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Brain mechanisms of insomnia: new perspectives on causes and consequences

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Van Someren, Eus J. W.·2021·Physiological Reviews

DOI 10.1152/physrev.00046.2019

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Abstract

While insomnia is the second most common mental disorder, progress in our understanding of underlying neurobiological mechanisms has been limited. The present review addresses the definition and prevalence of insomnia and explores its subjective and objective characteristics across the 24-hour day. Subsequently, the review extensively addresses how the vulnerability to develop insomnia is affected by genetic variants, early life stress, major life events, and brain structure and function. Further supported by the clear mental health risks conveyed by insomnia, the integrated findings suggest that the vulnerability to develop insomnia could rather be found in brain circuits regulating emotion and arousal than in circuits involved in circadian and homeostatic sleep regulation. Finally, a testable model is presented. The model proposes that in people with a vulnerability to develop insomnia, the locus coeruleus is more sensitive to—or receives more input from—the salience network and related circuits, even during rapid eye movement sleep, when it should normally be sound asleep. This vulnerability may ignite a downward spiral of insufficient overnight adaptation to distress, resulting in accumulating hyperarousal, which, in turn, impedes restful sleep and moreover increases the risk of other mental health adversity. Sensitized brain circuits are likely to be subjectively experienced as “sleeping with one eye open”. The proposed model opens up the possibility for novel intervention studies and animal studies, thus accelerating the ignition of a neuroscience of insomnia, which is direly needed for better treatment.

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Beta receptor-mediated modulation of the late positive potential in humans
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Examining the Crux of Autonomic Dysfunction in Posttraumatic Stress Disorder: Whether Chronic or Situational Distress Underlies Elevated Heart Rate and Attenuated Heart Rate Variability
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More Severe Insomnia Complaints in People with Stronger Long-Range Temporal Correlations in Wake Resting-State EEG
Colombo, M. A., Wei, Y., Ramautar, J. R., Linkenkaer‐Hansen, K., Tagliazucchi, E., & Someren, E. J. W. V. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00576 · Cited by 41
Diffusion Tensor Imaging Tractography Reveals Disrupted White Matter Structural Connectivity Network in Healthy Adults with Insomnia Symptoms
Lu, F., Dai, J., Couto, T. A., Liu, C., Chen, H., Lu, S.-L., Tang, L., Tie, C.-L., Chen, H.-F., He, M., et al. (2017) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2017.00583 · Cited by 41
A Pilot, Randomized Clinical Trial of Bedtime Doses of Prazosin Versus Placebo in Suicidal Posttraumatic Stress Disorder Patients With Nightmares
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Correlation between Cortical State and Locus Coeruleus Activity: Implications for Sensory Coding in Rat Barrel Cortex
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Abnormal Topology of the Structural Connectome in the Limbic Cortico-Basal-Ganglia Circuit and Default-Mode Network Among Primary Insomnia Patients
Wu, Y., Liu, M., Zeng, S., Ma, X., Yan, J., Lin, C., Xu, G., Li, G., Yin, Y., Fu, S., et al. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00860 · Cited by 40
Prenatal stress is associated with depression-related electroencephalographic sleep changes in adult male rats: a preliminary report
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Data-Driven Analysis of EEG Reveals Concomitant Superficial Sleep During Deep Sleep in Insomnia Disorder
Christensen, J. A. E., Wassing, R., Wei, Y., Ramautar, J. R., Lakbila‐Kamal, O., Jennum, P., & Someren, E. J. W. V. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00598 · Cited by 38
Actigraphic multi‐night home‐recorded sleep estimates reveal three types of sleep misperception in Insomnia Disorder and good sleepers
Lindert, B. H. W. T., Blanken, T. F., van der Meijden, W. P., Dekker, K., Wassing, R., van der Werf, Y. D., Ramautar, J. R., & Someren, E. J. W. V. (2019) · Journal of Sleep Research · doi:10.1111/jsr.12937 · Cited by 38
Recovery of Performance during Sleep following Sleep Deprivation in Older Normal and Insomniac Adult Males
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Association of Adenosine Receptor Gene Polymorphisms and In Vivo Adenosine A1 Receptor Binding in The Human Brain
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Brain structural connectivity network alterations in insomnia disorder reveal a central role of the right angular gyrus
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Long-term Effect of Cued Fear Conditioning on REM Sleep Microarchitecture in Rats
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The European Insomnia Guideline: An update on the diagnosis and treatment of insomnia 2023
Riemann, D., Espie, C. A., Altena, E., Arnardottir, E. S., Baglioni, C., Bassetti, C. L. A., Bastien, C., Berzina, N., Bjorvatn, B., Dikeos, D., et al. (2023) · Journal of Sleep Research · doi:10.1111/jsr.14035 · Cited by 834
“The interested reader is referred to recent work, much of which is part of the special insomnia issue of JSR (Dressle & Riemann, 2023; Espie, 2023; Fernandez & Perlis, 2023; Palagini et al., 2023; Reffi et al., 2023; Riemann et al., 2022; Tang et al., 2023; van Someren, 2021).”
The microbiota-gut-brain axis in sleep disorders
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Noradrenergic circuit control of non-REM sleep substates
Osorio-Forero, A., Cardis, R., Vantomme, G., Guillaume-Gentil, A., Katsioudi, G., Devenoges, C., Fernandez, L. M. J., & Lüthi, A. (2021) · Current Biology · doi:10.1016/j.cub.2021.09.041 · Cited by 230
Hyperarousal in insomnia disorder: Current evidence and potential mechanisms
Dressle, R. J., & Riemann, D. (2023) · Journal of Sleep Research · doi:10.1111/jsr.13928 · Cited by 218
Adenosine, caffeine, and sleep–wake regulation: state of the science and perspectives
Reichert, C. F., Deboer, T., & Landolt, H. (2022) · Journal of Sleep Research · doi:10.1111/jsr.13597 · Cited by 183
“Notwithstanding, large genome-wide association studies failed to provide evidence for enriched variant adenosinergic genes in patients with insomnia (Jansen et al., 2019; Van Someren, 2021).”
Background

See all 543

Authors: Van Someren, E. J. W.
Venue: Physiological Reviews
Publisher: American Physiological Society
Published: 2021-07-01
Volume: 101
Issue: 3
Pages: 995-1046
ISSN: 0031-9333 (ISSN-L)
1522-1210
DOI: 10.1152/physrev.00046.2019
OpenAlex: W3049362359
Cited by: 543
References: 441
FWCI: 8.75
Type: journal article
Language: en
Open access: green

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Brain mechanisms of insomnia: new perspectives on causes and consequences

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