NeuroImage (May 2023)

Association between sleep slow-wave activity and in-vivo estimates of myelin in healthy young men

  • Michele Deantoni,
  • Marion Baillet,
  • Gregory Hammad,
  • Christian Berthomier,
  • Mathilde Reyt,
  • Mathieu Jaspar,
  • Christelle Meyer,
  • Maxime Van Egroo,
  • Puneet Talwar,
  • Eric Lambot,
  • Sarah L. Chellappa,
  • Christian Degueldre,
  • André Luxen,
  • Eric Salmon,
  • Evelyne Balteau,
  • Christophe Phillips,
  • Derk-Jan Dijk,
  • Gilles Vandewalle,
  • Fabienne Collette,
  • Pierre Maquet,
  • Vincenzo Muto,
  • Christina Schmidt

Journal volume & issue
Vol. 272
p. 120045

Abstract

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Sleep has been suggested to contribute to myelinogenesis and associated structural changes in the brain. As a principal hallmark of sleep, slow-wave activity (SWA) is homeostatically regulated but also differs between individuals. Besides its homeostatic function, SWA topography is suggested to reflect processes of brain maturation. Here, we assessed whether interindividual differences in sleep SWA and its homeostatic response to sleep manipulations are associated with in-vivo myelin estimates in a sample of healthy young men. Two hundred twenty-six participants (18–31 y.) underwent an in-lab protocol in which SWA was assessed at baseline (BAS), after sleep deprivation (high homeostatic sleep pressure, HSP) and after sleep saturation (low homeostatic sleep pressure, LSP). Early-night frontal SWA, the frontal-occipital SWA ratio, as well as the overnight exponential SWA decay were computed over sleep conditions. Semi-quantitative magnetization transfer saturation maps (MTsat), providing markers for myelin content, were acquired during a separate laboratory visit. Early-night frontal SWA was negatively associated with regional myelin estimates in the temporal portion of the inferior longitudinal fasciculus. By contrast, neither the responsiveness of SWA to sleep saturation or deprivation, its overnight dynamics, nor the frontal/occipital SWA ratio were associated with brain structural indices. Our results indicate that frontal SWA generation tracks inter-individual differences in continued structural brain re-organization during early adulthood. This stage of life is not only characterized by ongoing region-specific changes in myelin content, but also by a sharp decrease and a shift towards frontal predominance in SWA generation.

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