Cognitive brain responses during circadian wake-promotion: evidence for sleep-pressure-dependent hypothalamic activations

Carolin F Reichert,Thomas Götz,Eric Salmon,Christian Cajochen,Christian Berthomier,Christina Schmidt,Klaus Scheffler,Micheline Maire,Christophe Phillips,Markus Klarhöfer,Werner Strobel,Antoine U Viola,Virginie Gabel

doi:10.1038/s41598-017-05695-1

Carolin F Reichert, Thomas Götz + Show 11 more

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https://doi.org/10.1038/s41598-017-05695-1

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The two-process model of sleep-wake regulation posits that sleep-wake-dependent homeostatic processes interact with the circadian timing system to affect human behavior. The circadian timing system is fundamental to maintaining stable cognitive performance, as it counteracts growing homeostatic sleep pressure during daytime. Using magnetic resonance imaging, we explored brain responses underlying working memory performance during the time of maximal circadian wake-promotion under varying sleep pressure conditions. Circadian wake-promoting strength was derived from the ability to sleep during an evening nap. Hypothalamic BOLD activity was positively linked to circadian wake-promoting strength under normal, but not under disproportionally high or low sleep pressure levels. Furthermore, higher hypothalamic activity under normal sleep pressure levels predicted better performance under sleep loss. Our results reappraise the two-process model by revealing a homeostatic-dose-dependent association between circadian wake-promotion and cognition-related hypothalamic activity.

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The two-process model of sleep-wake regulation posits that sleep-wake-dependent homeostatic processes interact with the circadian timing system to affect human behavior
The magnetic resonance imaging (MRI) sessions were scheduled 13 h after habitual wake-up time, on average 2.2 hours before the evening onset of melatonin secretion, which hallmarks the end of the wake-maintenance zone (WMZ) and opens the gate for sleep[25]
We measured working memory (WM) and underlying cerebral correlates with a visual n-back task, frequently used in neuroimaging studies[24, 28]

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The two-process model of sleep-wake regulation posits that sleep-wake-dependent homeostatic processes interact with the circadian timing system to affect human behavior. Lacking or mistimed circadian wake-promotion affects state stability during wakefulness[5, 6] and is associated with deterioration in neurobehavioral performance, when sleep propensity is high[7, 8] Accumulating evidence from both animal and human experiments indicates that the magnitude of circadian output signalling depends on homeostatic sleep pressure levels[7,8,9,10,11,12,13,14] and vice versa[15,16,17]. We predicted that hypothalamic BOLD activity during successful task performance is linked to circadian wake-promoting strength, and that this link is modulated by sleep pressure levels We expected this association to be attenuated under high sleep pressure conditions. On the other hand, assuming a monotonic dose-response relationship, the association should be amplified by disproportionally low sleep pressure levels induced by the NP condition

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