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Synchronicity: The Role of Midbrain Dopamine in Whole-Brain Coordination

Midbrain dopamine seems to play an outsized role in motivated behavior and learning. Widely associated with mediating reward-related behavior, decision making, and learning, dopamine continues to generate controversies in the field. While many studies and theories focus on what dopamine cells encode...

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Detalles Bibliográficos
Autores principales: Beeler, Jeff A., Kisbye Dreyer, Jakob
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6500793/
https://www.ncbi.nlm.nih.gov/pubmed/31053604
http://dx.doi.org/10.1523/ENEURO.0345-18.2019
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author Beeler, Jeff A.
Kisbye Dreyer, Jakob
author_facet Beeler, Jeff A.
Kisbye Dreyer, Jakob
author_sort Beeler, Jeff A.
collection PubMed
description Midbrain dopamine seems to play an outsized role in motivated behavior and learning. Widely associated with mediating reward-related behavior, decision making, and learning, dopamine continues to generate controversies in the field. While many studies and theories focus on what dopamine cells encode, the question of how the midbrain derives the information it encodes is poorly understood and comparatively less addressed. Recent anatomical studies suggest greater diversity and complexity of afferent inputs than previously appreciated, requiring rethinking of prior models. Here, we elaborate a hypothesis that construes midbrain dopamine as implementing a Bayesian selector in which individual dopamine cells sample afferent activity across distributed brain substrates, comprising evidence to be evaluated on the extent to which stimuli in the on-going sensorimotor stream organizes distributed, parallel processing, reflecting implicit value. To effectively generate a temporally resolved phasic signal, a population of dopamine cells must exhibit synchronous activity. We argue that synchronous activity across a population of dopamine cells signals consensus across distributed afferent substrates, invigorating responding to recognized opportunities and facilitating further learning. In framing our hypothesis, we shift from the question of how value is computed to the broader question of how the brain achieves coordination across distributed, parallel processing. We posit the midbrain is part of an “axis of agency” in which the prefrontal cortex (PFC), basal ganglia (BGS), and midbrain form an axis mediating control, coordination, and consensus, respectively.
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spelling pubmed-65007932019-05-06 Synchronicity: The Role of Midbrain Dopamine in Whole-Brain Coordination Beeler, Jeff A. Kisbye Dreyer, Jakob eNeuro Commentary Midbrain dopamine seems to play an outsized role in motivated behavior and learning. Widely associated with mediating reward-related behavior, decision making, and learning, dopamine continues to generate controversies in the field. While many studies and theories focus on what dopamine cells encode, the question of how the midbrain derives the information it encodes is poorly understood and comparatively less addressed. Recent anatomical studies suggest greater diversity and complexity of afferent inputs than previously appreciated, requiring rethinking of prior models. Here, we elaborate a hypothesis that construes midbrain dopamine as implementing a Bayesian selector in which individual dopamine cells sample afferent activity across distributed brain substrates, comprising evidence to be evaluated on the extent to which stimuli in the on-going sensorimotor stream organizes distributed, parallel processing, reflecting implicit value. To effectively generate a temporally resolved phasic signal, a population of dopamine cells must exhibit synchronous activity. We argue that synchronous activity across a population of dopamine cells signals consensus across distributed afferent substrates, invigorating responding to recognized opportunities and facilitating further learning. In framing our hypothesis, we shift from the question of how value is computed to the broader question of how the brain achieves coordination across distributed, parallel processing. We posit the midbrain is part of an “axis of agency” in which the prefrontal cortex (PFC), basal ganglia (BGS), and midbrain form an axis mediating control, coordination, and consensus, respectively. Society for Neuroscience 2019-05-03 /pmc/articles/PMC6500793/ /pubmed/31053604 http://dx.doi.org/10.1523/ENEURO.0345-18.2019 Text en Copyright © 2019 Beeler and Dreyer http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Commentary
Beeler, Jeff A.
Kisbye Dreyer, Jakob
Synchronicity: The Role of Midbrain Dopamine in Whole-Brain Coordination
title Synchronicity: The Role of Midbrain Dopamine in Whole-Brain Coordination
title_full Synchronicity: The Role of Midbrain Dopamine in Whole-Brain Coordination
title_fullStr Synchronicity: The Role of Midbrain Dopamine in Whole-Brain Coordination
title_full_unstemmed Synchronicity: The Role of Midbrain Dopamine in Whole-Brain Coordination
title_short Synchronicity: The Role of Midbrain Dopamine in Whole-Brain Coordination
title_sort synchronicity: the role of midbrain dopamine in whole-brain coordination
topic Commentary
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6500793/
https://www.ncbi.nlm.nih.gov/pubmed/31053604
http://dx.doi.org/10.1523/ENEURO.0345-18.2019
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