Advertisement
Research Article| Volume 7, ISSUE 1, P72-78, February 2021

Download started.

Ok

Stress, sleep, and autonomic function in healthy adolescent girls and boys: Findings from the NCANDA study

      Abstract

      Objectives

      Starting in adolescence, female sex is a strong risk factor for the development of insomnia. Reasons for this are unclear but could involve altered stress reactivity and/or autonomic nervous system (ANS) dysregulation, which are strongly associated with the pathophysiology of insomnia. We investigated sex differences in the effect of stress on sleep and ANS activity in adolescents, using the first night in the laboratory as an experimental sleep-related stressor.

      Design

      Repeated measures (first night vs. a subsequent night) with age (older/younger) and sex (males/females) as between factors.

      Setting

      Recordings were performed at the human sleep laboratory at SRI International.

      Participants

      One hundred six healthy adolescents (Age, mean ± SD: 15.2 ± 2.0 years; 57 boys).

      Measures

      Polysomnographic sleep, nocturnal heart rate (HR), and frequency-domain spectral ANS HR variability (HRV) indices.

      Results

      Boys and girls showed a first-night effect, characterized by lower sleep efficiency, lower %N1 and %N2 sleep, more wake after sleep onset and %N3 sleep, altered sleep microstructure (increased high-frequency sigma and Beta1 electroencephalographic activity), and reduced vagal activity (P < .05) on the first laboratory night compared to a subsequent night. The first night ANS stress effect (increases in HR and suppression in vagal HRV during rapid eye movement sleep) was greater in girls than boys (P < .05).

