey fronto-parietal network
title Reward uncertainty asymmetrically affects information transmission within the monkey fronto-parietal network
title_full Reward uncertainty asymmetrically affects information transmission within the monkey fronto-parietal network
title_fullStr Reward uncertainty asymmetrically affects information transmission within the monkey fronto-parietal network
title_full_unstemmed Reward uncertainty asymmetrically affects information transmission within the monkey fronto-parietal network
title_short Reward uncertainty asymmetrically affects information transmission within the monkey fronto-parietal network
title_sort reward uncertainty asymmetrically affects information transmission within the monkey fronto-parietal network
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7578031/
https://www.ncbi.nlm.nih.gov/pubmed/33087809
http://dx.doi.org/10.1038/s42003-020-01320-6
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