Effects of sleep deprivation on neural functioning: an integrative review

Boonstra, Tjeerd W.; Stins, John F.; Daffertshofer, Andreas; Beek, Peter J. · 2007 · OpenAlex-citations

DOI: 10.1007/s00018-007-6457-8

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Summary

This integrative review examines the neurophysiological mechanisms underlying the cognitive and behavioral impairments caused by sleep deprivation (SD). Motivated by the prevalence of chronic sleep loss in modern society and the need to understand how SD affects neural functioning across different scales, the authors synthesize experimental literature involving human participants and animal models. The review structures its analysis across three levels of observation: the macro-level (behavior and large-scale brain activity), the meso-level (neural synchronization and ensembles), and the micro-level (molecular and cellular processes). The primary goal is to elucidate the links between SD-induced cognitive deterioration and specific changes in neural activity, particularly focusing on the prefrontal cortex (PFC) and attentional networks. The authors analyze data from neuroimaging studies (fMRI, PET), encephalography (EEG, MEG), and molecular research. At the macro-level, SD is shown to impair executive functions, especially in novel tasks requiring attention, while also causing subjective sleepiness and mood disturbances. Neuroimaging results regarding the PFC are mixed; some studies report decreased activity in the dorsolateral PFC, suggesting an inability to meet task demands, while others report increased activity, interpreted as a compensatory mechanism similar to neural changes in aging. At the meso-level, the review highlights changes in event-related potentials (ERPs). Specifically, SD reduces the amplitude of the N1 component (associated with sensory processing and attention) and the P300 component (associated with frontal lobe function and attentional network engagement). These reductions indicate decreased cortical responsiveness to stimuli. Spectral analysis of EEG data reveals a shift toward slower frequencies, with increased theta activity and decreased alpha activity, reflecting cortical deactivation and increased sleep propensity. At the micro-level, the review identifies adenosine (AD) and acetylcholine (ACh) as key mediators. Extracellular adenosine levels in the basal forebrain progressively increase during prolonged wakefulness, acting as an inhibitory neuromodulator. This accumulation inhibits cholinergic neurons, leading to reduced cortical acetylcholine levels. The authors argue that this decrease in ACh is a critical link between molecular changes and macroscopic effects, as reduced cholinergic activity mirrors the attentional deficits and ERP changes observed in SD. Furthermore, the review notes that psychostimulants like caffeine and modafinil can temporarily reverse these effects by antagonizing adenosine receptors or activating cholinergic systems, thereby restoring vigilance and executive function. The significance of this review lies in its integrative approach, connecting behavioral deficits to specific neural and molecular alterations. It concludes that the inhibition of cholinergic nuclei by accumulating adenosine is a central mechanism explaining the reduced cortical responsiveness and attentional impairments seen in sleep deprivation. The authors emphasize that while the relationships between effects across observation scales are becoming clearer, further research is needed to fully understand these cross-level interactions. This understanding is crucial for developing interventions to mitigate the cognitive costs of sleep loss in populations affected by chronic sleep debt.

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• sleep deprivation