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Associations Between Sleep Health and Amygdala Reactivity to Negative Facial Expressions in the UK Biobank Cohort

  • Julian E. Schiel
    Correspondence
    Address correspondence to Julian E. Schiel, M.Sc.
    Affiliations
    Department of Psychiatry and Psychotherapy, Medical Centre – University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany
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  • Sandra Tamm
    Affiliations
    Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden

    Department of Psychiatry, University of Oxford, Oxford, United Kingdom
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  • Florian Holub
    Affiliations
    Department of Psychiatry and Psychotherapy, Medical Centre – University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany
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  • Roxana Petri
    Affiliations
    Department of Psychiatry and Psychotherapy, Medical Centre – University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany
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  • Hassan S. Dashti
    Affiliations
    Broad Institute of MIT and Harvard, Cambridge, Massachusetts

    Center for Genomic Medicine, Massachusetts General Hospital, Boston, Massachusetts

    Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts
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  • Katharina Domschke
    Affiliations
    Department of Psychiatry and Psychotherapy, Medical Centre – University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany
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  • Bernd Feige
    Affiliations
    Department of Psychiatry and Psychotherapy, Medical Centre – University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany
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  • Jacqueline M. Lane
    Affiliations
    Broad Institute of MIT and Harvard, Cambridge, Massachusetts

    Center for Genomic Medicine, Massachusetts General Hospital, Boston, Massachusetts

    Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts
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  • Dieter Riemann
    Affiliations
    Department of Psychiatry and Psychotherapy, Medical Centre – University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany
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  • Martin K. Rutter
    Affiliations
    Centre for Biological Timing, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, United Kingdom

    Diabetes, Endocrinology and Metabolism Centre, Manchester University NHS Foundation Trust, Manchester Academic Health Sciences Centre, Manchester, United Kingdom
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  • Richa Saxena
    Affiliations
    Broad Institute of MIT and Harvard, Cambridge, Massachusetts

    Center for Genomic Medicine, Massachusetts General Hospital, Boston, Massachusetts

    Department of Anesthesia, Critical Care and Pain Medicine, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts
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  • Masoud Tahmasian
    Affiliations
    Institute of Neuroscience and Medicine, Brain and Behavior (INM-7), Research Center Jülich, Jülich, Germany

    Institute for Systems Neuroscience, Medical Faculty, Heinrich-Heine-Universität Düsseldorf, Düsseldorf, Germany
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  • Heming Wang
    Affiliations
    Broad Institute of MIT and Harvard, Cambridge, Massachusetts

    Division of Sleep and Circadian Disorders, Brigham and Women’s Hospital and Harvard Medical School, Boston, Massachusetts

    Department of Population and Quantitative Health Sciences, Case Western Reserve University, Cleveland, Ohio
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  • Author Footnotes
    1 SDK and KS contributed equally to this work.
    Simon D. Kyle
    Footnotes
    1 SDK and KS contributed equally to this work.
    Affiliations
    Sleep and Circadian Neuroscience Institute, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
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  • Author Footnotes
    1 SDK and KS contributed equally to this work.
    Kai Spiegelhalder
    Footnotes
    1 SDK and KS contributed equally to this work.
    Affiliations
    Department of Psychiatry and Psychotherapy, Medical Centre – University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany
    Search for articles by this author
  • Author Footnotes
    1 SDK and KS contributed equally to this work.

      Abstract

      Background

      Sleep health (SH) is considered a key determinant of human physiological and psychological well-being. In line with this, previous studies have found that poor sleep is associated with various psychiatric disorders, in particular, with anxiety and depression. Although little is known about the neural mechanisms underlying these associations, recent findings suggest that essential dimensions of SH are associated with altered amygdala reactivity (AR); however, evidence to date is inconsistent and reliant on small sample sizes.

      Methods

      To address this problem, the current preregistered study investigated associations between SH and AR to negative facial expressions in the UK Biobank cohort (25,758 participants). Drawing on a large sample size and consistent data acquisition, 5 dimensions of SH (insomnia symptoms, sleep duration, daytime sleepiness, chronotype, and sleep medication) were examined.

      Results

      Exploratory analyses revealed that short sleep duration was associated with decreased AR. The remaining SH dimensions and a composite measure of all SH dimensions were not associated with AR.

