REM sleep remains paradoxical: sub-states determined by thalamo-cortical and cortico-cortical functional connectivity

During paradoxical sleep (PS, aka REM sleep) the cerebral cortex displays rapid electroencephalographic activity similar to that of wakefulness, whereas in the posterior associative thalamus, rapid activity is interrupted by frequent periods of slow-wave (delta) oscillations at 2-3 Hz, thereby dissociating the intrinsic frequency in thalamus and cortex. Here we studied the functional consequences of such a dissociation using intrathalamic and intracortical recordings in 21 epileptic patients, applying coherence analysis to examine changes in functional connectivity between the posterior thalamus (mainly medial pulvinar) and six cortical functional networks, and also between each cortical network with respect to the others. Periods of slow-wave thalamic activity ('delta PS') were more prevalent than phases of 'rapid PS,' and the delta/rapid thalamic alternance did not overlap with the classical tonic/phasic dichotomy based on rapid eye movements. Thalamo-cortical and cortico-cortical functional connectivity significantly decreased during delta PS, relative to both rapid PS periods and to wakefulness. The fact that delta thalamic activity and low thalamo-cortical binding coincided with a suppression of cortico-cortical connectivity supports a crucial role for the posterior associative thalamus, and particularly the medial pulvinar, in ensuring trans-thalamic communication between distant cortical areas. Disruption of such a trans-thalamic communication during delta PS compromises the functional binding between cortical areas, and consequently might contribute to the alteration of perceptual experiences commonly reported during dreams. KEY POINTS: During paradoxical, or REM, sleep (PS), rapid thalamic activity is interrupted by frequent periods of slow delta waves at 2-3 Hz. During these periods of thalamic delta activity there was a drastic drop of functional connectivity between associative thalamus and cortex, and also among different cortical networks. The delta/rapid alternance did not overlap with the classically defined 'tonic/phasic' periods and therefore suggests a distinct dichotomy of functional states in PS. Recurrent decrease in thalamo-cortical and cortico-cortical functional connectivity during PS may compromise the spatio-temporal binding between cortical areas, which in turn could hinder the formation of coherent mental content during dreams.