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Ventral striatum dopamine release encodes unique properties of visual stimuli in mice

The mesolimbic dopamine system is an evolutionarily conserved set of brain circuits that play a role in attention, appetitive behavior, and reward processing. In this circuitry, ascending dopaminergic projections from the ventral midbrain innervate targets throughout the limbic forebrain, such as th...

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Autores principales: Gonzalez, L Sofia, Fisher, Austen A, D'Souza, Shane P, Cotella, Evelin M, Lang, Richard A, Robinson, J Elliott
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10162799/
https://www.ncbi.nlm.nih.gov/pubmed/37067979
http://dx.doi.org/10.7554/eLife.85064
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author Gonzalez, L Sofia
Fisher, Austen A
D'Souza, Shane P
Cotella, Evelin M
Lang, Richard A
Robinson, J Elliott
author_facet Gonzalez, L Sofia
Fisher, Austen A
D'Souza, Shane P
Cotella, Evelin M
Lang, Richard A
Robinson, J Elliott
author_sort Gonzalez, L Sofia
collection PubMed
description The mesolimbic dopamine system is an evolutionarily conserved set of brain circuits that play a role in attention, appetitive behavior, and reward processing. In this circuitry, ascending dopaminergic projections from the ventral midbrain innervate targets throughout the limbic forebrain, such as the ventral striatum/nucleus accumbens (NAc). Dopaminergic signaling in the NAc has been widely studied for its role in behavioral reinforcement, reward prediction error encoding, and motivational salience. Less well characterized is the role of dopaminergic neurotransmission in the response to surprising or alerting sensory events. To address this, we used the genetically encoded dopamine sensor dLight1 and fiber photometry to explore the ability of striatal dopamine release to encode the properties of salient sensory stimuli in mice, such as threatening looming discs. Here, we report that lateral NAc (LNAc) dopamine release encodes the rate and magnitude of environmental luminance changes rather than the visual stimulus threat level. This encoding is highly sensitive, as LNAc dopamine could be evoked by light intensities that were imperceptible to human experimenters. We also found that light-evoked dopamine responses are wavelength-dependent at low irradiances, independent of the circadian cycle, robust to previous exposure history, and involve multiple phototransduction pathways. Thus, we have further elaborated the mesolimbic dopamine system’s ability to encode visual information in mice, which is likely relevant to a wide body of scientists employing light sources or optical methods in behavioral research involving rodents.
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spelling pubmed-101627992023-05-06 Ventral striatum dopamine release encodes unique properties of visual stimuli in mice Gonzalez, L Sofia Fisher, Austen A D'Souza, Shane P Cotella, Evelin M Lang, Richard A Robinson, J Elliott eLife Neuroscience The mesolimbic dopamine system is an evolutionarily conserved set of brain circuits that play a role in attention, appetitive behavior, and reward processing. In this circuitry, ascending dopaminergic projections from the ventral midbrain innervate targets throughout the limbic forebrain, such as the ventral striatum/nucleus accumbens (NAc). Dopaminergic signaling in the NAc has been widely studied for its role in behavioral reinforcement, reward prediction error encoding, and motivational salience. Less well characterized is the role of dopaminergic neurotransmission in the response to surprising or alerting sensory events. To address this, we used the genetically encoded dopamine sensor dLight1 and fiber photometry to explore the ability of striatal dopamine release to encode the properties of salient sensory stimuli in mice, such as threatening looming discs. Here, we report that lateral NAc (LNAc) dopamine release encodes the rate and magnitude of environmental luminance changes rather than the visual stimulus threat level. This encoding is highly sensitive, as LNAc dopamine could be evoked by light intensities that were imperceptible to human experimenters. We also found that light-evoked dopamine responses are wavelength-dependent at low irradiances, independent of the circadian cycle, robust to previous exposure history, and involve multiple phototransduction pathways. Thus, we have further elaborated the mesolimbic dopamine system’s ability to encode visual information in mice, which is likely relevant to a wide body of scientists employing light sources or optical methods in behavioral research involving rodents. eLife Sciences Publications, Ltd 2023-04-17 /pmc/articles/PMC10162799/ /pubmed/37067979 http://dx.doi.org/10.7554/eLife.85064 Text en © 2023, Gonzalez, Fisher 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
Gonzalez, L Sofia
Fisher, Austen A
D'Souza, Shane P
Cotella, Evelin M
Lang, Richard A
Robinson, J Elliott
Ventral striatum dopamine release encodes unique properties of visual stimuli in mice
title Ventral striatum dopamine release encodes unique properties of visual stimuli in mice
title_full Ventral striatum dopamine release encodes unique properties of visual stimuli in mice
title_fullStr Ventral striatum dopamine release encodes unique properties of visual stimuli in mice
title_full_unstemmed Ventral striatum dopamine release encodes unique properties of visual stimuli in mice
title_short Ventral striatum dopamine release encodes unique properties of visual stimuli in mice
title_sort ventral striatum dopamine release encodes unique properties of visual stimuli in mice
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10162799/
https://www.ncbi.nlm.nih.gov/pubmed/37067979
http://dx.doi.org/10.7554/eLife.85064
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