Rapid Eye Movement Sleep, Sleep Continuity and Slow Wave Sleep as Predictors of Cognition, Mood, and Subjective Sleep Quality in Healthy Men and Women, Aged 20–84 Years

Sleep and its sub-states are assumed to be important for brain function across the lifespan but which aspects of sleep associate with various aspects of cognition, mood and self-reported sleep quality has not yet been established in detail. Sleep was quantified by polysomnography, quantitative Electroencephalogram (EEG) analysis and self-report in 206 healthy men and women, aged 20–84 years, without sleep complaints. Waking brain function was quantified by five assessments scheduled across the day covering objectively assessed performance across cognitive domains including sustained attention and arousal, decision and response time, motor and sequence control, working memory, and executive function as well as self-reports of alertness, mood and affect. Controlled for age and sex, self-reported sleep quality was negatively associated with number of awakenings and positively associated with the duration of Rapid Eye Movement (REM) sleep, but no significant associations with Slow Wave Sleep (SWS) measures were observed. Controlling only for age showed that associations between objective and subjective sleep quality were much stronger in women than in men. Analysis of 51 performance measures demonstrated that, after controlling for age and sex, fewer awakenings and more REM sleep were associated significantly with better performance on the Goal Neglect task, which is a test of executive function. Factor analysis of the individual performance measures identified four latent variables labeled Mood/Arousal, Response Time, Accuracy, and Visual Perceptual Sensitivity. Whereas Mood/Arousal improved with age, Response Times became slower, while Accuracy and Visual perceptual sensitivity showed little change with age. After controlling for sex and age, nominally significant association between sleep and factor scores were observed such that Response Times were faster with more SWS, and Accuracy was reduced where individuals woke more often or had less REM sleep. These data identify a positive contribution of SWS to processing speed and in particular highlight the importance of sleep continuity and REM sleep for subjective sleep quality and performance accuracy across the adult lifespan. These findings warrant further investigation of the contribution of sleep continuity and REM sleep to brain function.

[1]  Anna C. Schapiro,et al.  Individual Differences in Frequency and Topography of Slow and Fast Sleep Spindles , 2017, bioRxiv.

[2]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[3]  Cassandra J. Lowe,et al.  The neurocognitive consequences of sleep restriction: A meta-analytic review , 2017, Neuroscience & Biobehavioral Reviews.

[4]  F. Feppon,et al.  Partial , 2020, Definitions.

[5]  Y. Benjamini,et al.  THE CONTROL OF THE FALSE DISCOVERY RATE IN MULTIPLE TESTING UNDER DEPENDENCY , 2001 .

[6]  S. Redline,et al.  Correlates of sleep quality in midlife and beyond: a machine learning analysis. , 2017, Sleep medicine.

[7]  S. Redline,et al.  Relationships between sleep stages and changes in cognitive function in older men: the MrOS Sleep Study. , 2015, Sleep.

[8]  Daniel J Buysse,et al.  The Pittsburgh sleep quality index: A new instrument for psychiatric practice and research , 1989, Psychiatry Research.

[9]  A. R. Gilpin Table for Conversion of Kendall'S Tau to Spearman'S Rho Within the Context of Measures of Magnitude of Effect for Meta-Analysis , 1993 .

[10]  P. Markopoulos,et al.  Determinants of perceived sleep quality in normal sleepers , 2019, Behavioral sleep medicine.

[11]  C. Lord,et al.  Sex differences in age-related changes in the sleep-wake cycle , 2017, Frontiers in Neuroendocrinology.

[12]  P. Colombo,et al.  Lexical priming deficits as a function of age. , 1990, Behavioral neuroscience.

[13]  C. Alessi,et al.  Report and Research Agenda of the American Geriatrics Society and National Institute on Aging Bedside‐to‐Bench Conference on Sleep, Circadian Rhythms, and Aging: New Avenues for Improving Brain Health, Physical Health, and Functioning , 2016, Journal of the American Geriatrics Society.

[14]  A J Parkin,et al.  Recollective experience, normal aging, and frontal dysfunction. , 1992, Psychology and aging.

[15]  Sudha Seshadri,et al.  Sleep architecture and the risk of incident dementia in the community , 2017, Neurology.

[16]  Christopher N. Kaufmann,et al.  Paradoxical Trend for Improvement in Mental Health With Aging: A Community-Based Study of 1,546 Adults Aged 21-100 Years. , 2016, The Journal of clinical psychiatry.