      Conclusions

      To our knowledge, this is the largest study to test associations between SH and AR. Habitual short sleep duration may be associated with decreased AR, possibly indicating compensation for impaired prefrontal processes and hampered emotion regulation.

      Keywords

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      References

        • Baglioni C.
        • Spiegelhalder K.
        • Lombardo C.
        • Riemann D.
        Sleep and emotions: A focus on insomnia.
        Sleep Med Rev. 2010; 14: 227-238
        • Baglioni C.
        • Battagliese G.
        • Feige B.
        • Spiegelhalder K.
        • Nissen C.
        • Voderholzer U.
        • et al.
        Insomnia as a predictor of depression: A meta-analytic evaluation of longitudinal epidemiological studies.
        J Affect Disord. 2011; 135: 10-19
        • Hertenstein E.
        • Feige B.
        • Gmeiner T.
        • Kienzler C.
        • Spiegelhalder K.
        • Johann A.
        • et al.
        Insomnia as a predictor of mental disorders: A systematic review and meta-analysis.
        Sleep Med Rev. 2019; 43: 96-105
        • Pigeon W.R.
        • Hegel M.
        • Unützer J.
        • Fan M.Y.
        • Sateia M.J.
        • Lyness J.M.
        • et al.
        Is insomnia a perpetuating factor for late-life depression in the IMPACT cohort?.
        Sleep. 2008; 31: 481-488
        • Lustberg L.
        • Reynolds 3rd, C.F.
        Depression and insomnia: Questions of cause and effect.
        Sleep Med Rev. 2000; 4: 253-262
        • Baglioni C.
        • Nanovska S.
        • Regen W.
        • Spiegelhalder K.
        • Feige B.
        • Nissen C.
        • et al.
        Sleep and mental disorders: A meta-analysis of polysomnographic research.
        Psychol Bull. 2016; 142: 969-990
        • Riemann D.
        • Krone L.B.
        • Wulff K.
        • Nissen C.
        Sleep, insomnia, and depression.
        Neuropsychopharmacology. 2020; 45: 74-89
        • Yoo S.S.
        • Gujar N.
        • Hu P.
        • Jolesz F.A.
        • Walker M.P.
        The human emotional brain without sleep – A prefrontal amygdala disconnect.
        Curr Biol. 2007; 17: R877-R878
        • Motomura Y.
        • Kitamura S.
        • Oba K.
        • Terasawa Y.
        • Enomoto M.
        • Katayose Y.
        • et al.
        Sleep debt elicits negative emotional reaction through diminished amygdala-anterior cingulate functional connectivity.
        PLoS One. 2013; 8e56578
        • Baglioni C.
        • Spiegelhalder K.
        • Regen W.
        • Feige B.
        • Nissen C.
        • Lombardo C.
        • et al.
        Insomnia disorder is associated with increased amygdala reactivity to insomnia-related stimuli.
        Sleep. 2014; 37: 1907-1917
        • Wassing R.
        • Lakbila-Kamal O.
        • Ramautar J.R.
        • Stoffers D.
        • Schalkwijk F.
        • Van Someren E.J.W.
        Restless REM sleep impedes overnight amygdala adaptation.
        Curr Biol. 2019; 29: 2351-2358.e4
        • Klumpp H.
        • Hosseini B.
        • Phan K.L.
        Self-reported sleep quality modulates amygdala resting-state functional connectivity in anxiety and depression.
        Front Psychiatry. 2018; 9: 220
        • Furihata R.
        • Hall M.H.
        • Stone K.L.
        • Ancile-Israel S.
        • Smagula S.F.
        • Cauley J.A.
        • et al.
        An aggregate measure of sleep health is associated with prevalent and incident clinically significant depression symptoms among community-dwelling older women.
        Sleep. 2017; 40: zsw075
        • Brindle R.C.
        • Cribbet M.R.
        • Samuelsson L.B.
        • Gao C.
        • Frank E.
        • Krafty R.T.
        • et al.
        The relationship between childhood trauma and poor sleep health in adulthood.
        Psychosom Med. 2018; 80: 200-207
        • Dong L.
        • Martinez A.J.
        • Buysse D.J.
        • Harvey A.G.
