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

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 proce...

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Main Authors: Ana C Sias, Ashleigh K Morse, Sherry Wang, Venuz Y Greenfield, Caitlin M Goodpaster, Tyler M Wrenn, Andrew M Wikenheiser, Sandra M Holley, Carlos Cepeda, Michael S Levine, Kate M Wassum
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-06-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/68617
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author Ana C Sias
Ashleigh K Morse
Sherry Wang
Venuz Y Greenfield
Caitlin M Goodpaster
Tyler M Wrenn
Andrew M Wikenheiser
Sandra M Holley
Carlos Cepeda
Michael S Levine
Kate M Wassum
spellingShingle Ana C Sias
Ashleigh K Morse
Sherry Wang
Venuz Y Greenfield
Caitlin M Goodpaster
Tyler M Wrenn
Andrew M Wikenheiser
Sandra M Holley
Carlos Cepeda
Michael S Levine
Kate M Wassum
A bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memories
eLife
decision making
pavlovian-to-instrumental transfer
basolateral amygdala
orbitofrontal cortex
learning
memory
author_facet Ana C Sias
Ashleigh K Morse
Sherry Wang
Venuz Y Greenfield
Caitlin M Goodpaster
Tyler M Wrenn
Andrew M Wikenheiser
Sandra M Holley
Carlos Cepeda
Michael S Levine
Kate M Wassum
author_sort Ana C Sias
title A bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memories
title_short A bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memories
title_full A bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memories
title_fullStr A bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memories
title_full_unstemmed A bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memories
title_sort bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memories
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2021-06-01
description 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 rewards 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 lOFC→BLA and BLA→lOFC pathways form a functional circuit regulating the encoding (lOFC→BLA) and subsequent use (BLA→lOFC) of the stimulus-dependent, sensory-specific reward memories that are critical for adaptive, appetitive decision making.
topic decision making
pavlovian-to-instrumental transfer
basolateral amygdala
orbitofrontal cortex
learning
memory
url https://elifesciences.org/articles/68617
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spelling doaj-f13e8ca44fc446ad953247be2041e83e2021-07-08T15:10:55ZengeLife Sciences Publications LtdeLife2050-084X2021-06-011010.7554/eLife.68617A bidirectional corticoamygdala circuit for the encoding and retrieval of detailed reward memoriesAna C Sias0Ashleigh K Morse1https://orcid.org/0000-0003-0773-5790Sherry Wang2Venuz Y Greenfield3Caitlin M Goodpaster4https://orcid.org/0000-0002-2456-9010Tyler M Wrenn5Andrew M Wikenheiser6Sandra M Holley7Carlos Cepeda8Michael S Levine9Kate M Wassum10https://orcid.org/0000-0002-2635-7433Department of Psychology, University of California, Los Angeles, Los Angeles, United StatesDepartment of Psychology, University of California, Los Angeles, Los Angeles, United StatesDepartment of Psychology, University of California, Los Angeles, Los Angeles, United StatesDepartment of Psychology, University of California, Los Angeles, Los Angeles, United StatesDepartment of Psychology, University of California, Los Angeles, Los Angeles, United StatesDepartment of Psychology, University of California, Los Angeles, Los Angeles, United StatesDepartment of Psychology, University of California, Los Angeles, Los Angeles, United States; Brain Research Institute, University of California, Los Angeles, Los Angeles, United States; Integrative Center for Learning and Memory, University of California, Los Angeles, Los Angeles, United StatesIntellectual and Developmental Disabilities Research Center, Semel Institute for Neuroscience and Human Behavior, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, United StatesIntellectual and Developmental Disabilities Research Center, Semel Institute for Neuroscience and Human Behavior, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, United StatesBrain Research Institute, University of California, Los Angeles, Los Angeles, United States; Intellectual and Developmental Disabilities Research Center, Semel Institute for Neuroscience and Human Behavior, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, United StatesDepartment of Psychology, University of California, Los Angeles, Los Angeles, United States; Brain Research Institute, University of California, Los Angeles, Los Angeles, United States; Integrative Center for Learning and Memory, University of California, Los Angeles, Los Angeles, United States; Integrative Center for Addictive Disorders, University of California, Los Angeles, Los Angeles, United StatesAdaptive 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 rewards 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 lOFC→BLA and BLA→lOFC pathways form a functional circuit regulating the encoding (lOFC→BLA) and subsequent use (BLA→lOFC) of the stimulus-dependent, sensory-specific reward memories that are critical for adaptive, appetitive decision making.https://elifesciences.org/articles/68617decision makingpavlovian-to-instrumental transferbasolateral amygdalaorbitofrontal cortexlearningmemory