Journal of Neuroscience 16 April 2021, JN-RM-1899-20; DOI: https://doi.org/10.1523/JNEUROSCI.1899-20.2021

Péter Simor1,2,3, Orsolya Szalárdy2,4, Ferenc Gombos5, Péter Przemyslaw Ujma2,6, Zsófia Jordán6, László Halász6, Loránd Erőss6, Dániel Fabó6, and Róbert Bódizs2,4

1Institute of Psychology, ELTE, Eötvös Loránd University, 1064, Budapest, Hungary

2Institute of Behavioural Sciences, Semmelweis University, 1089, Budapest, Hungary

3UR2NF, Neuropsychology and Functional Neuroimaging Research Unit at CRCN – Center for Research in Cognition and Neurosciences and UNI – ULB Neurosciences Institute, Université Libre de Bruxelles (ULB), 1050, Brussels, Belgium

4Institute of Cognitive Neuroscience and Psychology, Research Centre for Natural Sciences, 1117, Budapest, Hungary

5MTA-PPKE Adolescent Development Research Group, 1088, Budapest, Hungary

6National Institute of Clinical Neurosciences, 1145, Budapest, Hungary

 

ABSTRACT

Rapid eye movement sleep is an elusive neural state that is associated with a variety of functions from physiological regulatory mechanisms to complex cognitive processing. REM periods consist of the alternation of phasic and tonic REM microstates that differ in spontaneous and evoked neural activity. Although previous studies indicate, that cortical and thalamo-cortical activity differs across phasic and tonic microstates, the characterization of neural activity, particularly in subcortical structures that are critical in the initiation and maintenance of REM sleep is still limited in humans. Here, we examined electric activity patterns of the anterior nuclei of the thalamus as well as their functional connectivity with scalp EEG recordings during REM microstates and wakefulness in a group of epilepsy patients (N = 12, 7 females). Anterothalamic local field potentials showed increased high-alpha and beta frequency power in tonic compared to phasic REM, emerging as an intermediate state between phasic REM and wakefulness. Moreover, we observed increased thalamocortical synchronization in phasic compared to tonic REM sleep, especially in the slow and fast frequency ranges. Wake-like activity in tonic REM sleep may index the regulation of arousal and vigilance facilitating environmental alertness. On the other hand, increased thalamocortical synchronization may reflect the intrinsic activity of fronto-limbic networks supporting emotional and memory processes during phasic REM sleep. In sum, our findings highlight that the heterogeneity of phasic and tonic REM sleep is not limited to cortical activity, but is also manifested by anterothalamic local field potentials and thalamocortical synchronization.