        A composite measure of sleep health predicts concurrent mental and physical health outcomes in adolescents prone to eveningness.
        Sleep Health. 2019; 5: 166-174
        • Buysse D.J.
        Sleep health: Can we define it? Does it matter?.
        Sleep. 2014; 37: 9-17
        • Kyle S.D.
        • Sexton C.E.
        • Feige B.
        • Luik A.I.
        • Lane J.
        • Saxena R.
        • et al.
        Sleep and cognitive performance: Cross-sectional associations in the UK Biobank.
        Sleep Med. 2017; 38: 85-91
        • Cappuccio F.P.
        • Cooper D.
        • D’Elia L.
        • Strazzullo P.
        • Miller M.A.
        Sleep duration predicts cardiovascular outcomes: A systematic review and meta-analysis of prospective studies.
        Eur Heart J. 2011; 32: 1484-1492
        • Liu T.Z.
        • Xu C.
        • Rota M.
        • Cai H.
        • Zhang C.
        • Shi M.J.
        • et al.
        Sleep duration and risk of all-cause mortality: A flexible, non-linear, meta-regression of 40 prospective cohort studies.
        Sleep Med Rev. 2017; 32: 28-36
        • Li M.
        • Zhang X.W.
        • Hou W.S.
        • Tang Z.Y.
        Insomnia and risk of cardiovascular disease: A meta-analysis of cohort studies.
        Int J Cardiol. 2014; 176: 1044-1047
        • Meng L.
        • Zheng Y.
        • Hui R.
        The relationship of sleep duration and insomnia to risk of hypertension incidence: A meta-analysis of prospective cohort studies.
        Hypertens Res. 2013; 36: 985-995
        • Pigeon W.R.
        • Pinquart M.
        • Conner K.
        Meta-analysis of sleep disturbance and suicidal thoughts and behaviors.
        J Clin Psychiatry. 2012; 73: e1160-e1167
        • Empana J.P.
        • Dauvilliers Y.
        • Dartigues J.F.
        • Ritchie K.
        • Gariepy J.
        • Jouven X.
        • et al.
        Excessive daytime sleepiness is an independent risk indicator for cardiovascular mortality in community-dwelling elderly: The three city study.
        Stroke. 2009; 40: 1219-1224
        • Jaussent I.
        • Bouyer J.
        • Ancelin M.L.
        • Akbaraly T.
        • Pérès K.
        • Ritchie K.
        • et al.
        Insomnia and daytime sleepiness are risk factors for depressive symptoms in the elderly.
        Sleep. 2011; 34: 1103-1110
        • Merikanto I.
        • Lahti T.
        • Puolijoki H.
        • Vanhala M.
        • Peltonen M.
        • Laatikainen T.
        • et al.
        Associations of chronotype and sleep with cardiovascular diseases and type 2 diabetes.
        Chronobiol Int. 2013; 30: 470-477
        • Au J.
        • Reece J.
        The relationship between chronotype and depressive symptoms: A meta-analysis.
        J Affect Disord. 2017; 218: 93-104
        • Bouwmans M.E.J.
        • Bos E.H.
        • Hoenders H.J.R.
        • Oldehinkel A.J.
        • de Jonge P.
        Sleep quality predicts positive and negative affect but not vice versa. An electronic diary study in depressed and healthy individuals.
        J Affect Disord. 2017; 207: 260-267
        • Sin N.L.
        • Almeida D.M.
        • Crain T.L.
        • Kossek E.E.
        • Berkman L.F.
        • Buxton O.M.
        Bidirectional, temporal associations of sleep with positive events, affect, and stressors in daily life across a week.
        Ann Behav Med. 2017; 51: 402-415
        • Chiang J.J.
        • Kim J.J.
        • Almeida D.M.
        • Bower J.E.
        • Dahl R.E.
        • Irwin M.R.
        • et al.
        Sleep efficiency modulates associations between family stress and adolescent depressive symptoms and negative affect.
        J Adolesc Health. 2017; 61: 501-507
        • Schiel J.E.
        • Holub F.
        • Petri R.
        • Leerssen J.
        • Tamm S.
        • Tahmasian M.
        • et al.
        Affect and arousal in insomnia: Through a lens of neuroimaging studies.
        Curr Psychiatry Rep. 2020; 22: 44
        • Riemann D.
        • Spiegelhalder K.
        • Feige B.
        • Voderholzer U.
