Cargando…

Contexts facilitate dynamic value encoding in the mesolimbic dopamine system

Adaptive behavior in a dynamic environment often requires rapid revaluation of stimuli that deviates from well-learned associations. The divergence between stable value-encoding and appropriate behavioral output remains a critical test to theories of dopamine’s function in learning, motivation, and...

Descripción completa

Detalles Bibliográficos
Autores principales: Fraser, Kurt M., Collins, Val L., Wolff, Amy R., Ottenheimer, David J., Bornhoft, Kaisa N., Pat, Fiona, Chen, Bridget J., Janak, Patricia H, Saunders, Benjamin T.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10635154/
https://www.ncbi.nlm.nih.gov/pubmed/37961363
http://dx.doi.org/10.1101/2023.11.05.565687
_version_ 1785146296582012928
author Fraser, Kurt M.
Collins, Val L.
Wolff, Amy R.
Ottenheimer, David J.
Bornhoft, Kaisa N.
Pat, Fiona
Chen, Bridget J.
Janak, Patricia H
Saunders, Benjamin T.
author_facet Fraser, Kurt M.
Collins, Val L.
Wolff, Amy R.
Ottenheimer, David J.
Bornhoft, Kaisa N.
Pat, Fiona
Chen, Bridget J.
Janak, Patricia H
Saunders, Benjamin T.
author_sort Fraser, Kurt M.
collection PubMed
description Adaptive behavior in a dynamic environment often requires rapid revaluation of stimuli that deviates from well-learned associations. The divergence between stable value-encoding and appropriate behavioral output remains a critical test to theories of dopamine’s function in learning, motivation, and motor control. Yet how dopamine neurons are involved in the revaluation of cues when the world changes to alter our behavior remains unclear. Here we make use of pharmacology, in vivo electrophysiology, fiber photometry, and optogenetics to resolve the contributions of the mesolimbic dopamine system to the dynamic reorganization of reward-seeking. Male and female rats were trained to discriminate when a conditioned stimulus would be followed by sucrose reward by exploiting the prior, non-overlapping presentation of a separate discrete cue - an occasion setter. Only when the occasion setter’s presentation preceded the conditioned stimulus did the conditioned stimulus predict sucrose delivery. As a result, in this task we were able to dissociate the average value of the conditioned stimulus from its immediate expected value on a trial-to-trial basis. Both the activity of ventral tegmental area dopamine neurons and dopamine signaling in the nucleus accumbens were essential for rats to successfully update behavioral responding in response to the occasion setter. Moreover, dopamine release in the nucleus accumbens following the conditioned stimulus only occurred when the occasion setter indicated it would predict reward. Downstream of dopamine release, we found that single neurons in the nucleus accumbens dynamically tracked the value of the conditioned stimulus. Together these results reveal a novel mechanism within the mesolimbic dopamine system for the rapid revaluation of motivation.
format Online
Article
Text
id pubmed-10635154
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Cold Spring Harbor Laboratory
record_format MEDLINE/PubMed
spelling pubmed-106351542023-11-13 Contexts facilitate dynamic value encoding in the mesolimbic dopamine system Fraser, Kurt M. Collins, Val L. Wolff, Amy R. Ottenheimer, David J. Bornhoft, Kaisa N. Pat, Fiona Chen, Bridget J. Janak, Patricia H Saunders, Benjamin T. bioRxiv Article Adaptive behavior in a dynamic environment often requires rapid revaluation of stimuli that deviates from well-learned associations. The divergence between stable value-encoding and appropriate behavioral output remains a critical test to theories of dopamine’s function in learning, motivation, and motor control. Yet how dopamine neurons are involved in the revaluation of cues when the world changes to alter our behavior remains unclear. Here we make use of pharmacology, in vivo electrophysiology, fiber photometry, and optogenetics to resolve the contributions of the mesolimbic dopamine system to the dynamic reorganization of reward-seeking. Male and female rats were trained to discriminate when a conditioned stimulus would be followed by sucrose reward by exploiting the prior, non-overlapping presentation of a separate discrete cue - an occasion setter. Only when the occasion setter’s presentation preceded the conditioned stimulus did the conditioned stimulus predict sucrose delivery. As a result, in this task we were able to dissociate the average value of the conditioned stimulus from its immediate expected value on a trial-to-trial basis. Both the activity of ventral tegmental area dopamine neurons and dopamine signaling in the nucleus accumbens were essential for rats to successfully update behavioral responding in response to the occasion setter. Moreover, dopamine release in the nucleus accumbens following the conditioned stimulus only occurred when the occasion setter indicated it would predict reward. Downstream of dopamine release, we found that single neurons in the nucleus accumbens dynamically tracked the value of the conditioned stimulus. Together these results reveal a novel mechanism within the mesolimbic dopamine system for the rapid revaluation of motivation. Cold Spring Harbor Laboratory 2023-11-05 /pmc/articles/PMC10635154/ /pubmed/37961363 http://dx.doi.org/10.1101/2023.11.05.565687 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Fraser, Kurt M.
Collins, Val L.
Wolff, Amy R.
Ottenheimer, David J.
Bornhoft, Kaisa N.
Pat, Fiona
Chen, Bridget J.
Janak, Patricia H
Saunders, Benjamin T.
Contexts facilitate dynamic value encoding in the mesolimbic dopamine system
title Contexts facilitate dynamic value encoding in the mesolimbic dopamine system
title_full Contexts facilitate dynamic value encoding in the mesolimbic dopamine system
title_fullStr Contexts facilitate dynamic value encoding in the mesolimbic dopamine system
title_full_unstemmed Contexts facilitate dynamic value encoding in the mesolimbic dopamine system
title_short Contexts facilitate dynamic value encoding in the mesolimbic dopamine system
title_sort contexts facilitate dynamic value encoding in the mesolimbic dopamine system
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10635154/
https://www.ncbi.nlm.nih.gov/pubmed/37961363
http://dx.doi.org/10.1101/2023.11.05.565687
work_keys_str_mv AT fraserkurtm contextsfacilitatedynamicvalueencodinginthemesolimbicdopaminesystem
AT collinsvall contextsfacilitatedynamicvalueencodinginthemesolimbicdopaminesystem
AT wolffamyr contextsfacilitatedynamicvalueencodinginthemesolimbicdopaminesystem
AT ottenheimerdavidj contextsfacilitatedynamicvalueencodinginthemesolimbicdopaminesystem
AT bornhoftkaisan contextsfacilitatedynamicvalueencodinginthemesolimbicdopaminesystem
AT patfiona contextsfacilitatedynamicvalueencodinginthemesolimbicdopaminesystem
AT chenbridgetj contextsfacilitatedynamicvalueencodinginthemesolimbicdopaminesystem
AT janakpatriciah contextsfacilitatedynamicvalueencodinginthemesolimbicdopaminesystem
AT saundersbenjamint contextsfacilitatedynamicvalueencodinginthemesolimbicdopaminesystem