A theory-guided model maps four recurrent modes of fear-goal arbitration across learning and relapse in rats

Abstract

When defensive behavior declines, has the individual recovered? Addressing this translational question requires testing whether exploration and goal pursuit also return, and whether those gains survive time and context. We adapted rat fear-conditioning, extinction, delay, and contextual relapse paradigms to this problem. Male rats first explored the chambers under safer conditions and learned to press for food; aversive conditioning then reorganized the repertoire around danger. Extending tri-reference-point (TRP) theory from risky choice, we framed the repertoire around danger, the current condition, and goals. Across 47,004 five-second windows from 29 animals and 213 subject-sessions, we aligned freezing, 22- and 50-kHz calls, and lever presses. Subject-grouped, discrete-aware validation selected a diagonal Gaussian hidden Markov model at theory-guided K=4, decoding recurrent Fear/Danger, Quiescent, Exploratory, and Goal-directed modes. K=8 predicted held-out data better and subdivided these functional regions. Conditioning shifted occupancy from Exploratory toward Fear/Danger. By the final decile of initial extinction, Fear/Danger had fallen to 2.7%, yet Quiescent occupied 95.8%, with Exploratory at 0.6% and Goal-directed at 1.0%: fear reduction without broader functional restoration. Across related cohorts, later tests revealed exploratory-rich and renewed-defense trajectories. Goal-to-Fear transitions were depleted under two null models, and Fear/Danger occupancy was associated with fecal boli after session adjustment (bias-reduced p=0.036). Count-tailored models preserved temporal dependence but regrouped behavior, showing that state identity depends partly on representation. Together, multimodal measurement, TRP-derived landmarks, and temporal modeling make functional recovery testable as the history-dependent restoration of an individual's behavioral repertoire, not merely the suppression of defense.