Memory consolidation requires the encoding of neocortical memory traces, which is thought to occur during hippocampal oscillations called sharp-wave ripples (SWR). Evidence suggests that the hippocampus communicates memory-related neural patterns across distributed cortical circuits via its major output pathways. Here, we sought to understand how this information is processed in the retrosplenial cortex (RSC), a primary target circuit. Using patch-clamp recordings from mice during quiet wakefulness, we found that SWR-aligned synaptic modulation is widespread but weak, and that spiking responses are sparse. However, using cell type and projection-specific two-photon calcium imaging and optogenetics, we show that, starting 1-2 seconds before SWR, superficial inhibition in RSC is reduced, along with thalamocortical input. We propose that pyramidal dendrites experience a period of decreased local inhibition and subcortical interference in a seconds-long time window preceding hippocampal SWR. This may aid communication of weak and sparse SWR-aligned excitation between the hippocampus and neocortex, and promote the selective strengthening of memory-related connections.