Rapid eye movement sleep (REM) is often considered as a homogeneous state of sleep, defined by a striking resemblance of its electroencephalogram (EEG) to the one observed in wakefulness. The occurrence of transient events in REM, such as limb twitches or facial and rapid eye movements, supports the view of a paradoxical state of sleep. Here, we investigated the local activity of the primary somatosensory or barrel cortex (S1) in naturally sleeping head-fixed male mice during REM. Through local field potential (LFP) recordings, we uncovered local appearances of spindle waves in the barrel cortex during REM concomitant with strong delta power, challenging the view of a wakefulness-like activity in REM. We further performed extra- and intracellular recordings of thalamic cells in head-fixed mice. Our data show high frequency thalamic bursts of spikes and subthreshold spindle oscillations in neurons of the ventral posterior medial nucleus which further confirmed the thalamic origin of local cortical spindles in S1 in REM. Cortical spindle oscillations were suppressed, while thalamus spike firing increased, associated with rapid mouse whisker movements and S1 cortical activity transitioned to an activated state. During REM, sensory thalamus and barrel cortex therefore alternate between high (wake-like) and low (non-REM sleep-like) activation states, potentially providing a neuronal substrate for mnemonic processes occurring during this paradoxical sleep stage.