The geometry of hippocampal CA2 representations enables abstract coding of social familiarity and identity

Abstract

Social recognition memory encompasses two distinct processes: familiarity – the ability to rapidly distinguish a novel from familiar individual – and recollection, the recall of detailed episodic memories of prior encounters with familiar individuals (1). Although it is clear that the hippocampus is important for different forms of episodic memory (2), including spatial memory (3) and social recognition memory (4–7), whether and how neural activity in this single brain region may be able to encode both social familiarity and social recollection remains unclear (8–13). We addressed such questions using microendoscopic calcium imaging from pyramidal neurons in the dorsal CA2 region of the hippocampus (dCA2), an area crucial for social recognition memory (6, 14, 15) that encodes social and spatial information (16–18), as mice explored novel and familiar conspecifics. Here we demonstrate that the geometry of dCA2 representations in neural activity space enables social familiarity, social identity, and spatial information to be readily disentangled. Importantly, highly familiar littermates were encoded in higher-dimensional neural representations compared to novel individuals. As a result of this coding strategy, dCA2 neural activity was able to both provide an abstract, low-dimensional representation of social familiarity that could readily distinguish a novel from familiar individual and encode detailed episodic memories associated with familiar individuals.