      Conclusions

      Sleep and ANS activity were altered during the first laboratory night in adolescents, with girls exhibiting greater ANS alterations than boys. Findings suggest that girls may be more vulnerable than boys to sleep-specific stressors, which could contribute to their increased risk for developing stress-related sleep disturbances.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Sleep Health: Journal of the National Sleep Foundation
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Shochat T.
        • Cohen-Zion M.
        • Tzischinsky O
        Functional consequences of inadequate sleep in adolescents: a systematic review.
        Sleep Med Rev. 2014; 18: 75-87
        • National Institutes of Health
        National Institutes of Health state of the science conference statement on manifestations and management of chronic insomnia in adults, June 13-15, 2005.
        Sleep. 2005; 28: 1049-1057
        • Zhang B.
        • Wing Y.K.
        Sex differences in insomnia: a meta-analysis.
        Sleep. 2006; 29: 85-93
        • Groeger J.A.
        • Zijlstra F.R.
        • Dijk D.J
        Sleep quantity, sleep difficulties and their perceived consequences in a representative sample of some 2000 British adults.
        J Sleep Res. 2004; 13: 359-371
        • Collop N.A.
        • Adkins D.
        • Phillips B.A
        Gender differences in sleep and sleep-disordered breathing.
        Clin Chest Med. 2004; 25: 257-268
        • Mong J.A.
        • Cusmano D.M.
        Sex differences in sleep: impact of biological sex and sex steroids.
        Philos Trans R Soc Lond B Biol Sci. 2016; 37120150110
        • Redline S.
        • Kirchner H.L.
        • Quan S.F.
        • et al.
        The effects of age, sex, ethnicity, and sleep-disordered breathing on sleep architecture.
        Arch Intern Med. 2004; 164: 406-418
        • Krystal A.D.
        • Edinger J.D
        Measuring sleep quality.
        Sleep Med. 2008; 9: S10-S17
        • Baker F.C.
        • de Zambotti M.
        • Colrain I.M.
        • et al.
        Sleep problems during the menopausal transition: prevalence, impact, and management challenges.
        Nat Sci Sleep. 2018; 10: 73-95
        • de Zambotti M.
        • Goldstone A.
        • Colrain I.M.
        • et al.
        Insomnia disorder in adolescence: diagnosis, impact, and treatment.
        Sleep Med Rev. 2018; 39: 12-24
        • Roberts R.E.
        • Duong H.T.
        The prospective association between sleep deprivation and depression among adolescents.
        Sleep. 2014; 37: 239-244
        • Colrain I.M.
        • Baker F.C.
        Changes in sleep as a function of adolescent development.
        Neuropsychol Rev. 2011; 21: 5-21
        • Hale L.
        • Guan S
        Screen time and sleep among school-aged children and adolescents: a systematic literature review.
        Sleep Med Rev. 2015; 21: 50-58
        • Owens J.A.
        • Mindell J.
        • Baylor A
        Effect of energy drink and caffeinated beverage consumption on sleep, mood, and performance in children and adolescents.
        Nutr Rev. 2014; 72: 65-71
        • Harvey C.J.
        • Gehrman P.
        • Espie C.A
        Who is predisposed to insomnia: a review of familial aggregation, stress-reactivity, personality and coping style.
        Sleep Med Rev. 2014; 18: 237-247
        • Drake C.L.
        • Pillai V.
        • Roth T
        Stress and sleep reactivity: a prospective investigation of the stress-diathesis model of insomnia.
        Sleep. 2014; 37: 1295-1304
        • Brindle R.
        • Ginty A.
        • Phillips A.
        • et al.
        A tale of two mechanisms: a meta-analytic approach toward understanding the autonomic basis of cardiovascular reactivity to acute psychological stress.
        Psychophysiology. 2014; 51: 964-976
        • Bonnet M.H.
        • Arand D.L
        Hyperarousal and insomnia: state of the science.
        Sleep Med Rev. 2010; 14: 9-15
        • de Zambotti M.
        • Trinder J.
        • Silvani A.
        • et al.
        Dynamic coupling between the central and autonomic nervous systems during sleep: a review.
        Neurosci Biobehav Rev. 2018; 90: 84-103
        • de Zambotti M.
        • Cellini N.
        • Baker F.C.
        • et al.
        Nocturnal cardiac autonomic profile in young primary insomniacs and good sleepers.
        Int J Psychophysiol. 2014; 93: 332-339
        • Nano M.M.
        • Fonseca P.
        • Vullings R.
        • et al.
        Measures of cardiovascular autonomic activity in insomnia disorder: a systematic review.
        PLoS One. 2017; 12e0186716
        • Jurysta F.
        • Lanquart J.P.
        • Sputaels V.
        • et al.
        The impact of chronic primary insomnia on the heart rate–EEG variability link.
        Clin Neurophysiol. 2009; 120: 1054-1060
        • de Zambotti M.
        • Javitz H.
        • Franzen P.L.
        • et al.
        Sex- and age-dependent differences in autonomic nervous system functioning in adolescents.
        J Adolesc Health. 2018; 62: 184-190
        • Allgood-Merten B.
        • Lewinsohn P.M.
        • Hops H
        Sex differences and adolescent depression.
        J Abnorm Psychol. 1990; 99: 55-63
        • Ge X.
        • Lorenz F.O.
        • Conger R.D.
        • et al.
        Trajectories of stressful life events and depressive symptoms during adolescence.
        Dev Psychol. 1994; 30: 467-483
        • Hamilton J.L.
        • Stange J.P.
        • Abramson L.Y.
        • et al.
        Stress and the development of cognitive vulnerabilities to depression explain sex differences in depressive symptoms during adolescence.
        Clin Psychol Sci. 2015; 3: 702-714
        • Hankin B.L.
        • Mermelstein R.
        • Roesch L
        Sex differences in adolescent depression: stress exposure and reactivity models.
        Child Dev. 2007; 78: 279-295
        • Drake C.
        • Richardson G.
        • Roehrs T.
        • et al.
        Vulnerability to stress-related sleep disturbance and hyperarousal.
        Sleep. 2004; 27: 285-291
        • Agnew Jr., H.W.
        • Webb W.B.
        • Williams R.L
        The first night effect: an EEG study of sleep.
        Psychophysiology. 1966; 2: 263-266
        • Tamaki M.
        • Bang J.W.
        • Watanabe T.
        • et al.
        Night watch in one brain hemisphere during sleep associated with the first-night effect in humans.
        Curr Biol. 2016; 26: 1190-1194
        • Lorenzo J.L.
        • Barbanoj M.J.
        Variability of sleep parameters across multiple laboratory sessions in healthy young subjects: the "very first night effect".
        Psychophysiology. 2002; 39: 409-413
        • Brown S.A.
        • Brumback T.
        • Tomlinson K.
        • et al.
        The National Consortium on Alcohol and NeuroDevelopment in Adolescence (NCANDA): a multisite study of adolescent development and substance use.
        J Stud Alcohol Drugs. 2015; 76: 895-908
        • Bucholz K.K.
        • Cadoret R.
        • Cloninger C.R.
        • et al.
        A new, semi-structured psychiatric interview for use in genetic linkage studies: a report on the reliability of the SSAGA.
        J Stud Alcohol. 1994; 55: 149-158
        • Petersen A.C.
        • Crockett L.
        • Richards M.
        • et al.
        A self-report measure of pubertal status: reliability, validity, and initial norms.
        J Youth Adolesc. 1988; 17: 117-133
        • Shirtcliff E.A.
        • Dahl R.E.
        • Pollak S.D
        Pubertal development: correspondence between hormonal and physical development.
        Child Dev. 2009; 80: 327-337
        • Radloff L.S.
        The CES-D Scale.
        Appl Psychol Meas. 1977; 1: 385-401
        • Buysse D.
        • Reynolds III, C.
        • Monk T.
        • et al.
        The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research.
        Psychiatry Res. 1989; 28: 193-213
      1. IberC.The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications: American Academy of Sleep Medicine, 2007.

