Generative emergence of non-local representations in the hippocampus

The role of internally-generated network dynamics in rapid temporal sequence coding, updating, and parallel recalling of alternate spatial and mental navigation contexts has remained unclear. Here, we revealed rapid emergence of temporally-compressed hippocampal theta sequences in adult male rats within 1-2 laps of a novel detour via re-purposing of pre-existing correlated neuronal sequence motifs expressed during pre-detour sleep. Detour experience-induced neuronal remapping and plasticity were consolidated and reconfigured hippocampal network during post-detour sleep, which predicted future representational drift expressed during the following post-detour reversal-track runs. Pre-detour or reversal-track representations flickered with detour representation across distinct phases of theta oscillation, revealing segregation of non-local internally-generated/recalled and local experience-related hippocampal representations by theta phase. These findings demonstrate that internal generative network dynamics across brain states support rapid theta-scale sequential coding, within-day representational updating, and flickering parallel representations - collectively forming non-local representations - during navigation.