Abstract

Memory consolidation is thought to rely on hippocampo-cortical dialogue orchestrated by three cardinal sleep oscillations: cortical slow oscillations, thalamic spindles, and hippocampal sharp-wave ripples. However, how hippocampal outputs are routed to specific cortical targets and dynamically regulated across brain states remains unclear. Here, we performed simultaneous multisite recordings from the dorsal and ventral hippocampus, and frontal and retrosplenial cortex in rats alternating between wakefulness and sleep. Frontal slow oscillations operated as a global temporal scaffold, resetting thalamic circuits and initiating spindle volleys in both anterior and posterior cortex, while retrosplenial slow oscillations more effectively recruited hippocampal ripples. Ripple-spindle reflected direct anatomical connectivity, as dorsal ripples preferentially enhanced retrosplenial spindles, while ventral ripples engaged mainly frontal spindling. When ripples synchronized across dorsal and ventral hippocampus, associated slow oscillations and spindles were attenuated, hippocampal spiking decreased locally and redistributed to the opposite pole, and cortical neuronal responses were suppressed in their corresponding anatomical pathways. These effects indicate that dorso-ventral ripple synchrony gates, rather than amplifies, hippocampo-cortical communication. This gating effect was brain-state dependent, as dorsal-driven reactivation persisted across vigilance states, whereas ventral pathways were more prominent during sleep. Together, these results outline a hierarchical architecture in which slow oscillations provide a global clock, spindles implement anatomically specific reactivation channels, and ripple synchrony dynamically gates hippocampal output, likely shaping the precision and specificity of memory consolidation within a highly variable neural substrate.