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Specialized coding of sensory, motor, and cognitive variables in VTA dopamine neurons

There is increased appreciation that dopamine (DA) neurons in the midbrain respond not only to reward(1) and reward-predicting cues(1,2), but also to other variables such as distance to reward(3), movements(4–9), and behavioral choices(10,11). Based on these findings, a major open question is how th...

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Autores principales: Engelhard, Ben, Finkelstein, Joel, Cox, Julia, Fleming, Weston, Jang, Hee Jae, Ornelas, Sharon, Koay, Sue Ann, Thiberge, Stephan Y., Daw, Nathaniel, Tank, David W., Witten, Ilana B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7147811/
https://www.ncbi.nlm.nih.gov/pubmed/31142844
http://dx.doi.org/10.1038/s41586-019-1261-9
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author Engelhard, Ben
Finkelstein, Joel
Cox, Julia
Fleming, Weston
Jang, Hee Jae
Ornelas, Sharon
Koay, Sue Ann
Thiberge, Stephan Y.
Daw, Nathaniel
Tank, David W.
Witten, Ilana B.
author_facet Engelhard, Ben
Finkelstein, Joel
Cox, Julia
Fleming, Weston
Jang, Hee Jae
Ornelas, Sharon
Koay, Sue Ann
Thiberge, Stephan Y.
Daw, Nathaniel
Tank, David W.
Witten, Ilana B.
author_sort Engelhard, Ben
collection PubMed
description There is increased appreciation that dopamine (DA) neurons in the midbrain respond not only to reward(1) and reward-predicting cues(1,2), but also to other variables such as distance to reward(3), movements(4–9), and behavioral choices(10,11). Based on these findings, a major open question is how the responses to these diverse variables are organized across the population of DA neurons. In other words, do individual DA neurons multiplex multiple variables, or are subsets of neurons specialized in encoding specific behavioral variables? The reason that this fundamental question has been difficult to resolve is that recordings from large populations of individual DA neurons have not been performed in a behavioral task with sufficient complexity to examine these diverse variables simultaneously. To address this gap, we used 2-photon calcium imaging through an implanted lens to record activity of >300 midbrain DA neurons in the ventral tegmental area (VTA) during a complex decision-making task. As mice navigated in a virtual reality (VR) environment, DA neurons encoded an array of sensory, motor, and cognitive variables. These responses were functionally clustered, such that subpopulations of neurons transmitted information about a subset of behavioral variables, in addition to encoding reward. These functional clusters were spatially organized, such that neighboring neurons were more likely to be part of the same cluster. Taken together with the topography between DA neurons and their projections, this specialization and anatomical organization may aid downstream circuits in correctly interpreting the wide range of signals transmitted by DA neurons.
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spelling pubmed-71478112020-04-10 Specialized coding of sensory, motor, and cognitive variables in VTA dopamine neurons Engelhard, Ben Finkelstein, Joel Cox, Julia Fleming, Weston Jang, Hee Jae Ornelas, Sharon Koay, Sue Ann Thiberge, Stephan Y. Daw, Nathaniel Tank, David W. Witten, Ilana B. Nature Article There is increased appreciation that dopamine (DA) neurons in the midbrain respond not only to reward(1) and reward-predicting cues(1,2), but also to other variables such as distance to reward(3), movements(4–9), and behavioral choices(10,11). Based on these findings, a major open question is how the responses to these diverse variables are organized across the population of DA neurons. In other words, do individual DA neurons multiplex multiple variables, or are subsets of neurons specialized in encoding specific behavioral variables? The reason that this fundamental question has been difficult to resolve is that recordings from large populations of individual DA neurons have not been performed in a behavioral task with sufficient complexity to examine these diverse variables simultaneously. To address this gap, we used 2-photon calcium imaging through an implanted lens to record activity of >300 midbrain DA neurons in the ventral tegmental area (VTA) during a complex decision-making task. As mice navigated in a virtual reality (VR) environment, DA neurons encoded an array of sensory, motor, and cognitive variables. These responses were functionally clustered, such that subpopulations of neurons transmitted information about a subset of behavioral variables, in addition to encoding reward. These functional clusters were spatially organized, such that neighboring neurons were more likely to be part of the same cluster. Taken together with the topography between DA neurons and their projections, this specialization and anatomical organization may aid downstream circuits in correctly interpreting the wide range of signals transmitted by DA neurons. 2019-05-29 2019-06 /pmc/articles/PMC7147811/ /pubmed/31142844 http://dx.doi.org/10.1038/s41586-019-1261-9 Text en Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:http://www.nature.com/authors/editorial_policies/license.html#terms
spellingShingle Article
Engelhard, Ben
Finkelstein, Joel
Cox, Julia
Fleming, Weston
Jang, Hee Jae
Ornelas, Sharon
Koay, Sue Ann
Thiberge, Stephan Y.
Daw, Nathaniel
Tank, David W.
Witten, Ilana B.
Specialized coding of sensory, motor, and cognitive variables in VTA dopamine neurons
title Specialized coding of sensory, motor, and cognitive variables in VTA dopamine neurons
title_full Specialized coding of sensory, motor, and cognitive variables in VTA dopamine neurons
title_fullStr Specialized coding of sensory, motor, and cognitive variables in VTA dopamine neurons
title_full_unstemmed Specialized coding of sensory, motor, and cognitive variables in VTA dopamine neurons
title_short Specialized coding of sensory, motor, and cognitive variables in VTA dopamine neurons
title_sort specialized coding of sensory, motor, and cognitive variables in vta dopamine neurons
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7147811/
https://www.ncbi.nlm.nih.gov/pubmed/31142844
http://dx.doi.org/10.1038/s41586-019-1261-9
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