High-density EEG power topography and connectivity during confusional arousal

• Published in: Cortex Vol. 155; pp. 62 - 74
• Main Authors: Castelnovo, Anna, Amacker, Julian, Maiolo, Massimo, Amato, Ninfa, Pereno, Matteo, Riccardi, Silvia, Danani, Andrea, Ulzega, Simone, Manconi, Mauro
• Format: Journal Article
• Language: English
• Published: Elsevier Ltd 01.10.2022
• Subjects: Disorders of arousal; Night terror; NREM-sleep parasomnia; Pavor nocturnus; Somnambulism; PSD; PTE; EEG; NREM; sLORETA; BEM; PLMSI; NREM-sleep parasomnia; SPECT; SHE; Night terror; Pavor nocturnus; Somnambulism; FDR; RDI; DOA; vPSG; Disorders of arousal; SWA
• ISSN: 0010-9452; 1973-8102
• DOI: 10.1016/j.cortex.2022.05.021

Confusional arousal is the milder expression of a family of disorders known as Disorders of Arousal (DOA) from non-REM sleep. These disorders are characterized by recurrent abnormal behaviors that occur in a state of reduced awareness for the external environment. Despite frequent amnesia for the nocturnal events, when actively probed, patients are able to report vivid hallucinatory/dream-like mental imagery. Traditional (low-density) scalp and stereo-electroencephalographic (EEG) recordings previously showed a pathological admixture of slow oscillations typical of NREM sleep and wake-like fast-mixed frequencies during these phenomena. However, our knowledge about the specific neural EEG dynamics over the entire brain is limited. We collected 2 consecutive in-laboratory sleep recordings using high-density (hd)-EEG (256 vertex-referenced geodesic system) coupled with standard video-polysomnography (v-PSG) from a 12-year-old drug-naïve and otherwise healthy child with a long-lasting history of sleepwalking. Source power topography and functional connectivity were computed during 20 selected confusional arousal episodes (from −6 to +18 sec after motor onset), and during baseline slow wave sleep preceding each episode (from – 3 to −2 min before onset). We found a widespread increase in slow wave activity (SWA) theta, alpha, beta, gamma power, associated with a parallel decrease in the sigma range during behavioral episodes compared to baseline sleep. Bilateral Broadman area 7 and right Broadman areas 39 and 40 were relatively spared by the massive increase in SWA power. Functional SWA connectivity analysis revealed a drastic increase in the number and complexity of connections from baseline sleep to full-blown episodes, that mainly involved an increased out-flow from bilateral fronto-medial prefrontal cortex and left temporal lobe to other cortical regions. These effects could be appreciated in the 6 sec window preceding behavioral onset. Overall, our results support the idea that DOA are the expression of peculiar brain states, compatible with a partial re-emergence of consciousness.