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The Journal of Neuroscience, June 24, 2009, 29(25):7948-7956; doi:10.1523/JNEUROSCI.0229-09.2009

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Behavioral/Systems/Cognitive
Functional Magnetic Resonance Imaging-Assessed Brain Responses during an Executive Task Depend on Interaction of Sleep Homeostasis, Circadian Phase, and PER3 Genotype

Gilles Vandewalle,¹ Simon N. Archer,² Catherine Wuillaume,¹ Evelyne Balteau,¹ Christian Degueldre,¹ André Luxen,¹ Pierre Maquet,¹ and Derk-Jan Dijk²

¹Cyclotron Research Centre, University of Liège, B-4000 Liège, Belgium, and ²Surrey Sleep Research Centre, University of Surrey, Guildford, Surrey GU2 7XP, United Kingdom

Correspondence should be addressed to Pierre Maquet, Centre de Recherches du Cyclotron, Université de Liège, B30, Sart Tilman, B-4000 Liège, Belgium. Email: pmaquet{at}ulg.ac.be

Cognition is regulated across the 24 h sleep-wake cycle by circadian rhythmicity and sleep homeostasis through unknown brain mechanisms. We investigated these mechanisms in a functional magnetic resonance imaging study of executive function using a working memory 3-back task during a normal sleep-wake cycle and during sleep loss. The study population was stratified according to homozygosity for a variable-number (4 or 5) tandem-repeat polymorphism in the coding region of the clock gene PERIOD3. This polymorphism confers vulnerability to sleep loss and circadian misalignment through its effects on sleep homeostasis. In the less-vulnerable genotype, no changes were observed in brain responses during the normal-sleep wake cycle. During sleep loss, these individuals recruited supplemental anterior frontal, temporal and subcortical regions, while executive function was maintained. In contrast, in the vulnerable genotype, activation in a posterior prefrontal area was already reduced when comparing the evening to the morning during a normal sleep-wake cycle. Furthermore, in the morning after a night of sleep loss, widespread reductions in activation in prefrontal, temporal, parietal and occipital areas were observed in this genotype. These differences occurred in the absence of genotype-dependent differences in circadian phase. The data show that dynamic changes in brain responses to an executive task evolve across the sleep-wake and circadian cycles in a regionally specific manner that is determined by a polymorphism which affects sleep homeostasis. The findings support a model of individual differences in executive control, in which the allocation of prefrontal resources is constrained by sleep pressure and circadian phase.

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Received Jan. 14, 2009; revised April 15, 2009; accepted April 24, 2009.

Correspondence should be addressed to Pierre Maquet, Centre de Recherches du Cyclotron, Université de Liège, B30, Sart Tilman, B-4000 Liège, Belgium. Email: pmaquet{at}ulg.ac.be

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