Electrophysiological Evidence for Alternative Motor Networks in REM Sleep Behavior Disorder

Abstract

Patients with Parkinson's disease (PD) and REM sleep behavior disorder (RBD) show mostly unimpaired motor behavior during REM sleep, which contrasts strongly to coexistent nocturnal bradykinesia. The reason for this sudden amelioration of motor control in REM sleep is unknown, however. We set out to determine whether movements during REM sleep are processed by different motor networks than movements in the waking state. We recorded local field potentials in the subthalamic nucleus (STN) and scalp EEG (modified 10/20 montage) during sleep in humans with PD and RBD. Time-locked event-related ␤ band oscillations were calculated during movements in REM sleep compared with movements in the waking state and during NREM sleep. Spectral analysis of STN local field potentials revealed elevated ␤ power during REM sleep compared with NREM sleep and ␤ power in REM sleep reached levels similar as in the waking state. Event-related analysis showed time-locked ␤ desynchronization during WAKE movements. In contrast, we found significantly elevated ␤ activity before and during movements in REM sleep and NREM sleep. Corticosubthalamic coherence was reduced during REM and NREM movements. We conclude that sleep-related movements are not processed by the same corticobasal ganglia network as movements in the waking state. Therefore, the well-known seemingly normal motor performance during RBD in PD patients might be generated by activating alternative motor networks for movement initiation. These findings support the hypothesis that pathological movement-inhibiting basal ganglia networks in PD patients are bypassed during sleep.

Automatic Sleep Stage Classification Based on Subthalamic Local Field Potentials

“…It was first reported by Urrestarazu et al [13] (2009) that beta oscillations in the STN of PD patients decreased in non-REM sleep and recovered in REM sleep. The modulation of beta oscillation during movements in REM sleep was shown to be different with that during wakefulness [35], [42]. It was also suggested by Thompson et al [14] (2017) that all frequency bands were significantly different between sleep stages.…”

A video polysomnographic study of spontaneous smiling during sleep in newborns

“…This study also showed that half of patients with REM sleep behaviour disorder (RBD) smiled, although that only some controls did. Indeed, recent studies have suggested that during RBD, unlike what happens when awake, muscle activation is driven by the motor cortex and bypasses the basal ganglia (Arnulf, 2012; Hackius, Werth, Surucu, Baumann, & Imbach, 2016; Mayer, Bitterlich, Kuwert, Ritt, & Stefan, 2015).…”

Smiling asleep: A study of happy emotional expressions during adult sleep

“…This result supports previous works suggesting that the motor signature of RBD is the same across disorders (Oudiette et al., ), and that movements and facial expressions are produced by different networks when asleep to when awake (Arnulf, ). Several lines of evidence (provided by movement analysis, functional imaging and deep brain recordings) suggest that during RBD, the activation of muscles is driven by the motor cortex and bypasses the basal ganglia (De Cock et al., ; Hackius, Werth, Surucu, Baumann, & Imbach, ; Mayer, Bitterlich, Kuwert, Ritt, & Stefan, ).…”