The cortical amygdala mediates individual recognition in mice

Mice are territorial animals whose spatial navigation ability relies on integrating multiple stimuli from various sensory modalities. Among all these types of information, the pattern of major urinary proteins contained in the urine landmarks provide the identity of the conspecific owner of each territory, constituting the “who” component of episodic memory. We identified a neuroanatomical pathway responsible for integrating individual recognition information into the complex socio-spatial memories stored within the hippocampus. Within this pathway, the posteromedial cortical amygdaloid nucleus serves as the primary relay for vomeronasal information to the hippocampus. We recorded single unit extracellular activity in this nucleus in a head-fixed paradigm in which the female mice were exposed to distinct male-derived stimuli. We subjected the female mice to a range of stimuli, including urine from two different males, a synthetic mixture of these males’ urines, urine from one male countermarked over the others, and the own urine of the female being studied. To analyze our large-scale dataset, we utilized tensor decomposition techniques for neural activity analysis, alongside CEBRA low-dimensional embeddings and decoding accuracy methods. Tensor decomposition revealed that the cortical amygdala comprises neurons that respond to a broad range of stimuli and neurons that specifically activate in response to a particular stimulus, indicating the coexistence of a generalizing and adaptive mechanism alongside another dedicated to precise and unambiguous recognition. Furthermore, CEBRA embeddings indicated that this nucleus exhibits distinct global activity patterns specific to each stimulus.Funded by the Ministry of Science, Innovation and Universities, PID2022-141733NB-I00/AEI/10.13039/501100011033/ FEDER, UE.