A bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memories
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).
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A bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memoriesDryad Digital Repository, doi:10.5068/dryad.D1109S.
Article and author information
Author details
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
- 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
- Received: March 21, 2021
- Accepted: June 16, 2021
- Accepted Manuscript published: June 18, 2021 (version 1)
- 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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