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

  1. L Sofia Gonzalez
  2. Austen A Fisher
  3. Shane P D'Souza
  4. Evelin M Cotella
  5. Richard A Lang
  6. J Elliott Robinson  Is a corresponding author
  1. Cincinnati Children's Hospital Medical Center, United States

Abstract

The mesolimbic dopamine system is an evolutionarily conserved set of brain circuits that plays 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 in 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 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.

Data availability

Viral vector plasmids used in this study are available on Addgene. Codes used for fiber photometry signal extraction and analysis are available at https://www.tdt.com/docs/sdk/offline-data-analysis/offline-data-python/FibPhoEpocAveraging/. Codes used for visual stimulus generation are available at https://github.com/jelliottrobinson/Robinson_Lab. Source data is available in the provided Supplemental Data and Statistical Analysis file.

Article and author information

Author details

  1. L Sofia Gonzalez

    Department of Pediatrics, Cincinnati Children's Hospital Medical Center, Cincinnati, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Austen A Fisher

    Department of Pediatrics, Cincinnati Children's Hospital Medical Center, Cincinnati, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Shane P D'Souza

    Abrahamson Pediatric Eye Institute, Cincinnati Children's Hospital Medical Center, Cincinnati, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6344-1434
  4. Evelin M Cotella

    Department of Pediatrics, Cincinnati Children's Hospital Medical Center, Cincinnati, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Richard A Lang

    Abrahamson Pediatric Eye Institute, Cincinnati Children's Hospital Medical Center, Cincinnati, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. J Elliott Robinson

    Department of Pediatrics, Cincinnati Children's Hospital Medical Center, Cincinnati, United States
    For correspondence
    elliott.robinson@cchmc.org
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9417-3938

Funding

Simons Foundation Autism Research Initiative (BTI Award 663007)

  • J Elliott Robinson

Gilbert Family Foundation (Team Science Award)

  • J Elliott Robinson

Cincinnati Children's Research Foundation (Trustee Award)

  • J Elliott Robinson

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Animal husbandry and experimental procedures involving animal subjects were conducted in compliance with the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health and approved by the Institutional Animal Care and Use Committee (IACUC) and by the Department of Veterinary Services at Cincinnati Children's Hospital Medical Center (CCHMC) under IACUC protocol 2020-0058.

Copyright

© 2023, Gonzalez et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. L Sofia Gonzalez
  2. Austen A Fisher
  3. Shane P D'Souza
  4. Evelin M Cotella
  5. Richard A Lang
  6. J Elliott Robinson
(2023)
Ventral striatum dopamine release encodes unique properties of visual stimuli in mice
eLife 12:e85064.
https://doi.org/10.7554/eLife.85064

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https://doi.org/10.7554/eLife.85064