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Instrumental Avoidance Promotes Safety Learning Across Distributed Neural Circuits
Zhenfu Wen1, Lihan Cui1, Muhammad Badarnee1
1Faillace Department of Psychiatry and Behavioral Sciences, McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, Texas.
Background:
Instrumental avoidance is a coping strategy that plays a critical role in anxiety and trauma-related disorders. However, the neural mechanisms supporting instrumental avoidance and its interaction with extinction learning remain incompletely understood.
Methods:
Fifty-nine healthy adults completed a 2-day functional magnetic resonance imaging paradigm including Pavlovian threat conditioning, avoidance learning, extinction, and memory recall. Subjective reports measuring the fear ratings for each conditioned stimulus (CS) were administered and analyzed across all experimental phases. Neural responses were analyzed using univariate general linear modeling and multivariate pattern analysis with a validated threat/safety decoder. To assess generalizability, the analysis pipeline was repeated in an independent cohort (n = 59) using a variant design.
Results:
Subjective fear ratings indicated successful fear acquisition, instrumental avoidance learning, and extinction learning. During extinction recall, fear ratings to the avoidable CS+ (CS+A) were significantly lower compared with those for the nonavoidable CS+ (CS+N). As for the neural correlates, instrumental avoidance learning engaged the ventromedial prefrontal cortex, amygdala, and striatum. Multivariate decoding revealed a dynamic shift from threat-like to safety-like neural representations for CS+A, emerging after only 2 successful avoidance trials. This avoidance-related neural shift predicted reduced neural recruitment during subsequent extinction learning. During memory recall, participants were charged a monetary cost for avoidance responses but still showed reduced threat expression in response to CS+A, supporting consolidation of safety representations. All key findings were replicated in the independent cohort.
Conclusions:
Our findings show that controllable avoidance can promote adaptive regulation of threat and support long-term safety learning, with implications for anxiety and trauma-related disorders.
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