Enhanced frontoparietal synchronized activation during the wake-sleep transition in patients with primary insomnia

Abstract

Introduction: Cognitive and brain hyperactivation have been associated with trouble falling asleep and sleep misperception in patients with primary insomnia (PI). Activation and synchronization/temporal coupling in frontal and frontoparietal regions involved in executive control and endogenous attention might be implicated in these symptoms.

Methods: Standard polysomnography (PSG) and electroencephalogram (EEG) were recorded in 10 unmedicated young patients (age 19-34 yr) with PI with no other sleep/medical condition, and in 10 matched control subjects. Absolute power, temporal coupling, and topographic source distribution (variable resolution electromagnetic tomography or VARETA) were obtained for all time spent in waking, Stage 1 and Stage 2 of the wake-sleep transition period (WSTP), and the first 3 consecutive min of N3. Subjective sleep quality and continuity were evaluated.

Results: In comparison with control subjects, patients with PI exhibited significantly higher frontal beta power and current density, and beta and gamma frontoparietal temporal coupling during waking and Stage 1.

Conclusion: These findings suggest that frontal deactivation and disengagement of brain regions involved in executive control, attention, and self-awareness are impaired in patients with PI. The persistence of this activated and coherent network during the wake-sleep transition period (WSTP) may contribute to a better understanding of underlying mechanisms involved in difficulty in falling asleep, in sleep misperception, and in the lighter, poorer, and nonrefreshing sleep experienced by some patients with PI.

Keywords: EEG coherence; EEG temporal coupling; EEG topography; Primary insomnia; VARETA; spectral EEG.

Figures

Figure 1

Frontal Beta power from four electrode locations (F3, F7, Fz, F1) as a function of group and stage. Mean and standard error of beta absolute power, log transformed, in the primary insomnia (PI) and control groups (CG) during waking (W), stage 1 (N1), stage 2 (N2) and the first 3 min of stage 3+4 (SN3). Electrodes showing post-hoc significant differences for group-by-stage-by-derivation interaction are illustrated. Horizontal brackets indicate significant differences between groups.

Figure 2

Frontoparietal temporal coupling as a function of group and stage. Mean and standard error of beta and gamma cross-correlations, transformed to Fisher Z scores, in the primary insomnia (PI) and control groups (CG) for significant group main effects (A), and for electrodes showing post-hoc significant differences for group-by-stage-by-derivation interactions (B). Horizontal brackets indicate significant differences between groups.

Figure 3

Statistical map showing the significant distributed current source density in 29 Hz for the contrast between primary insomnia and control groups during waking. The scale represents significance level of current density differences between groups. Red represents a significantly higher current density in the primary insomnia group compared to the control group (P

Figure 4

Statistical map showing the significant distributed current source density in 29 Hz for the contrast between primary insomnia and control groups during Stage 1. The scale represents significance level of current density differences between groups. Red represents a significantly higher current density in the primary insomnia group compared to the control group (P