Amygdala-Cortical Control of Striatal Plasticity Drives the Acquisition of Goal-Directed Action

Fisher, Simon D.; Ferguson, Lachlan A.; Bertran‐Gonzalez, Jesus; Balleine, Bernard W.

doi:10.1016/j.cub.2020.08.090

Cited by 23 publications

(16 citation statements)

References 29 publications

(37 reference statements)

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“…Thus lOFCBLAlOFC is a functional circuit for the encoding (lOFCBLA) and subsequent use (BLAlOFC) of sensory-specific reward memories. Although the BLA-lOFC circuit is not the only amygdala circuit involved in sensory-specific reward memory (Corbit et al, 2013;Fisher et al, 2020;Kochli et al, 2020;Morse et al, 2020;Parkes & Balleine, 2013), we have found it to be a critical one, consistent with prior evidence from disconnection lesions in non-human primates (Baxter et al, 2000;Fiuzat et al, 2017).…”

Section: Discussionsupporting

confidence: 88%

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

Sias¹,

Morse²,

Wang³

et al. 2021

Preprint

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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 an 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 that 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 to perform a serial circuit disconnection, we found that activity in lOFC→BLA projections regulates the encoding of the same components of the stimulus-outcome memory that are later used to allow cues to guide choice via activity in BLA→lOFC projections. Thus, the lOFC→BLA→lOFC circuit regulates 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.

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Section: Discussionsupporting

confidence: 88%

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

Sias¹,

Morse²,

Wang³

et al. 2021

Preprint

View full text Add to dashboard Cite

show abstract

“…The encoding of such information would have been disrupted by bilateral lOFCBLA or BLA inactivation during learning, but in the disconnection experiment could have been learned in the hemisphere that did not receive lOFCBLA inactivation and subsequently retrieved via an alternate BLA pathway. Indeed, BLAlOFC are not the only amygdala projections involved in reward memory (Beyeler et al, 2016;Corbit et al, 2013;Fisher et al, 2020;Kochli et al, 2020;Morse et al, 2020;Parkes & Balleine, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…The encoding of such information would have been disrupted by bilateral lOFC→BLA or BLA inactivation during learning, but in the disconnection experiment could have been learned in the hemisphere that did not receive lOFC→BLA inactivation and subsequently retrieved via an alternate BLA pathway. Indeed, BLA→lOFC are not the only amygdala projections involved in reward memory ( Beyeler et al, 2016 ; Corbit et al, 2013 ; Fisher et al, 2020 ; Kochli et al, 2020 ; Morse et al, 2020 ; Parkes and Balleine, 2013 ). lOFC activity in both humans and non-human animals can encode the features of an expected reward ( Howard et al, 2015 ; Howard and Kahnt, 2018 ; Klein-Flügge et al, 2013 ; Lopatina et al, 2015 ; McDannald et al, 2014 ; Pritchard et al, 2005 ; Suzuki et al, 2017 ; van Duuren et al, 2007 ; Zhou et al, 2019 ) and the lOFC has been proposed to be critical for using this information to guide decision making ( Bradfield and Hart, 2020 ; Delamater, 2007 ; Groman et al, 2019 ; Keiflin et al, 2013 ; Rich and Wallis, 2016 ; Rudebeck and Rich, 2018 ; Rudebeck and Murray, 2014 ; Sharpe and Schoenbaum, 2016 ; Wilson et al, 2014 ).…”

Section: Discussionmentioning

confidence: 99%

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

Sias

Morse

Wang

et al. 2021

eLife

View full text Add to dashboard Cite

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.

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“…In mammals and rodents in particular, the areas involved in goal-oriented action are comparatively similar to those of birds, and rely on cognitive processes depending on a circuit of cortical, limbic and striatal areas, centered in the posterior dorsomedial striatum (Fisher et al 2020).…”

Section: Natale Emilio Baldaccinimentioning

confidence: 99%

Moving towards a far-away goal: a foreword

Baldaccini

2021

Ethology Ecology & Evolution

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Amygdala-Cortical Control of Striatal Plasticity Drives the Acquisition of Goal-Directed Action

Cited by 23 publications

References 29 publications

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

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

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

Moving towards a far-away goal: a foreword

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