SPATIAL MEMORY PROCESSING UNDER AVERSIVE CONDITIONS IN THE HIPPOCAMPUS-AMYGDALA NETWORK

The formation of episodic memory relies on the creation of new memory traces in the dorsal hippocampus(dHPC) and their subsequent consolidation through the reactivation of neuronal activity during sleep. This process is influenced by emotions, notably via the basolateral amygdala (BLA), a key brain structure for processing emotional valence, both positive and negative. Interactions between the dorsal hippocampus and the BLA are implicated in the attribution of emotional valence to spatial memories, via the reactivation of dorsal hippocampus-BLA place-threat representations during sleep. Although these two regions lack direct anatomical connectivity, the BLA is reciprocally connected with the ventral-hippocampus(vHPC), which plays a key role in emotional processing and may serve as a hub for integrating spatial and emotional information. Here, we investigated how spatial learning under threat influences sleep-dependent consolidation within the dHPC–vHPC–BLA network. We performed large-scale simultaneous electrophysiological recordings from these three brain regions in freely behaving rats. Animals were trained on a task requiring daily learning of three reward locations. Learning sessions occurred under either a safe or a threatening context induced by unpredictable eyelid shocks. Learning in a threatening context altered behavioral dynamics, as shown by reduced locomotion speed and increased travel distance, whereas successful acquisition of reward locations was preserved regardless of context. We examined coordination at the local field potential and single-cell levels during sleep before and after learning sessions in safe or threatening contexts to determine how the emotional valence modulates sleep-dependent consolidation across the dHPC-vHPC-BLA network.