Frontal grey matter microstructure is associated with sleep slow waves characteristics in late midlife

• Published in: Sleep (New York, N.Y.) Vol. 45; no. 11; p. 1
• Main Authors: Chylinski, Daphne, Narbutas, Justinas, Balteau, Evelyne, Collette, Fabienne, Bastin, Christine, Berthomier, Christian, Salmon, Eric, Maquet, Pierre, Carrier, Julie, Phillips, Christophe, Lina, Jean-Marc, Vandewalle, Gilles, Van Egroo, Maxime
• Format: Journal Article Web Resource
• Language: English
• Published: US Oxford University Press 09-11-2022; The American Academy of Sleep Medicine
• Subjects: ageing; Aging; Brain; brain microstructure; Cerebral Cortex; diffusion-weighted imaging; fast switcher slow wave; Female; frontal cortex; Frontal lobes; Gray Matter - diagnostic imaging; Health aspects; Humans; Middle age; Middle Aged; Neural oscillations; neurite density; neurite orientation dispersion; Neurites; Neurosciences & behavior; Neurosciences & comportement; NODDI; Physiological aspects; Sciences sociales & comportementales, psychologie; Sleep; Sleep Across the Lifespan; Slow wave sleep; slow waves; Social & behavioral sciences, psychology; White Matter; Belgium; slow waves; fast switcher slow wave; frontal cortex; neurite density; ageing; brain microstructure; diffusion-weighted imaging; NODDI; neurite orientation dispersion
• ISSN: 0161-8105; 1550-9109; 1550-9109
• DOI: 10.1093/sleep/zsac178

Abstract
Study Objectives
The ability to generate slow waves (SW) during non-rapid eye movement (NREM) sleep decreases as early as the 5th decade of life, predominantly over frontal regions. This decrease may concern prominently SW characterized by a fast switch from hyperpolarized to depolarized, or down-to-up, state. Yet, the relationship between these fast and slow switcher SW and cerebral microstructure in ageing is not established.
Methods
We recorded habitual sleep under EEG in 99 healthy late midlife individuals (mean age = 59.3 ± 5.3 years; 68 women) and extracted SW parameters (density, amplitude, frequency) for all SW as well as according to their switcher type (slow vs. fast). We further used neurite orientation dispersion and density imaging (NODDI) to assess microstructural integrity over a frontal grey matter region of interest (ROI).
Results
In statistical models adjusted for age, sex, and sleep duration, we found that a lower SW density, particularly for fast switcher SW, was associated with a reduced orientation dispersion of neurites in the frontal ROI (p = 0.018, R2β* = 0.06). In addition, overall SW frequency was positively associated with neurite density (p = 0.03, R2β* = 0.05). By contrast, we found no significant relationships between SW amplitude and NODDI metrics.
Conclusions
Our findings suggest that the complexity of neurite organization contributes specifically to the rate of fast switcher SW occurrence in healthy middle-aged individuals, corroborating slow and fast switcher SW as distinct types of SW. They further suggest that the density of frontal neurites plays a key role for neural synchronization during sleep.
Trial registration number
EudraCT 2016-001436-35.