Spatial memory performance is associated with region-specific coordination of hippocampo-cortical sleep oscillations

Sleep plays a critical role in memory consolidation, yet how coordination among sleep oscillations across hippocampo-cortical circuits relates to behavioral performance remains incompletely understood. Here, we examined how cross-regional coordination of cardinal sleep oscillations during non-rapid eye movement (nREM) sleep relates to spatial memory performance. Adult rats were trained in an object-place recognition task and allowed to sleep while local field potentials were recorded simultaneously from dorsal and ventral hippocampus (CA1d and CA1v) and retrosplenial, prefrontal, and lateral entorhinal cortices. We first confirm that nREM sleep duration, but not REM sleep, is positively associated with spatial memory performance. We then characterized the temporal relationships between hippocampal sharp-wave ripples and cortical spindles and slow oscillations, revealing region- and oscillation-specific coordination patterns that depend on the dorso-ventral origin of hippocampal ripple events. Finally, by comparing task-related changes in ripple-triggered cortical activity between low- and high-performing sessions, we identify selective, performance-dependent modulation of hippocampo-cortical coupling during task-related sleep. Spatial memory performance was consistently associated with enhanced ripple-spindle and ripple-slow oscillation coupling driven by dorsal hippocampal ripples, particularly in interactions with entorhinal and prefrontal cortices, whereas ventral hippocampal interactions failed to show behavioural association. Together, these results reveal that spatial memory performance is linked to region- and timing-specific coordination of sleep oscillations across hippocampo-cortical networks during nREM sleep, highlighting a functional differentiation of dorsal and ventral hippocampal contributions to sleep-dependent memory consolidation.