Spectral Dynamics Prior to Motor Events Differ Between NREM Sleep Parasomnias and Healthy Sleepers

Anna Castelnovo; Greta Mainieri; Giuseppe Loddo; Spyros Balafas; Chiara Brombin; Giulia Balella; Angelica Montini; Clelia Di Serio; Mauro Manconi; Federica Provini

doi:10.1093/sleep/zsae252

Spectral Dynamics Prior to Motor Events Differ Between NREM Sleep Parasomnias and Healthy Sleepers

Sleep. 2024 Oct 25:zsae252. doi: 10.1093/sleep/zsae252. Online ahead of print.

Authors

Anna Castelnovo^{1

2

3}, Greta Mainieri^{4

5}, Giuseppe Loddo⁶, Spyros Balafas^{7

8}, Chiara Brombin⁷, Giulia Balella⁴, Angelica Montini⁴, Clelia Di Serio^{2

7}, Mauro Manconi^{1

2

9}, Federica Provini^{4

5}

Affiliations

¹ Sleep Medicine Unit, Neurocenter of Italian Switzerland, Ospedale Civico, Lugano, Ente Ospedaliero Cantonale (EOC), Switzerland.
² Faculty of Biomedical Sciences, University of Italian Switzerland, Lugano, Switzerland.
³ University Hospital of Psychiatry, University of Bern, Bern, Switzerland.
⁴ Department of Biomedical and NeuroMotor Sciences, University of Bologna, Bologna, Italy.
⁵ IRCCS Istituto delle Scienze Neurologiche di Bologna, Bologna, Italia.
⁶ Department of Primary Care, Azienda AUSL di Bologna, Bologna, Italy.
⁷ University Center for Statistics in the Biomedical Sciences, Vita-Salute San Raffaele University, Milan, Italy.
⁸ Groningen Research Institute of Pharmacy, Unit of Pharmacotherapy, Epidemiology and Economics, University of Groningen, Groningen, The Netherlands.
⁹ Department of Neurology, University Hospital, Inselspital, Bern, Switzerland.

PMID: 39453616
DOI: 10.1093/sleep/zsae252

Abstract

Study objectives: The umbrella term "Disorders of Arousal" (DoA), encompassing sleepwalking, confusional arousals, and sleep terrors, refers to parasomnias manifesting during non-rapid eye movement (NREM) sleep, commonly thought to arise from an aberrant arousal process. While previous studies have detailed EEG changes linked to DoA episodes, it remains uncertain how these alterations differ from a physiological arousal process. This study directly compared brain activity between DoA episodes and arousals associated with physiological movements (motor arousal) in individuals with DoA and healthy sleepers.

Methods: Fifty-three adult patients with DoA (25 males, 32.2±15.5years) and 33 control subjects (14 males, 31.4±11.4years) underwent one or more home-EEG recordings. A semiparametric regression model was employed to elucidate the complex relationship between EEG activity across channels, within and across different groups, including motor arousals in DoA (n=169), parasomnia episodes in DoA (n=361), and motor arousals in healthy sleepers (n=137).

Results: Parasomnia episodes and motor arousals in both groups were preceded by a diffuse increase in slow-wave activity (SWA) and beta power, and a widespread decrease in sigma power. However, motor arousals in DoA displayed lower beta and central sigma than in healthy sleepers. Within DoA patients, episodes were preceded by lower beta, frontal sigma, and higher SWA than motor arousals.

Conclusions: Our findings suggest that the arousal process is altered in DOA patients, and that specific EEG patterns are required for DOA episodes to emerge. These insights will help guide future research into the underlying circuits and objective markers of DOA.

Keywords: Electroencephalography; NREM Parasomnias; Sleep Spindles; Somnambulism; Topography.

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