[17]  Sara J. Aton,et al.  Form and Function of Sleep Spindles across the Lifespan , 2016, Neural plasticity.

[18]  D. Sheehan,et al.  The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. , 1998, The Journal of clinical psychiatry.

[19]  T. Åkerstedt,et al.  The relation between polysomnography and subjective sleep and its dependence on age – poor sleep may become good sleep , 2016, Journal of sleep research.

[20]  I Feinberg,et al.  EEG sleep patterns as a function of normal and pathological aging in man. , 1967, Journal of psychiatric research.

[21]  Yongfei Tan,et al.  Sleep disturbance in mild cognitive impairment: a systematic review of objective measures , 2017, Neurological Sciences.

[22]  G. Plazzi,et al.  REM Sleep EEG Instability in REM Sleep Behavior Disorder and Clonazepam Effects , 2017, Sleep.

[23]  Todd Gardner The Slow Wave , 2001 .

[24]  E. Wolpert A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. , 1969 .

[25]  Jie Shi,et al.  Sleep disturbances increase the risk of dementia: A systematic review and meta-analysis. , 2017, Sleep medicine reviews.

[26]  D. Dinges,et al.  Neurocognitive consequences of sleep deprivation. , 2005, Seminars in neurology.

[27]  C. Harada,et al.  Normal cognitive aging. , 2013, Clinics in geriatric medicine.

[28]  Sara J. Aton,et al.  Linking Network Activity to Synaptic Plasticity during Sleep: Hypotheses and Recent Data , 2017, Front. Neural Circuits.

[29]  J. Born,et al.  System Consolidation During Sleep – A Common Principle Underlying Psychological and Immunological Memory Formation , 2015, Trends in Neurosciences.

[30]  M. Bonnet The effect of sleep fragmentation on sleep and performance in younger and older subjects , 1989, Neurobiology of Aging.

[31]  M. Delgado-Rodríguez,et al.  Systematic review and meta-analysis. , 2017, Medicina intensiva.

[32]  D. Dijk,et al.  Dynamics of electroencephalographic sleep spindles and slow wave activity in men: effect of sleep deprivation , 1993, Brain Research.

[33]  J. Rhudy,et al.  Partial Sleep Deprivation Attenuates the Positive Affective System: Effects Across Multiple Measurement Modalities , 2017, Sleep.

[34]  M. Fabiani It was the best of times, it was the worst of times: a psychophysiologist's view of cognitive aging. , 2012, Psychophysiology.

[35]  Sarah G. Woo,et al.  Role of sleep continuity and total sleep time in executive function across the adult lifespan. , 2014, Psychology and aging.

[36]  D. Dijk,et al.  Dissociating effects of global SWS disruption and healthy aging on waking performance and daytime sleepiness. , 2014, Sleep.

[37]  G. Tononi,et al.  Sleep and the Price of Plasticity: From Synaptic and Cellular Homeostasis to Memory Consolidation and Integration , 2014, Neuron.

[38]  Emma L. Arbon,et al.  Effects of Partial and Acute Total Sleep Deprivation on Performance across Cognitive Domains, Individuals and Circadian Phase , 2012, PloS one.

[39]  M. Irwin,et al.  Sleep Health: Reciprocal Regulation of Sleep and Innate Immunity , 2017, Neuropsychopharmacology.

[40]  D. Dijk,et al.  Self-reported sleep duration and cognitive performance in older adults: a systematic review and meta-analysis. , 2016, Sleep medicine.

[41]  T. Åkerstedt,et al.  Association Between Sleep Characteristics and Incident Dementia Accounting for Baseline Cognitive Status: A Prospective Population-Based Study , 2017, The journals of gerontology. Series A, Biological sciences and medical sciences.

[42]  T. Åkerstedt,et al.  The meaning of good sleep: a longitudinal study of polysomnography and subjective sleep quality , 1994, Journal of sleep research.

[43]  T. Åkerstedt,et al.  Normative data on the diurnal pattern of the Karolinska Sleepiness Scale ratings and its relation to age, sex, work, stress, sleep quality and sickness absence/illness in a large sample of daytime workers , 2017, Journal of sleep research.

[44]  Gérard Waeber,et al.  Age and gender variations of sleep in subjects without sleep disorders , 2015, Annals of medicine.

[45]  M. Preisig,et al.  Sleep characteristics and cognitive impairment in the general population , 2017, Neurology.

