Shared and unique properties of place cells in anterior cingulate cortex and hippocampus

Abstract

Hippocampal sharp-wave ripples (SWRs) and the associated replay of neuronal sequences are well-established as the primary physiological substrates for memory consolidation. While the local transformations they induce within the hippocampus are well-characterized, their impact on the downstream cortical representations remains unknown. Here, we identify a distinct functional class of neurons in the anterior cingulate cortex "spatial context cells" that emerge through the multi-day integration of discrete hippocampal inputs. Using closed-loop disruption of SWRs and longitudinal calcium imaging, we demonstrate that formation of this global spatial framework depends on SWRs during offline periods. Whereas standard cortical place maps remain intact following SWR disruption, the emergence of spatial context cells is selectively abolished. These cells preferentially express c-Fos, identifying them as constituents of the cortical memory engram, and exhibit broad receptive fields that develop through an experience-dependent process of field convergence. Collectively, these findings establish SWR-mediated replay as a computational bridge transforming high-resolution, fragmented hippocampal spatial codes into generalized, stable cortical schemas. This work reveals a bifurcated consolidation process, identifying SWR-dependent synaptic remodeling as a fundamental mechanism for the ontogeny of remote memory.