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Neural substrates of parallel devaluation-sensitive and devaluation-insensitive Pavlovian learning in humans.

ABSTRACT: We aim to differentiate the brain regions involved in the learning and encoding of Pavlovian associations sensitive to changes in outcome value from those that are not sensitive to such changes by combining a learning task with outcome devaluation, eye-tracking, and functional magnetic resonance imaging in humans. Contrary to theoretical expectation, voxels correlating with reward prediction errors in the ventral striatum and subgenual cingulate appear to be sensitive to devaluation. Moreover, regions encoding state prediction errors appear to be devaluation insensitive. We can also distinguish regions encoding predictions about outcome taste identity from predictions about expected spatial location. Regions encoding predictions about taste identity seem devaluation sensitive while those encoding predictions about an outcome's spatial location seem devaluation insensitive. These findings suggest the existence of multiple and distinct associative mechanisms in the brain and help identify putative neural correlates for the parallel expression of both devaluation sensitive and insensitive conditioned behaviors.

SUBMITTER: Pool ER

PROVIDER: S-EPMC10697955 | biostudies-literature | 2023 Dec

REPOSITORIES: biostudies-literature

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Neural substrates of parallel devaluation-sensitive and devaluation-insensitive Pavlovian learning in humans.

Pool Eva R ER Pauli Wolfgang M WM Cross Logan L O'Doherty John P JP

Nature communications 20231205 1

We aim to differentiate the brain regions involved in the learning and encoding of Pavlovian associations sensitive to changes in outcome value from those that are not sensitive to such changes by combining a learning task with outcome devaluation, eye-tracking, and functional magnetic resonance imaging in humans. Contrary to theoretical expectation, voxels correlating with reward prediction errors in the ventral striatum and subgenual cingulate appear to be sensitive to devaluation. Moreover, r ...[more]

PMID: 38052792

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Project description:Individual differences in Pavlovian approach predict differences in devaluation sensitivity. Recent studies indicate goal-tracking (GT) rats are sensitive to outcome devaluation while sign-tracking (ST) rats are not. With extended training in Pavlovian lever autoshaping (PLA), GT rats display more lever-directed behavior, typical of ST rats, suggesting they may become insensitive to devaluation with more Pavlovian training experience. Here, we use a within-subject satiety-induced outcome devaluation procedure to test devaluation sensitivity after limited and extended PLA training in GT and ST rats. We trained rats in PLA to determine GT and ST groups. Then, we sated rats on either the training pellets (devalued condition) or homecage chow (valued condition) prior to brief non-reinforced test sessions after limited (sessions 5/6) and extended (sessions 17/18) PLA training. GT rats decreased conditioned responding under devalued relative to valued conditions after both limited and extended training, demonstrating they are sensitive to satiety devaluation regardless of the amount of PLA training. While ST rats were insensitive to satiety devaluation after limited training, their lever directed behavior became devaluation sensitive after extended training. To determine whether sign-tracking rats also displayed sensitivity to illness-induced outcome devaluation after extended training, we trained a separate cohort of rats in extended PLA and devalued the outcome with lithium chloride injections after pellet consumption in the homecage. ST rats failed to decrease conditioned responding after illness-induced outcome devaluation, while Non-ST rats (GT and intermediates) were sensitive to illness-induced outcome devaluation after extended training. Together, our results confirm devaluation sensitivity is stable in GT rats across training and devaluation approaches. Extended training unmasks devaluation sensitivity in ST rats after satiety, but not illness-induced devaluation, suggesting ST rats respond appropriately by decreasing responding to cues during state-dependent but not inference-based devaluation. The differences in behavioral flexibility across tracking groups and devaluation paradigms have translational relevance for the understanding state- vs. inference-based reward devaluation as it pertains to drug addiction vulnerability.

Dataset Information

Neural substrates of parallel devaluation-sensitive and devaluation-insensitive Pavlovian learning in humans.

Publications

Neural substrates of parallel devaluation-sensitive and devaluation-insensitive Pavlovian learning in humans.

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