Rapid eye movement (REM, also called paradoxical) sleep correlates with enhanced cellular activity in region-specific thalamo-cortical circuits and subcortical structures including the hippocampus, midbrain or hypothalamus. This REM sleep specific neuronal activity is hypothesized to promote structural plasticity and provide a window for the consolidation of contextual and emotional memories previously acquired during wakefulness, yet the underlying mechanism remains unclear.Amongst the cortical structures, the activity of neurons located in the retrosplenial cortex (RSC) is increased during REM sleep. Here we characterized the activity of RSC microcircuit across the sleep wake cycle using simultaneous 2-photon calcium imaging and electrophysiological recordings in spontaneously head-restrained sleeping mice. We observed a REM sleep-specific pyramidal somato-dendritic decoupling with a reduction of pyramidal cell somatic activity concomitant to an increase in pyramidal dendritic activity. This decoupling is associated with the activation of the interneurons expressing either parvalbumin (PV), somatostatin (SST) or vasoactive intestinal peptide (VIP). The absence of a VIP-SST mediated dendritic disinhibition was confirmed by anatomical retrograde tracing. REM sleep-specific optogenetic disinhibition of pyramidal somatic activity led to an enhanced contextual memory consolidation, whereas optogenetic silencing of SST REM sleep-specific activity did not impact contextual memory consolidation. Collectively, these results suggest a region-specific fine-tuning of excitatory/inhibitory balance in RSC during REM sleep that ultimately contribute to information integration, memory consolidation and behavioural optimization.