Dynamic mesolimbic dopamine signaling during action sequence learning and expectation violation

Prolonged mesolimbic dopamine concentration changes have been detected during spatial navigation, but little is known about the conditions that engender this signaling profile or how it develops with learning. To address this, we monitored dopamine concentration changes in the nucleus accumbens core...

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Main Authors: Collins, Anne L., Greenfield, Venuz Y., Bye, Jeffrey K., Linker, Kay E., Wang, Alice S., Wassum, Kate M.
Format: Online
Language:English
Published: Nature Publishing Group 2016
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4751524/
id pubmed-4751524
recordtype oai_dc
spelling pubmed-47515242016-02-22 Dynamic mesolimbic dopamine signaling during action sequence learning and expectation violation Collins, Anne L. Greenfield, Venuz Y. Bye, Jeffrey K. Linker, Kay E. Wang, Alice S. Wassum, Kate M. Article Prolonged mesolimbic dopamine concentration changes have been detected during spatial navigation, but little is known about the conditions that engender this signaling profile or how it develops with learning. To address this, we monitored dopamine concentration changes in the nucleus accumbens core of rats throughout acquisition and performance of an instrumental action sequence task. Prolonged dopamine concentration changes were detected that ramped up as rats executed each action sequence and declined after earned reward collection. With learning, dopamine concentration began to rise increasingly earlier in the execution of the sequence and ultimately backpropagated away from stereotyped sequence actions, becoming only transiently elevated by the most distal and unexpected reward predictor. Action sequence-related dopamine signaling was reactivated in well-trained rats if they became disengaged in the task and in response to an unexpected change in the value, but not identity of the earned reward. Throughout training and test, dopamine signaling correlated with sequence performance. These results suggest that action sequences can engender a prolonged mode of dopamine signaling in the nucleus accumbens core and that such signaling relates to elements of the motivation underlying sequence execution and is dynamic with learning, overtraining and violations in reward expectation. Nature Publishing Group 2016-02-12 /pmc/articles/PMC4751524/ /pubmed/26869075 http://dx.doi.org/10.1038/srep20231 Text en Copyright © 2016, Macmillan Publishers Limited http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Collins, Anne L.
Greenfield, Venuz Y.
Bye, Jeffrey K.
Linker, Kay E.
Wang, Alice S.
Wassum, Kate M.
spellingShingle Collins, Anne L.
Greenfield, Venuz Y.
Bye, Jeffrey K.
Linker, Kay E.
Wang, Alice S.
Wassum, Kate M.
Dynamic mesolimbic dopamine signaling during action sequence learning and expectation violation
author_facet Collins, Anne L.
Greenfield, Venuz Y.
Bye, Jeffrey K.
Linker, Kay E.
Wang, Alice S.
Wassum, Kate M.
author_sort Collins, Anne L.
title Dynamic mesolimbic dopamine signaling during action sequence learning and expectation violation
title_short Dynamic mesolimbic dopamine signaling during action sequence learning and expectation violation
title_full Dynamic mesolimbic dopamine signaling during action sequence learning and expectation violation
title_fullStr Dynamic mesolimbic dopamine signaling during action sequence learning and expectation violation
title_full_unstemmed Dynamic mesolimbic dopamine signaling during action sequence learning and expectation violation
title_sort dynamic mesolimbic dopamine signaling during action sequence learning and expectation violation
description Prolonged mesolimbic dopamine concentration changes have been detected during spatial navigation, but little is known about the conditions that engender this signaling profile or how it develops with learning. To address this, we monitored dopamine concentration changes in the nucleus accumbens core of rats throughout acquisition and performance of an instrumental action sequence task. Prolonged dopamine concentration changes were detected that ramped up as rats executed each action sequence and declined after earned reward collection. With learning, dopamine concentration began to rise increasingly earlier in the execution of the sequence and ultimately backpropagated away from stereotyped sequence actions, becoming only transiently elevated by the most distal and unexpected reward predictor. Action sequence-related dopamine signaling was reactivated in well-trained rats if they became disengaged in the task and in response to an unexpected change in the value, but not identity of the earned reward. Throughout training and test, dopamine signaling correlated with sequence performance. These results suggest that action sequences can engender a prolonged mode of dopamine signaling in the nucleus accumbens core and that such signaling relates to elements of the motivation underlying sequence execution and is dynamic with learning, overtraining and violations in reward expectation.
publisher Nature Publishing Group
publishDate 2016
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4751524/
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