        • Delorme A.
        • Makeig S.
        EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis.
        J Neurosci Methods. 2004; 134: 9-21
        • Willoughby A.R.
        • de Zambotti M.
        • Baker F.C.
        • et al.
        Partial K-Complex recovery following short-term abstinence in individuals with alcohol use disorder.
        Alcohol Clin Exp Res. 2015; 39: 1417-1424
        • Trinder J.
        • Kleiman J.
        • Carrington M.
        • et al.
        Autonomic activity during human sleep as a function of time and sleep stage.
        J Sleep Res. 2001; 10: 253-264
        • Baker F.C.
        • Willoughby A.R.
        • de Zambotti M.
        • et al.
        Age-related differences in sleep architecture and electroencephalogram in adolescents in the National Consortium on alcohol and neurodevelopment in adolescence sample.
        Sleep. 2016; 39: 1429-1439
        • Petersen H.
        • Kecklund G.
        • D'Onofrio P.
        • et al.
        Stress vulnerability and the effects of moderate daily stress on sleep polysomnography and subjective sleepiness.
        J Sleep Res. 2013; 22: 50-57
        • Newell J.
        • Mairesse O.
        • Verbanck P.
        • et al.
        Is a one-night stay in the lab really enough to conclude? First-night effect and night-to-night variability in polysomnographic recordings among different clinical population samples.
        Psychiatry Res. 2012; 200: 795-801
        • Curcio G.
        • Ferrara M.
        • Piergianni A.
        • et al.
        Paradoxes of the first-night effect: a quantitative analysis of antero-posterior EEG topography.
        Clin Neurophysiol. 2004; 115: 1178-1188
        • Scholle S.
        • Scholle H.C.
        • Kemper A.
        • et al.
        First night effect in children and adolescents undergoing polysomnography for sleep-disordered breathing.
        Clin Neurophysiol. 2003; 114: 2138-2145
        • Verhulst S.L.
        • Schrauwen N.
        • De Backer W.A.
        • et al.
        First night effect for polysomnographic data in children and adolescents with suspected sleep disordered breathing.
        Arch Dis Child. 2006; 91: 233-237
        • Dang-Vu T.T.
        • Salimi A.
        • Boucetta S.
        • et al.
        Sleep spindles predict stress-related increases in sleep disturbances.
        Front Hum Neurosci. 2015; 9: 68
        • Perlis M.L.
        • Merica H.
        • Smith M.T.
        • et al.
        Beta EEG activity and insomnia.
        Sleep Med Rev. 2001; 5: 363-374
        • Hall M.
        • Thayer J.F.
        • Germain A.
        • et al.
        Psychological stress is associated with heightened physiological arousal during NREM sleep in primary insomnia.
        Behav Sleep Med. 2007; 5: 178-193
        • de Zambotti M.
        • Sugarbaker D.
        • Trinder J.
        • et al.
        Acute stress alters autonomic modulation during sleep in women approaching menopause.
        Psychoneuroendocrinology. 2016; 66: 1-10
        • Virtanen I.
        • Kalleinen N.
        • Urrila A.S.
        • et al.
        First-night effect on cardiac autonomic function in different female reproductive states.
        J Sleep Res. 2018; 27: 150-158
        • Carrington M.J.
        • Trinder J.
        Blood pressure and heart rate during continuous experimental sleep fragmentation in healthy adults.
        Sleep. 2008; 31: 1701-1712
        • Hall M.
        • Vasko R.
        • Buysse D.
        • et al.
        Acute stress affects heart rate variability during sleep.
        Psychosom Med. 2004; 66: 56-62
        • de Zambotti M.
        • Covassin N.
        • De Min Tona G.
        • et al.
        Sleep onset and cardiovascular activity in primary insomnia.
        J Sleep Res. 2011; 20: 318-325
        • Sheth C.
        • McGlade E.
        • Yurgelun-Todd D
        Chronic stress in adolescents and its neurobiological and psychopathological consequences: an RDoC perspective.
        Chronic Stress (Thousand Oaks). 2017; 1