Association between circadian sleep regulation and cortical gyrification in young and older adults

Abstract

The circadian system orchestrates sleep timing and structure and is altered with increasing age. Sleep propensity, and particularly REM sleep is under strong circadian control and has been suggested to play an important role in brain plasticity. In this exploratory study, we assessed whether surface-based brain morphometry indices are associated with circadian sleep regulation and whether this link changes with age. Twenty-nine healthy older (55-82 years; 16 men) and 28 young participants (20-32 years; 13 men) underwent both structural magnetic resonance imaging and a 40-h multiple nap protocol to extract sleep parameters over day and night time. Cortical thickness and gyrification indices were estimated from T1-weighted images acquired during a classical waking day. We observed that REM sleep was significantly modulated over the 24-h cycle in both age groups, with older adults exhibiting an overall reduction in REM sleep modulation compared to young individuals. Interestingly, when taking into account the observed overall age-related reduction in REM sleep throughout the circadian cycle, higher day-night differences in REM sleep were associated with increased cortical gyrification in the right inferior frontal and paracentral regions in older adults. Our results suggest that a more distinctive allocation of REM sleep over the 24-h cycle is associated with regional cortical gyrification in aging, and thereby point towards a protective role of circadian REM sleep regulation for age-related changes in brain organization.

Napping and circadian sleep–wake regulation during healthy aging

“…First indications of our work go indeed in the direction that circadian REM sleep regulation affects regional macrostructural integrity (i.e. cortical gyrification) in the aging brain [51].…”

“…Amongst them, REM sleep has been shown to be under the strongest circadian control [73] and the circadian pacemaker has been suggested to actively promote REM sleep at specific times of the day [74,75]. Interestingly, a reduced modulation of REM sleep has been observed in older, compared to young individuals [9,51]. Our results provide first evidence that napping in the aged leads to or may be the consequence of a disproportional reduction in the circadian REM sleep propensity drive, leading to an overall higher REM sleep expression, when prompted to sleep during the active wake period.…”

“…Sleep stages were automatically scored in 30-second epochs according to the American Academy of Sleep Medicine criteria AASM [47] using the ASEEGA sleep scoring algorithm (ASEEGA, PHYSIP, Paris, France). The algorithm has been previously used to score nighttime sleep in healthy young [48] and older [49] adults, but also in a series of sleep pathologies [50] and during daytime naps [51]. During each sleep opportunity, classical sleep parameters were extracted, including sleep efficiency (SE: sum of sleep stages 1, 2, 3, and REM divided by total sleep opportunity), sleep stage 1-3 (N1%, N2%, and N3%), as well as REM (REM%), expressed as a percentage over total sleep time (TST).…”

Circadian rapid eye movement sleep expression is associated with brain microstructural integrity in older adults

“…Sleep stages were scored automatically in 30-second epochs according to the American Academy of Sleep Medicine criteria (AASM 52 ) using the ASEEGA sleep scoring algorithm (ASEEGA, PHYSIP, Paris, France), based on spectral composition of electroencephalographic signals acquired during sleep opportunities. We previously reported the use of this automatic algorithm to score sleep and REMS in the context of napping in young and older individuals 20 . In addition, the consistency between the hypnograms and the spectral plots of the ~860 nap recordings was visually inspected by a trained sleep scorer to ensure that the algorithm did not overlook any major episodes of REMS.…”

“…Assessing a specific sleep regulation process rather than the expression of a sleep stage per se, which may be affected by different factors including environmental constraints and/or sleep-wake history, may be particularly relevant for understanding the association between sleep and brain structure during aging. In a recent exploratory study, we gathered first evidence that circadian REMS expression is associated with local cortical gyrification in healthy older adults 20 . Importantly, such changes or re-organisation at the macrostructural level are assumed to be preceded by microstructural tissue alteration 21 .…”