        • Berger M.
        • Perlis M.
        • Nissen C.
        The hyperarousal model of insomnia: A review of the concept and its evidence.
        Sleep Med Rev. 2010; 14: 19-31
        • Lane J.M.
        • Jones S.E.
        • Dashti H.S.
        • Wood A.R.
        • Aragam K.G.
        • van Hees V.T.
        • et al.
        Biological and clinical insights from genetics of insomnia symptoms.
        Nat Genet. 2019; 51: 387-393
        • Hariri A.R.
        • Tessitore A.
        • Mattay V.S.
        • Fera F.
        • Weinberger D.R.
        The amygdala response to emotional stimuli: A comparison of faces and scenes.
        Neuroimage. 2002; 17: 317-323
        • van der Helm E.
        • Yao J.
        • Dutt S.
        • Rao V.
        • Saletin J.M.
        • Walker M.P.
        REM sleep depotentiates amygdala activity to previous emotional experiences.
        Curr Biol. 2011; 21: 2029-2032
        • Prather A.A.
        • Bogdan R.
        • Hariri A.R.
        Impact of sleep quality on amygdala reactivity, negative affect, and perceived stress.
        Psychosom Med. 2013; 75: 350-358
        • Etkin A.
        • Wager T.D.
        Functional neuroimaging of anxiety: A meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia.
        Am J Psychiatry. 2007; 164: 1476-1488
        • Zald D.H.
        The human amygdala and the emotional evaluation of sensory stimuli.
        Brain Res Brain Res Rev. 2003; 41: 88-123
        • Spiegelhalder K.
        • Regen W.
        • Baglioni C.
        • Nissen C.
        • Riemann D.
        • Kyle S.D.
        Neuroimaging insights into insomnia.
        Curr Neurol Neurosci Rep. 2015; 15: 9
        • Button K.S.
        • Ioannidis J.P.
        • Mokrysz C.
        • Nosek B.A.
        • Flint J.
        • Robinson E.S.
        • Munafò M.R.
        Power failure: Why small sample size undermines the reliability of neuroscience.
        Nat Rev Neurosci. 2013; 14: 365-376
        • Nord C.L.
        • Valton V.
        • Wood J.
        • Roiser J.P.
        Power-up: A reanalysis of ‘power failure’ in neuroscience using mixture modeling.
        J Neurosci. 2017; 37: 8051-8061
        • Sudlow C.
        • Gallacher J.
        • Allen N.
        • Beral V.
        • Burton P.
        • Danesh J.
        • et al.
        UK biobank: An open access resource for identifying the causes of a wide range of complex diseases of middle and old age.
        PLoS Med. 2015; 12e1001779
        • Miller K.L.
        • Alfaro-Almagro F.
        • Bangerter N.K.
        • Thomas D.L.
        • Yacoub E.
        • Xu J.
        • et al.
        Multimodal population brain imaging in the UK Biobank prospective epidemiological study.
        Nat Neurosci. 2016; 19: 1523-1536
        • Alfaro-Almagro F.
        • Jenkinson M.
        • Bangerter N.K.
        • Andersson J.L.R.
        • Griffanti L.
        • Douaud G.
        • et al.
        Image processing and quality control for the first 10,000 brain imaging datasets from UK Biobank.
        Neuroimage. 2018; 166: 400-424
        • Alvarez G.G.
        • Ayas N.T.
        The impact of daily sleep duration on health: A review of the literature.
        Prog Cardiovasc Nurs. 2004; 19: 56-59
        • Watson N.F.
        • Badr M.S.
        • Belenky G.
        • Bliwise D.L.
        • Buxton O.M.
        • et al.
        • Consensus Conference Panel
        Recommended amount of sleep for a healthy adult: A joint consensus statement of the American Academy of Sleep Medicine and Sleep Research Society.
        J Clin Sleep Med. 2015; 11: 591-592
        • Dashti H.S.
        • Jones S.E.
        • Wood A.R.
        • Lane J.M.
        • Van Hees V.T.
        • Wang H.
        • et al.
        Genome-wide association study identifies genetic loci for self-reported habitual sleep duration supported by accelerometer-derived estimates.
        Nat Commun. 2019; 10: 1100
        • Barch D.M.
        • Burgess G.C.
        • Harms M.P.
        • Petersen S.E.
