Dissociation of spatial and contextual memory encoding under fear and pain in mice

Negative emotional states strongly modulate memory formation, yet the relative contributions of spatial and contextual encoding under fear and pain remain insufficiently understood. In this study, we developed a modular three-chamber Y-maze paradigm that enables independent manipulation of spatial and contextual cues. Using this paradigm, we systematically compared memory encoding induced by foot-shock fear and formalin-evoked pain in mice. Behavioral analyses revealed that foot-shock supported the formation of composite aversive memories integrating both spatial and contextual features, such that animals avoided the shock-paired location even when contextual cues were removed. In contrast, formalin-induced pain memory was primarily context-dependent, with mice failing to discriminate spatial positions once contextual information was absent. Lesions of the dorsal hippocampus (dHPC) selectively abolished spatial but not contextual avoidance, confirming its critical role in spatial memory encoding. Furthermore, when spatial and contextual cues were placed in conflict, avoidance was preferentially guided by contextual features. These findings demonstrate that fear and pain bias memory encoding toward distinct information domains, with spatial memory critically dependent on the dHPC. The present paradigm provides a powerful tool for dissociating memory components under aversive conditions and offers a methodological framework for investigating maladaptive memory processes in chronic pain and post-traumatic stress disorder.