A bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memories

  1. Ana C Sias
  2. Ashleigh K Morse
  3. Sherry Wang
  4. Venuz Y Greenfield
  5. Caitlin M Goodpaster
  6. Tyler M Wrenn
  7. Andrew Wikenheiser
  8. Sandra M Holley
  9. Carlos Cepeda
  10. Michael S Levine
  11. Kate M Wassum  Is a corresponding author
  1. University of California, Los Angeles, United States
  2. Matilda Centre, University of Sydney, Australia
  3. UCLA, United States

Abstract

Adaptive reward-related decision making often requires accurate and detailed representation of potential available rewards. Environmental reward-predictive stimuli can facilitate these representations, allowing one to infer which specific rewards might be available and choose accordingly. This process relies on encoded relationships between the cues and the sensory-specific details of the reward they predict. Here we interrogated the function of the basolateral amygdala (BLA) and its interaction with the lateral orbitofrontal cortex (lOFC) in the ability to learn such stimulus-outcome associations and use these memories to guide decision making. Using optical recording and inhibition approaches, Pavlovian cue-reward conditioning, and the outcome-selective Pavlovian-to-instrumental transfer (PIT) test in male rats, we found that the BLA is robustly activated at the time of stimulus-outcome learning and that this activity is necessary for sensory-specific stimulus-outcome memories to be encoded, so they can subsequently influence reward choices. Direct input from the lOFC was found to support the BLA in this function. Based on prior work, activity in BLA projections back to the lOFC was known to support the use of stimulus-outcome memories to influence decision making. By multiplexing optogenetic and chemogenetic inhibition we performed a serial circuit disconnection and found that the lOFCàBLA and BLAàlOFC pathways form a functional circuit regulating the encoding (lOFCàBLA) and subsequent use (BLAàlOFC) of the stimulus-dependent, sensory-specific reward memories that are critical for adaptive, appetitive decision making.

Data availability

All data and code support the findings of this study are available from the corresponding author upon request and via Dryad (doi:10.5068/D1109S).

The following data sets were generated

Article and author information

Author details

  1. Ana C Sias

    Department of Psychology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    No competing interests declared.
  2. Ashleigh K Morse

    Faculty of Medicine and Health, Matilda Centre, University of Sydney, Darlington, Australia
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0773-5790
  3. Sherry Wang

    Department of Psychology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    No competing interests declared.
  4. Venuz Y Greenfield

    Department of Psychology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    No competing interests declared.
  5. Caitlin M Goodpaster

    Department of Psychology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2456-9010
  6. Tyler M Wrenn

    Department of Psychology, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    No competing interests declared.
  7. Andrew Wikenheiser

    UCLA, Los Angeles, United States
    Competing interests
    No competing interests declared.
  8. Sandra M Holley

    Intellectual and Developmental Disabilities Research Center, Brain Research Institute, Semel Institute for Neuroscience, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    No competing interests declared.
  9. Carlos Cepeda

    UCLA, Los Angeles, United States
    Competing interests
    No competing interests declared.
  10. Michael S Levine

    Intellectual and Developmental Disabilities Research Center, Brain Research Institute, Semel Institute for Neuroscience, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    No competing interests declared.
  11. Kate M Wassum

    Department of Psychology, University of California, Los Angeles, Los Angeles, United States
    For correspondence
    kwassum@ucla.edu
    Competing interests
    Kate M Wassum, Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2635-7433

Funding

National Institutes of Health (DA035443)

  • Kate M Wassum

National Science Foundation

  • Ana C Sias

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

Reviewing Editor

  1. Naoshige Uchida, Harvard University, United States

Ethics

Animal experimentation: All procedures were conducted in accordance with the NIH Guide for the Care and Use of Laboratory Animals and were approved by the UCLA Institutional Animal Care and Use Committee.

Version history

  1. Received: March 21, 2021
  2. Accepted: June 16, 2021
  3. Accepted Manuscript published: June 18, 2021 (version 1)
  4. Version of Record published: July 8, 2021 (version 2)

Copyright

© 2021, Sias 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. Ana C Sias
  2. Ashleigh K Morse
  3. Sherry Wang
  4. Venuz Y Greenfield
  5. Caitlin M Goodpaster
  6. Tyler M Wrenn
  7. Andrew Wikenheiser
  8. Sandra M Holley
  9. Carlos Cepeda
  10. Michael S Levine
  11. Kate M Wassum
(2021)
A bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memories
eLife 10:e68617.
https://doi.org/10.7554/eLife.68617

Share this article

https://doi.org/10.7554/eLife.68617

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