        • Schlage B.L.
        • Corbetta M.
        • et al.
        Function in the human connectome: Task-fMRI and individual differences in behavior.
        Neuroimage. 2013; 80: 169-189
        • Elam J.S.
        • Glasser M.F.
        • Harms M.P.
        • Sotiropoulos S.N.
        • Andersson J.L.R.
        • Burgess G.C.
        • et al.
        The Human Connectome Project: A retrospective.
        Neuroimage. 2021; 244118543
        • Taylor P.J.
        • Marsh J.E.
        E-prime. Software: The International Encyclopedia of Communication Research Methods.
        2017: 1-3
        • Hu S.
        Akaike information criterion. 93. Center for Research in Scientific Computation, 2007
        • Wassing R.
        • Schalkwijk F.
        • Lakbila-Kamal O.
        • Ramautar J.R.
        • Stoffers D.
        • Mutsaerts H.J.M.M.
        • et al.
        Haunted by the past: Old emotions remain salient in insomnia disorder.
        Brain. 2019; 142: 1783-1796
        • Beattie L.
        • Kyle S.D.
        • Espie C.A.
        • Biello S.M.
        Social interactions, emotion and sleep: A systematic review and research agenda.
        Sleep Med Rev. 2015; 24: 83-100
        • Cote K.
        • Jancsar C.
        • Hunt B.
        Event-related neural response to emotional picture stimuli following sleep deprivation.
        Psychol Neurosci. 2015; 8: 102-113
        • Mauss I.B.
        • Troy A.S.
        • LeBourgeois M.K.
        Poorer sleep quality is associated with lower emotion-regulation ability in a laboratory paradigm.
        Cogn Emot. 2013; 27: 567-576
        • Palmer C.A.
        • Alfano C.A.
        Sleep and emotion regulation: An organizing, integrative review.
        Sleep Med Rev. 2017; 31: 6-16
        • Thomas M.
        • Sing H.
        • Belenky G.
        • Holcomb H.
        • Mayberg H.
        • Dannals R.
        • et al.
        Neural basis of alertness and cognitive performance impairments during sleepiness. I. Effects of 24 h of sleep deprivation on waking human regional brain activity.
        J Sleep Res. 2000; 9: 335-352
        • Verweij I.M.
        • Romeijn N.
        • Smit D.J.
        • Piantoni G.
        • Van Someren E.J.
        • van der Werf Y.D.
        Sleep deprivation leads to a loss of functional connectivity in frontal brain regions.
        BMC Neurosci. 2014; 15: 88
        • Farah M.J.
        The neuroscience of socioeconomic status: Correlates, causes, and consequences.
        Neuron. 2017; 96: 56-71
        • Leclerc C.M.
        • Kensinger E.A.
        Neural processing of emotional pictures and words: A comparison of young and older adults.
        Dev Neuropsychol. 2011; 36: 519-538
        • Mather M.
        The affective neuroscience of aging.
        Annu Rev Psychol. 2016; 67: 213-238
        • Leehr E.J.
        • Krohmer K.
        • Schag K.
        • Dresler T.
        • Zipfel S.
        • Giel K.E.
        Emotion regulation model in binge eating disorder and obesity--a systematic review.
        Neurosci Biobehav Rev. 2015; 49: 125-134
        • Tamm S.
        • Harmer C.J.
        • Schiel J.E.
        • Holub F.
        • Rutter M.K.
        • Spiegelhalder K.
        • et al.
        Amygdala responses to negative faces are not associated with depressive symptoms: Cross-sectional data from 28,638 individuals in the UK Biobank cohort.
        Am J Psychiatry. 2022; 179: 509-513
        • Hammerschlag A.R.
        • Stringer S.
        • De Leeuw C.A.
        • Sniekers S.
        • Taskesen E.
        • Watanabe K.
        • et al.
        Genome-wide association analysis of insomnia complaints identifies risk genes and genetic overlap with psychiatric and metabolic traits.
        Nat Genet. 2017; 49: 1584-1592
        • Kohn N.
        • Eickhoff S.B.
        • Scheller M.
        • Laird A.R.
        • Fox P.T.
        • Habel U.
        Neural network of cognitive emotion regulation–An ALE meta-analysis and MACM analysis.
        Neuroimage. 2014; 87: 345-355