Transformations of the spatial activity manifold convey aversive information in CA3

Abstract

Hippocampal circuits form cognitive maps representing spatial position and integrating contextual information, including affective cues, within episodic memory representations. We investigated how spatial and affective information combine in the population activity of CA3 axons by imaging intermediate-to-dorsal and dorsal-to-dorsal projections in mice navigating a linear track before, during, and after exposure to an aversive air puff stimulus. Our analyses reveal that both axonal populations maintain a robust, time-invariant spatial coding manifold across recordings, independent of affective context. Alterations to this common manifold encode the presence of the aversive stimulus without disrupting the spatial representation. Both axonal pathways encoded affective information with similar efficacy. This population-level encoding was distributed similarly across place and non-place cells. Our findings demonstrate that hippocampal CA3 axons integrate spatial and affective information within a common representational geometry while preserving the ability to extract each information type separately.