Evidence of subthalamic PGO-like waves during REM sleep in humans: a deep brain polysomnographic study

Abstract

Study objectives: The aim of this study was to examine whether the subthalamic nucleus (STN) plays a role in the transmission of PGO-like waves during REM sleep in humans.

Design: Simultaneous recordings from deep brain electrodes to record local field potentials (LFPs), and standard polysomnography to ascertain sleep/wake states.

Setting: Main Hospital, department of clinical neurophysiology sleep laboratory.

Participants: 12 individuals with Parkinson's disease, with electrodes implanted in the STN; and, as a control for localization purposes, 4 cluster headache patients with electrodes implanted in the posterior hypothalamus.

Interventions: All subjects underwent functional neurosurgery for implantation of deep brain stimulation electrodes.

Results: Sharp, polarity-reversed LFPs were recorded within the STN during REM sleep in humans. These subthalamic PGO-like waves (2-3 Hz, 80-200 pV, and 300-500 msec) appeared during REM epochs as singlets or in clusters of 3-13 waves. During the pre-REM period, subthalamic PGO-like waves were temporally related to drops in the submental electromyogram and/or onset of muscular atonia. Clusters of PGO-like waves occurred typically before and during the bursts of rapid eye movements and were associated with an enhancement in fast (15-35 Hz) subthalamic oscillatory activity.

Conclusion: Subthalamic PGO-like waves can be recorded during pre-REM and REM sleep in humans. Our data suggest that the STN may play an active role in an ascending activating network implicated in the transmission of PGO waves during REM sleep in humans.

Figures

Figure 1

REM sleep related subthalamic activity. (A) A 30-s epoch of simultaneous PSG and bipolar subthalamic recording showing the pattern of PGO-like waves. A 0.5–100 Hz band-pass filter reveals the vascular pulse component in the right 2-3 derivation. (B) Axial MRI view showing DBS electrodes at the level of contact 0. (C) Enlarged section of the pattern of subthalamic PGO-like waves recorded during REM sleep.

Figure 2

Sequences of pre-REM and REM sleep. (A) A 90-s REM sleep period showing the clusters of subthalamic PGO-like waves associated with REMs. (B) Fast transition to REM sleep from a pre-REM sleep period where subthalamic PGO-like waves appeared as singlets linked to drops in the EMG and to onset of definite muscular atonia. (C) Transition to REM sleep from a pre-REM sleep period, where a cluster of subthalamic PGO-like waves appeared associated with short-lasting total EMG atonia and instability of the eyes recorded in the EOG. All subthalamic traces band-pass filtered at 1–100 Hz.

Figure 3

Subthalamic PGO-like waves, muscular atonia, and REMs. (A) A 15-s enlarged section of a pre-REM–REM sleep transition showing the close association of subthalamic PGO-like waves with drops in the EMG and the onset of muscular atonia during pre-REM sleep. Subthalamic traces band-pass filtered at 1–100 Hz. (B) Histogram showing the incidence of PGO-like waves 500 ms before and after REMs. The solid line represents the averaged amplitude deflection in the EOG (μV), and the dotted lines represent ± SD. Bars represent the incidence (num. = number) of PGO-like waves.

Figure 4

Subthalamic PGO-like clusters and fast (15–35Hz) oscillations. (A) A 15-s REM epoch of simultaneous PSG and STN traces from the period marked in light blue of the hypnogram (top). Subthalamic traces are displayed as raw (1–100 Hz), low-β (15–25 Hz; red) and high-β (25–35 Hz; pink) filtered derivations. Sawtooth waves in C3-A2 are temporally linked to subthalamic PGO-like waves. (B) Display of the fast Fourier transform (FFT) of 1-2R STN traces for different relative powers (μV2) for each second of the epoch: blue = δ (0.5–4 Hz), green = θ (4–8 Hz), yellow = α (8–12 Hz), orange = σ (12–15 Hz), red = low-β (15–25 Hz), pink = high-β (25–35 Hz). (C) Enlarged sections (1 s) of raw subthalamic traces revealing reduced β (15–35 Hz) activity before the clusters (C1), and polarity-reversed β activity (C2) with a higher amplitude after the cluster (C3). (D) Histogram showing the significant increase in beta power after the clusters of subthalamic PGO-like waves. (E) Histogram showing the linear increase in β power during the clusters (see Table 1).