Neurons in the Ventral Striatum Exhibit Cell-Type-Specific Representations of Outcome during Learning

The ventromedial striatum (VMS) is a node in circuits underpinning both affect and reinforcement learning. The cellular bases of these functions and especially their potential linkages have been unclear. VMS cholinergic interneurons, however, have been singled out as being related both to affect and...

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Main Authors: Atallah, Hisham E., McCool, Andrew D., Howe, Mark W., Graybiel, Ann M., Atallah, Hisham E., McCool, Andrew D., Howe, Mark W., Graybiel, Ann M.
Other Authors: Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Format: Article
Language:en_US
Published: Elsevier 2016
Online Access:http://hdl.handle.net/1721.1/102425
https://orcid.org/0000-0002-4326-7720
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author Atallah, Hisham E.
McCool, Andrew D.
Howe, Mark W.
Graybiel, Ann M.
Atallah, Hisham E.
McCool, Andrew D.
Howe, Mark W.
Graybiel, Ann M.
author2 Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
author_facet Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Atallah, Hisham E.
McCool, Andrew D.
Howe, Mark W.
Graybiel, Ann M.
Atallah, Hisham E.
McCool, Andrew D.
Howe, Mark W.
Graybiel, Ann M.
author_sort Atallah, Hisham E.
collection MIT
description The ventromedial striatum (VMS) is a node in circuits underpinning both affect and reinforcement learning. The cellular bases of these functions and especially their potential linkages have been unclear. VMS cholinergic interneurons, however, have been singled out as being related both to affect and to reinforcement-based conditioning, raising the possibility that unique aspects of their signaling could account for these functions. Here we show that VMS tonically active neurons (TANs), including putative cholinergic interneurons, generate unique bidirectional outcome responses during reward-based learning, reporting both positive (reward) and negative (reward omission) outcomes when behavioral change is prompted by switches in reinforcement contingencies. VMS output neurons (SPNs), by contrast, are nearly insensitive to switches in reinforcement contingencies, gradually losing outcome signaling while maintaining responses at trial initiation and goal approach. Thus, TANs and SPNs in the VMS provide distinct signals optimized for different aspects of the learning process.
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spelling mit-1721.1/1024252022-10-02T04:51:42Z Neurons in the Ventral Striatum Exhibit Cell-Type-Specific Representations of Outcome during Learning Atallah, Hisham E. McCool, Andrew D. Howe, Mark W. Graybiel, Ann M. Atallah, Hisham E. McCool, Andrew D. Howe, Mark W. Graybiel, Ann M. Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences McGovern Institute for Brain Research at MIT Atallah, Hisham E. McCool, Andrew D. Howe, Mark W. Graybiel, Ann M. The ventromedial striatum (VMS) is a node in circuits underpinning both affect and reinforcement learning. The cellular bases of these functions and especially their potential linkages have been unclear. VMS cholinergic interneurons, however, have been singled out as being related both to affect and to reinforcement-based conditioning, raising the possibility that unique aspects of their signaling could account for these functions. Here we show that VMS tonically active neurons (TANs), including putative cholinergic interneurons, generate unique bidirectional outcome responses during reward-based learning, reporting both positive (reward) and negative (reward omission) outcomes when behavioral change is prompted by switches in reinforcement contingencies. VMS output neurons (SPNs), by contrast, are nearly insensitive to switches in reinforcement contingencies, gradually losing outcome signaling while maintaining responses at trial initiation and goal approach. Thus, TANs and SPNs in the VMS provide distinct signals optimized for different aspects of the learning process. National Institutes of Health (U.S.) (Grant R01 MH060379) United States. Office of Naval Research (Grant N00014-04-1-0208) European Union (Grant 021716) Cure Huntington’s Disease Initiative, Inc. (Grant A-5552) Nancy Lurie Marks Family Foundation William N. & Bernice E. Bumpus Foundation (Grant RRDA Pilot: 2013.1) 2016-05-09T14:09:18Z 2016-05-09T14:09:18Z 2014-06 Article http://purl.org/eprint/type/JournalArticle 08966273 1097-4199 http://hdl.handle.net/1721.1/102425 Atallah, Hisham E., Andrew D. McCool, Mark W. Howe, and Ann M. Graybiel. “Neurons in the Ventral Striatum Exhibit Cell-Type-Specific Representations of Outcome During Learning.” Neuron 82, no. 5 (June 2014): 1145–1156. https://orcid.org/0000-0002-4326-7720 en_US http://dx.doi.org/10.1016/j.neuron.2014.04.021 Neuron Creative Commons Attribution-NonCommercial-NoDerivs License http://creativecommons.org/licenses/by-nc-nd/4.0/ application/pdf Elsevier PMC
spellingShingle Atallah, Hisham E.
McCool, Andrew D.
Howe, Mark W.
Graybiel, Ann M.
Atallah, Hisham E.
McCool, Andrew D.
Howe, Mark W.
Graybiel, Ann M.
Neurons in the Ventral Striatum Exhibit Cell-Type-Specific Representations of Outcome during Learning
title Neurons in the Ventral Striatum Exhibit Cell-Type-Specific Representations of Outcome during Learning
title_full Neurons in the Ventral Striatum Exhibit Cell-Type-Specific Representations of Outcome during Learning
title_fullStr Neurons in the Ventral Striatum Exhibit Cell-Type-Specific Representations of Outcome during Learning
title_full_unstemmed Neurons in the Ventral Striatum Exhibit Cell-Type-Specific Representations of Outcome during Learning
title_short Neurons in the Ventral Striatum Exhibit Cell-Type-Specific Representations of Outcome during Learning
title_sort neurons in the ventral striatum exhibit cell type specific representations of outcome during learning
url http://hdl.handle.net/1721.1/102425
https://orcid.org/0000-0002-4326-7720
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