Novelty, ecological relevance, and sexual receptivity modulate neuronal interactions between amygdala and hippocampus

Many studies have demonstrated that the basolateral complex of the amygdala (BLA) can facilitate offline consolidation processes in the hippocampus. However, an open question is how online neuronal oscillations in these regions dynamically couple at the moment of encoding to enable an episodic prioritization for important ecologically relevant stimuli. In the current study, local field potentials (LFPs) were recorded in the BLA and hippocampus (ventral CA1) of female rats as they spontaneously explored many novel and repeated plant-based odors and rat urine odors, which convey ecologically relevant information about conspecifics. Rats’ estrous cycle was tracked and used to estimate sexual receptivity. Moments of exploring urine odors, particularly from male donors, were associated with different neural activity in the BLA and hippocampus versus plant-based odors, activity that also depended on the novelty of the odors as well as the rats’ sexual receptivity. Specifically, prominent slow gamma (20-50 Hz) oscillations during odor exploration showed a BLA-to-hippocampus directionality and were associated with odor novelty, odor category (male urine vs. female urine vs. plant-based odors), and better subsequent memory. Spiking-associated (150-200 Hz) activity in the LFPs was also influenced by odor novelty and odor category and was significantly higher in both the BLA and hippocampus on days for which the rats were sexually receptive. Thus, stimulus novelty and ecological relevance combined with the rats’ emotional state to shape the neural correlates of prioritized encoding. The results are discussed in terms of endogenous mechanisms of memory enhancement for important to-be-remembered stimuli. Significance Statement The amygdala and hippocampus play complementary roles in making important information more memorable. A fundamental question is how neuronal activity in these regions becomes coordinated when encountering to-be-remembered information. We recorded neuronal activity in these regions as female rats encountered many new and repeated urine odor samples from other male and female rats. Urine odors convey key information about other rats. Investigating urine odors, particularly from males, led to different neural activity in the amygdala and hippocampus versus plant-based odors, activity that was also associated with the novelty of the odors, the rats’ sexual receptivity, and how well remembered the odors were. Stimulus novelty and biological significance may combine with one’s emotional state to determine the neural correlates of memorability.