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Reward cues readily direct monkeys’ auditory performance resulting in broad auditory cortex modulation and interaction with sites along cholinergic and dopaminergic pathways

In natural settings, the prospect of reward often influences the focus of our attention, but how cognitive and motivational systems influence sensory cortex is not well understood. Also, challenges in training nonhuman animals on cognitive tasks complicate cross-species comparisons and interpreting...

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Autores principales: Wikman, Patrik, Rinne, Teemu, Petkov, Christopher I.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6395775/
https://www.ncbi.nlm.nih.gov/pubmed/30816142
http://dx.doi.org/10.1038/s41598-019-38833-y
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author Wikman, Patrik
Rinne, Teemu
Petkov, Christopher I.
author_facet Wikman, Patrik
Rinne, Teemu
Petkov, Christopher I.
author_sort Wikman, Patrik
collection PubMed
description In natural settings, the prospect of reward often influences the focus of our attention, but how cognitive and motivational systems influence sensory cortex is not well understood. Also, challenges in training nonhuman animals on cognitive tasks complicate cross-species comparisons and interpreting results on the neurobiological bases of cognition. Incentivized attention tasks could expedite training and evaluate the impact of attention on sensory cortex. Here we develop an Incentivized Attention Paradigm (IAP) and use it to show that macaque monkeys readily learn to use auditory or visual reward cues, drastically influencing their performance within a simple auditory task. Next, this paradigm was used with functional neuroimaging to measure activation modulation in the monkey auditory cortex. The results show modulation of extensive auditory cortical regions throughout primary and non-primary regions, which although a hallmark of attentional modulation in human auditory cortex, has not been studied or observed as broadly in prior data from nonhuman animals. Psycho-physiological interactions were identified between the observed auditory cortex effects and regions including basal forebrain sites along acetylcholinergic and dopaminergic pathways. The findings reveal the impact and regional interactions in the primate brain during an incentivized attention engaging auditory task.
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spelling pubmed-63957752019-03-05 Reward cues readily direct monkeys’ auditory performance resulting in broad auditory cortex modulation and interaction with sites along cholinergic and dopaminergic pathways Wikman, Patrik Rinne, Teemu Petkov, Christopher I. Sci Rep Article In natural settings, the prospect of reward often influences the focus of our attention, but how cognitive and motivational systems influence sensory cortex is not well understood. Also, challenges in training nonhuman animals on cognitive tasks complicate cross-species comparisons and interpreting results on the neurobiological bases of cognition. Incentivized attention tasks could expedite training and evaluate the impact of attention on sensory cortex. Here we develop an Incentivized Attention Paradigm (IAP) and use it to show that macaque monkeys readily learn to use auditory or visual reward cues, drastically influencing their performance within a simple auditory task. Next, this paradigm was used with functional neuroimaging to measure activation modulation in the monkey auditory cortex. The results show modulation of extensive auditory cortical regions throughout primary and non-primary regions, which although a hallmark of attentional modulation in human auditory cortex, has not been studied or observed as broadly in prior data from nonhuman animals. Psycho-physiological interactions were identified between the observed auditory cortex effects and regions including basal forebrain sites along acetylcholinergic and dopaminergic pathways. The findings reveal the impact and regional interactions in the primate brain during an incentivized attention engaging auditory task. Nature Publishing Group UK 2019-02-28 /pmc/articles/PMC6395775/ /pubmed/30816142 http://dx.doi.org/10.1038/s41598-019-38833-y Text en © The Author(s) 2019 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
Wikman, Patrik
Rinne, Teemu
Petkov, Christopher I.
Reward cues readily direct monkeys’ auditory performance resulting in broad auditory cortex modulation and interaction with sites along cholinergic and dopaminergic pathways
title Reward cues readily direct monkeys’ auditory performance resulting in broad auditory cortex modulation and interaction with sites along cholinergic and dopaminergic pathways
title_full Reward cues readily direct monkeys’ auditory performance resulting in broad auditory cortex modulation and interaction with sites along cholinergic and dopaminergic pathways
title_fullStr Reward cues readily direct monkeys’ auditory performance resulting in broad auditory cortex modulation and interaction with sites along cholinergic and dopaminergic pathways
title_full_unstemmed Reward cues readily direct monkeys’ auditory performance resulting in broad auditory cortex modulation and interaction with sites along cholinergic and dopaminergic pathways
title_short Reward cues readily direct monkeys’ auditory performance resulting in broad auditory cortex modulation and interaction with sites along cholinergic and dopaminergic pathways
title_sort reward cues readily direct monkeys’ auditory performance resulting in broad auditory cortex modulation and interaction with sites along cholinergic and dopaminergic pathways
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6395775/
https://www.ncbi.nlm.nih.gov/pubmed/30816142
http://dx.doi.org/10.1038/s41598-019-38833-y
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