Rapid eye movement sleep (REM), also referred to as paradoxical sleep for the striking resemblance of its electroencephalogram (EEG) to the one observed in wakefulness, is characterized by the occurrence of transient events such as limb twitches or facial and rapid eye movements. 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 about half of the 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.Significance Statement Mammalian sleep includes slow wave sleep, or non-rapid eye movement sleep (NREM), and the subsequent REM sleep (REM). At the EEG global level, cortical activity during REM sleep has long been believed to share some similarities with awake cortical activity. The well-defined mouse whisker system offers the unique opportunity to precisely investigate cortical and thalamic dynamics during wakefulness and REM. Combining local field potential (LFP) recordings in primary somatosensory cortex, with single-unit neuronal recordings in its associated thalamic nucleus, we found that during REM, sensory thalamus and barrel cortex 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.