Infraslow modulation of theta synchrony in the hippocampus circuit during REM sleep

Abstract

Sleep dynamically reorganizes hippocampal activity, but how this reconfiguration supports large-scale coordination across the hippocampal circuit remains unclear. We performed simultaneous recordings from dorsal (CA1d) and ventral (CA1v) hippocampus, retrosplenial cortex (RSC), prefrontal cortex (PFC), and dorsal thalamus in rats across brain states. Theta oscillations dominated hippocampal activity during active behaviour and REM sleep, while delta oscillations prevailed during nREM and quiet waking. Phase synchrony between CA1d and CA1v varied across states, peaking during REM sleep and exhibiting infraslow fluctuations (0.02 Hz) unique to this stage. These slow modulations persisted after controlling for theta power, suggesting a genuine modulation of interregional synchrony. Transitions into REM were marked by rising CA1d-CA1v synchrony and widespread neuronal activation, with thalamic activity most strongly predicting coupling dynamics. During REM sleep, neuronal firing across hippocampal-cortical-thalamic circuits was phase-locked to the infraslow theta coupling cycle, indicating gain modulation at the network level. Such entrainment was strongest and most consistent in REM and aligned near a common phase, revealing temporally structured communication at multiple scales. Our findings identify an infraslow modulation of hippocampal theta coherence that temporally organizes neuronal excitability across brain regions during REM sleep, offering a systems-level mechanism for regulating inter-regional communication during sleep.