[46]  Michael K. Scullin,et al.  Sleep, Cognition, and Normal Aging , 2015, Perspectives on psychological science : a journal of the Association for Psychological Science.

[47]  E. Mohammadi,et al.  Barriers and facilitators related to the implementation of a physiological track and trigger system: A systematic review of the qualitative evidence , 2017, International journal for quality in health care : journal of the International Society for Quality in Health Care.

[48]  A. Newell,et al.  Technology in cognitive rehabilitation: introduction , 2004 .

[49]  D. Dijk,et al.  Age-related reduction in daytime sleep propensity and nocturnal slow wave sleep. , 2010, Sleep.

[50]  T. Lai,et al.  The prevalence of neuropsychiatric symptoms in Alzheimer's disease: Systematic review and meta-analysis. , 2016, Journal of affective disorders.

[51]  R. Spencer,et al.  Age-related changes in the cognitive function of sleep. , 2011, Progress in brain research.

[52]  A. Steptoe,et al.  Positive affect and sleep: A systematic review. , 2017, Sleep medicine reviews.

[53]  D. Dijk,et al.  Enhanced slow wave sleep and improved sleep maintenance after gaboxadol administration during seven nights of exposure to a traffic noise model of transient insomnia , 2012, Journal of psychopharmacology.

[54]  R. Ratcliff,et al.  The effects of aging on the speed-accuracy compromise: Boundary optimality in the diffusion model. , 2010, Psychology and aging.

[55]  A. Mandell,et al.  Stress in Subjects Undergoing Sleep Deprivation , 1966, Psychosomatic medicine.

[56]  C. Guilleminault,et al.  Meta-analysis of quantitative sleep parameters from childhood to old age in healthy individuals: developing normative sleep values across the human lifespan. , 2004, Sleep.

[57]  B. Feige,et al.  Sleep and mental disorders: A meta-analysis of polysomnographic research. , 2016, Psychological bulletin.

[58]  V. R. Carlson,et al.  Changes in EEG Amplitude During Sleep with Age , 1977 .

[59]  Paul Dolan,et al.  More years, less yawns: fresh evidence on tiredness by age and other factors. , 2015, The journals of gerontology. Series B, Psychological sciences and social sciences.

[60]  S. Siegel,et al.  Nonparametric Statistics for the Behavioral Sciences , 2022, The SAGE Encyclopedia of Research Design.

[61]  J. Groeger,et al.  Slow wave sleep enhancement with gaboxadol reduces daytime sleepiness during sleep restriction. , 2008, Sleep.

[62]  Kristine Yaffe,et al.  Connections between sleep and cognition in older adults , 2014, The Lancet Neurology.

[63]  Mark S. Seidenberg,et al.  Changes in cerebral functioning associated with normal aging. , 1989, Journal of clinical and experimental neuropsychology.

[64]  A. Avidan,et al.  Sleep, Cognition and Dementia , 2015, Current Psychiatry Reports.

[65]  Jean-François Gagnon,et al.  Sleep spindles and rapid eye movement sleep as predictors of next morning cognitive performance in healthy middle‐aged and older participants , 2014, Journal of sleep research.

[66]  C. Reynolds,et al.  Age-related differences and change in positive and negative affect over 23 years. , 2001, Journal of personality and social psychology.

[67]  John A Groeger,et al.  Sex differences in the circadian regulation of sleep and waking cognition in humans , 2016, Proceedings of the National Academy of Sciences.

[68]  Jamie M. Zeitzer,et al.  When a gold standard isn’t so golden: Lack of prediction of subjective sleep quality from sleep polysomnography , 2017, Biological Psychology.

[69]  Sleep loss in aging. , 1989, Clinics in geriatric medicine.

[70]  J. Walsh,et al.  Sleep: a health imperative. , 2012, Sleep.

[71]  T. Åkerstedt,et al.  Age affects sleep microstructure more than sleep macrostructure , 2017, Journal of sleep research.

[72]  Daniel J. R. Christensen,et al.  Sleep Drives Metabolite Clearance from the Adult Brain , 2013, Science.

[73]  P. Bright,et al.  The National Adult Reading Test: restandardisation against the Wechsler Adult Intelligence Scale—Fourth edition , 2018, Neuropsychological rehabilitation.

[74]  D. Dijk,et al.  Age-related increase in awakenings: impaired consolidation of nonREM sleep at all circadian phases. , 2001, Sleep.