Heartbeat-related activity in the anterior thalamus differs between phasic and tonic REM sleep

Rapid eye movement (REM) sleep is a fundamental sleep state associated with diverse functions from elemental physiological processes to higher order neurocognitive functions. A growing body of research indicates that REM sleep with eye movements (phasic REM) differs from REM periods without ocular activity (tonic) in terms of spontaneous and evoked neural responses. Studies using auditory stimulation consistently observed enhanced evoked responses in tonic versus phasic REM, indicating that external processing is largely diminished when the eyes move during REM sleep. Whereas exteroceptive processing during sleep is widely studied, investigations on interoception (the processing of bodily signals) during sleep are scarce, and limited to scalp electroencephalographic recordings. Here we studied interoceptive processing in a group of epileptic patients (N = 11) by measuring their heartbeat-related neural activity in the anterior nuclei of the thalamus (ANT) during phasic and tonic REM sleep and resting wakefulness. Evoked potentials and beta-low gamma spectral power locked to the heartbeat were significantly different in phasic REM compared with tonic REM and wakefulness. Heartbeat-related neural signals exhibited pronounced inter-trial phase synchronization at lower (7-20 Hz) oscillatory activity in all vigilance states, but reduced gamma synchronization at later time points in phasic REM only. Tonic REM and wakefulness did not show significant differences in heartbeat-related activity in the ANT. Our findings indicate that heartbeat-related neural activity is detectable at the level of the ANT, showing distinct signatures of interoceptive processing in phasic REM compared with tonic REM and wakefulness. KEY POINTS: We studied interoceptive processing in the anterior the thalamus (ANT). The ANT tracks cardiac signals during wakefulness and rapid eye movement (REM) sleep. Phasic REM shows distinct patterns of heartbeat-related oscillatory activity. Interoceptive processing might be attenuated during REM periods with eye movements.