Tuned geometries of hippocampal representations meet the demands of social memory

Abstract

Social recognition consists of multiple memory processes, including the detection of familiarity - the ability to rapidly distinguish familiar from novel individuals - and recollection - the effortful recall of where a social episode occurred and who was present. At present, the neural mechanisms for these different social memory processes remain unknown. Here, we investigate the population code for novel and familiar individuals in mice using calcium imaging of neural activity in a region crucial for social memory, the dorsal CA2 area of the hippocampus. We report that familiarity changes CA2 representations of social encounters to meet the different demands of social memory. While novel individuals are represented in a low-dimensional geometry that allows for rapid generalization, familiar individuals are represented in a higher-dimensional geometry that supports high-capacity memory storage. The magnitude of the change in dimensionality of CA2 representations for a given individual predicts the performance of that individual in a social recognition memory test, suggesting a direct relationship between the representational geometry and memory-guided behavior. Finally, we show that familiarity is encoded as an abstract variable with neural responses generalizing across different identities and spatial locations. Thus, through the tuning of the geometry of structured neural activity, CA2 is able to meet the complex demands of multiple social memory processes.