Proceedings of the Annual Meeting of the Cognitive Science Society

Fear extinction involves forming inhibitory safety memories that compete with the original fear traces. We recorded intracranial microelectrode data from 24 epilepsy patients to investigate how neuronal activity supports these representational shifts. During acquisition, amygdala neurons showed increased firing rates (475–525 ms) for aversive outcomes (n = 19). Oscillatory analyses (n = 24) revealed that the entorhinal cortex exhibited high-gamma enhancement (52–70 Hz and 74–88 Hz; both 0.80–1.10 s) following aversive outcome delivery during acquisition, while extinction was marked by low-frequency suppression (2–10 Hz, 1.15–1.50 s) following reinforcement. When combining acquisition and extinction phases, the hippocampus showed early high-gamma responses (76–98 Hz, 0.25–0.40 s) to aversive outcomes. Critically, hippocampal gamma power (38–62 Hz, 0.30–0.40 s) during extinction distinguished stimuli retaining threat value (CS++) from those undergoing extinction (CS+-), with the latter becoming indistinguishable from always-safe cues (CS--). Our results provide a cellular foundation for how the human mind adjudicates between competing memories and updates mental models through sensory evidence and threat evaluation.