The impact of sleep restriction on cerebrovascular reactivity and cognitive outcomes in healthy adolescents: A pilot crossover trial

Amy Chan; Chun Ting Au; Myrtha E Reyna; Amanda Robertson; Kirstin Walker; Robyn Westmacott; Manohar Shroff; Luc Mertens; Nomazulu Dlamini; Indra Narang

doi:10.1016/j.sleep.2024.11.005

The impact of sleep restriction on cerebrovascular reactivity and cognitive outcomes in healthy adolescents: A pilot crossover trial

Sleep Med. 2024 Nov 9:124:717-726. doi: 10.1016/j.sleep.2024.11.005. Online ahead of print.

Authors

Affiliations

¹ Translational Medicine, Research Institute, The Hospital for Sick Children, Toronto, Ontario, Canada; Institute of Medical Science, University of Toronto, Ontario, Canada.
² Translational Medicine, Research Institute, The Hospital for Sick Children, Toronto, Ontario, Canada.
³ Neurosciences and Mental Health, Research Institute, The Hospital for Sick Children, Toronto, Ontario, Canada.
⁴ Department of Psychology, The Hospital for Sick Children, Toronto, ON, Canada.
⁵ Department of Diagnostic and Interventional Imaging, The Hospital for Sick Children, Toronto, ON, Canada; Department of Medical Imaging, University of Toronto, Ontario, Canada.
⁶ Department of Cardiology, The Hospital for Sick Children, Toronto, Ontario, Canada; Department of Paediatrics, Faculty of Medicine, University of Toronto, Ontario, Canada.
⁷ Neurosciences and Mental Health, Research Institute, The Hospital for Sick Children, Toronto, Ontario, Canada; Department of Paediatrics, Faculty of Medicine, University of Toronto, Ontario, Canada; Division of Neurology, The Hospital for Sick Children, Toronto, Ontario, Canada.
⁸ Translational Medicine, Research Institute, The Hospital for Sick Children, Toronto, Ontario, Canada; Department of Paediatrics, Faculty of Medicine, University of Toronto, Ontario, Canada; Division of Respiratory Medicine, The Hospital for Sick Children, Toronto, Ontario, Canada. Electronic address: indra.narang@sickkids.ca.

PMID: 39546870
DOI: 10.1016/j.sleep.2024.11.005

Abstract

Background: The underlying mechanism for the association between sleep restriction (SR) and unfavorable cognitive outcomes in children and adolescents remains unclear. This study aimed to understand the effect of 5-night experimental SR on magnetic resonance imaging (MRI) measurements of cerebrovascular reactivity (CVR) and cognitive function in adolescents.

Methods: This randomized crossover study compared two sleep conditions, SR and Control Sleep (CS) in a home setting. Healthy adolescents aged 15-18 years were recruited. The protocol began with two nights of baseline sleep to record participants' habitual sleep duration, followed by the two sleep conditions in the randomly allocated sequence, either SR (6 h in bed for 5 nights) followed by CS (9 h in bed for 5 nights), or the reverse sequence. Their sleep-wake pattern was monitored by an accelerometer and a sleep diary throughout the study period. Cerebral hemodynamics were assessed by hypercapnic challenge blood oxygen level-dependent (BOLD) MRI of CVR. Cognitive function was evaluated by NIH Toolbox Cognitive Battery on the day immediately after each sleep condition.

Results: A total of 27 participants (8 males; mean age: 16.8 ± 0.7 years, range 15-18 years) were included in the study. The average sleep duration was significantly reduced in the SR condition compared to the CS condition (320 ± 34 min vs. 426 ± 45 min, p < 0.001). The CVR in the temporal occipital fusiform cortex [adjusted β(95 % CI) = -0.091(-0.010 to -0.172), p = 0.032] and occipital lobe [adjusted β(95 % CI) = -0.087 (-0.002 to -0.172), p = 0.045] was significantly lower following the SR condition when compared to the CS condition. Participants also had lower performance scores in the inhibitory control [adjusted β(95 % CI) = -6.0(-0.9 to -11.0), p = 0.019] and cognitive flexibility [adjusted β(95 % CI) = -6.6 (-1.7 to -11.6), p = 0.008] domains after the SR condition when compared to the CS condition.

Conclusions: Short-term SR is associated with poorer cognitive function possibly through reduced cerebral vasodilatory capacity in specific cognitive regions.

Keywords: Adolescents; Cerebral hemodynamics; Cerebrovascular reactivity; Cognitive function; MRI; RCT; Sleep restriction.