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Distinct representation of cue-outcome association by D1 and D2 neurons in the ventral striatum’s olfactory tubercle

Positive and negative associations acquired through olfactory experience are thought to be especially strong and long-lasting. The conserved direct olfactory sensory input to the ventral striatal olfactory tubercle (OT) and its convergence with dense dopaminergic input to the OT could underlie this...

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Autores principales: Martiros, Nuné, Kapoor, Vikrant, Kim, Spencer E, Murthy, Venkatesh N
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9203051/
https://www.ncbi.nlm.nih.gov/pubmed/35708179
http://dx.doi.org/10.7554/eLife.75463
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author Martiros, Nuné
Kapoor, Vikrant
Kim, Spencer E
Murthy, Venkatesh N
author_facet Martiros, Nuné
Kapoor, Vikrant
Kim, Spencer E
Murthy, Venkatesh N
author_sort Martiros, Nuné
collection PubMed
description Positive and negative associations acquired through olfactory experience are thought to be especially strong and long-lasting. The conserved direct olfactory sensory input to the ventral striatal olfactory tubercle (OT) and its convergence with dense dopaminergic input to the OT could underlie this privileged form of associative memory, but how this process occurs is not well understood. We imaged the activity of the two canonical types of striatal neurons, expressing D1- or D2-type dopamine receptors, in the OT at cellular resolution while mice learned odor-outcome associations ranging from aversive to rewarding. D1 and D2 neurons both responded to rewarding and aversive odors. D1 neurons in the OT robustly and bidirectionally represented odor valence, responding similarly to odors predicting similar outcomes regardless of odor identity. This valence representation persisted even in the absence of a licking response to the odors and in the absence of the outcomes, indicating a true transformation of odor sensory information by D1 OT neurons. In contrast, D2 neuronal representation of the odor-outcome associations was weaker, contingent on a licking response by the mouse, and D2 neurons were more selective for odor identity than valence. Stimulus valence coding in the OT was modality-sensitive, with separate sets of D1 neurons responding to odors and sounds predicting the same outcomes, suggesting that integration of multimodal valence information happens downstream of the OT. Our results point to distinct representation of identity and valence of odor stimuli by D1 and D2 neurons in the OT.
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spelling pubmed-92030512022-06-17 Distinct representation of cue-outcome association by D1 and D2 neurons in the ventral striatum’s olfactory tubercle Martiros, Nuné Kapoor, Vikrant Kim, Spencer E Murthy, Venkatesh N eLife Neuroscience Positive and negative associations acquired through olfactory experience are thought to be especially strong and long-lasting. The conserved direct olfactory sensory input to the ventral striatal olfactory tubercle (OT) and its convergence with dense dopaminergic input to the OT could underlie this privileged form of associative memory, but how this process occurs is not well understood. We imaged the activity of the two canonical types of striatal neurons, expressing D1- or D2-type dopamine receptors, in the OT at cellular resolution while mice learned odor-outcome associations ranging from aversive to rewarding. D1 and D2 neurons both responded to rewarding and aversive odors. D1 neurons in the OT robustly and bidirectionally represented odor valence, responding similarly to odors predicting similar outcomes regardless of odor identity. This valence representation persisted even in the absence of a licking response to the odors and in the absence of the outcomes, indicating a true transformation of odor sensory information by D1 OT neurons. In contrast, D2 neuronal representation of the odor-outcome associations was weaker, contingent on a licking response by the mouse, and D2 neurons were more selective for odor identity than valence. Stimulus valence coding in the OT was modality-sensitive, with separate sets of D1 neurons responding to odors and sounds predicting the same outcomes, suggesting that integration of multimodal valence information happens downstream of the OT. Our results point to distinct representation of identity and valence of odor stimuli by D1 and D2 neurons in the OT. eLife Sciences Publications, Ltd 2022-06-16 /pmc/articles/PMC9203051/ /pubmed/35708179 http://dx.doi.org/10.7554/eLife.75463 Text en © 2022, Martiros et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Martiros, Nuné
Kapoor, Vikrant
Kim, Spencer E
Murthy, Venkatesh N
Distinct representation of cue-outcome association by D1 and D2 neurons in the ventral striatum’s olfactory tubercle
title Distinct representation of cue-outcome association by D1 and D2 neurons in the ventral striatum’s olfactory tubercle
title_full Distinct representation of cue-outcome association by D1 and D2 neurons in the ventral striatum’s olfactory tubercle
title_fullStr Distinct representation of cue-outcome association by D1 and D2 neurons in the ventral striatum’s olfactory tubercle
title_full_unstemmed Distinct representation of cue-outcome association by D1 and D2 neurons in the ventral striatum’s olfactory tubercle
title_short Distinct representation of cue-outcome association by D1 and D2 neurons in the ventral striatum’s olfactory tubercle
title_sort distinct representation of cue-outcome association by d1 and d2 neurons in the ventral striatum’s olfactory tubercle
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9203051/
https://www.ncbi.nlm.nih.gov/pubmed/35708179
http://dx.doi.org/10.7554/eLife.75463
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