[en] Fixed sleep schedules with an 8 h time in bed (TIB) are used to ensure participants are well-rested before laboratory studies. However, such schedules may lead to cumulative excess wakefulness in young individuals. Effects on older individuals are unknown. We combine modelling and experimental data to quantify the effects of sleep debt on sleep propensity in healthy younger and older participants. A model of arousal dynamics was fitted to sleep data from 22 young (20–31 y.o.) and 26 older (61–82 y.o.) individuals (25 male) undertaking 10 short sleep–wake cycles during a 40 h napping protocol, following >1 week of fixed 8 h TIB schedules. Homeostatic sleep drive at the study start was varied systematically to identify best fits between observed and predicted sleep profiles for individuals and group averages. Daytime sleep duration was the same on the two days of the protocol within the groups but different between the groups (young: 3.14 ± 0.98 h vs. 3.06 ± 0.75 h, older: 2.60 ± 0.98 h vs. 2.37 ± 0.64 h). The model predicted an initial homeostatic drive of 11.2 ± 3.5% (young) and 10.1 ± 3.5% (older) above well-rested. Individual variability in first-day, but not second-day, sleep patterns was explained by the differences in the initial homeostatic drive for both age groups. Our study suggests that both younger and older participants arrive at the laboratory with cumulative sleep debt, despite 8 h TiB schedules, which dissipates after the first four sleep opportunities on the protocol. This has implications for protocol design and the interpretation of laboratory studies.
Disciplines :
Neurosciences & behavior
Author, co-author :
de Haan, Stella ; University of Liège > GIGA-CRC Human Imaging, Sleep and Chronobiology Laboratory
Dourte, Marine ; University of Liège > GIGA-CRC Human Imaging, Sleep and Chronobiology Laboratory ; University of Liège > Faculty of Psychology and Educational Sciences, Psychology and Neurosciences of Cognition Research Unit (PsyNCog)
Deantoni, Michele ; University of Liège > GIGA-CRC Human Imaging, Sleep and Chronobiology Laboratory
Reyt, Mathilde ; University of Liège > GIGA-CRC Human Imaging, Sleep and Chronobiology Laboratory ; University of Liège > Faculty of Psychology and Educational Sciences, Psychology and Neurosciences of Cognition Research Unit (PsyNCog)
Baillet, Marion ; University of Liège > GIGA-CRC Human Imaging, Sleep and Chronobiology Laboratory ; Massachusetts General Hospital and Harvard Medical School > Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology
Berthomier, Christian ; Physip S.A., 6 Rue Gobert, 75011 Paris, France
Muto, Vincenzo ; University of Liège > GIGA-CRC Human Imaging, Sleep and Chronobiology Laboratory
Hammad, Grégory ; University of Liège > GIGA-CRC Human Imaging, Sleep and Chronobiology Laboratory ; University of Surrey > Sleep and Chronobiology Laboratory
Cajochen, Christian ; Centre for Chronobiology, Psychiatric Hospital of the University of Basel, 4002 Basel, Switzerland ; Research Cluster Molecular and Cognitive Neurosciences, University of Basel, 4055 Basel, Switzerland
Reichert, Carolin F.; Centre for Chronobiology, Psychiatric Hospital of the University of Basel, 4002 Basel, Switzerland ; Research Cluster Molecular and Cognitive Neurosciences, University of Basel, 4055 Basel, Switzerland
Maire, Micheline; Centre for Chronobiology, Psychiatric Hospital of the University of Basel, 4002 Basel, Switzerland
Schmidt, Christina ; University of Liège > GIGA-CRC Human Imaging, Sleep and Chronobiology Laboratory ; University of Liège > Faculty of Psychology and Educational Sciences, Psychology and Neurosciences of Cognition Research Unit (PsyNCog)
Postnova, Svetlana; Circadian Physics Group, School of Physics, University of Sydney, Sydney, NSW 2006, Australia
H2020 - 757763 - COGNAP - To nap or not to nap? Why napping habits interfere with cognitive fitness in ageing
Funders :
ERC - European Research Council F.R.S.-FNRS - Fonds de la Recherche Scientifique SNSF - Swiss National Science Foundation ARC - Australian Research Council European Union
Funding text :
This study was supported by the European Research Council (ERC, ERCStG-COGNAP) under the European Union’s Horizon 2020 research and innovation programme (grant agreement #757763). This study was also supported by the Fonds de la Recherche Scientifique—FNRS (grant agreement #T.0220.20) and the Swiss National Foundation (grant agreement #310030_130689), the L. & Th. La Roche-Stiftung, and the Niklaus und Bertha BurckhardtBürgin-Stiftung. C.S. is a research associate and S.d.H., M.D. (Marine Dourte) and M.D. (Michele Deantoni) received PhD grants from the Fonds de la Recherche Scientifique—FNRS, Belgium. C.F.R. is supported by the the Gertrud Thalmann funds of the Psychiatric University Clinics of Basel, Switzerland. C.C. is a research professor funded by the Swiss National Foundation. S.P. and C.S. acknowledge the funding from the Australian Research Council (DP230101113).
Borbely A.A. A Two Process Model of Sleep Regulation Hum. Neurobiol. 1982 1 195 204
Daan S. Beersma D.G. Borbély A.A. Timing of Human Sleep: Recovery Process Gated by a Circadian Pacemaker Am. J. Physiol. 1984 246 R161 R183 10.1152/ajpregu.1984.246.2.R161 6696142
Edgar D. Dement W. Fuller C. Effect of SCN Lesions on Sleep in Squirrel Monkeys: Evidence for Opponent Processes in Sleep-Wake Regulation J. Neurosci. 1993 13 1065 1079 10.1523/JNEUROSCI.13-03-01065.1993
Borbély A.A. Achermann P. Chapter 33—Sleep Homeostasis and Models of Sleep Regulation Principles and Practice of Sleep Medicine (Fourth Edition) Kryger M.H. Roth T. Dement W.C. W.B. Saunders Philadelphia, PA, USA 2005 405 417 978-0-7216-0797-9
Dijk D.J. Czeisler C.A. Paradoxical Timing of the Circadian Rhythm of Sleep Propensity Serves to Consolidate Sleep and Wakefulness in Humans Neurosci. Lett. 1994 166 63 68 10.1016/0304-3940(94)90841-9
Dijk D.J. Duffy J.F. Riel E. Shanahan T.L. Czeisler C.A. Ageing and the Circadian and Homeostatic Regulation of Human Sleep during Forced Desynchrony of Rest, Melatonin and Temperature Rhythms J. Physiol. 1999 516 Pt 2 611 627 10.1111/j.1469-7793.1999.0611v.x
Li J. Vitiello M.V. Gooneratne N.S. Sleep in Normal Aging Sleep Med. Clin. 2018 13 1 11 10.1016/j.jsmc.2017.09.001 29412976
Vitiello M.V. Sleep in Normal Aging Sleep Med. Clin. 2006 1 171 176 10.1016/j.jsmc.2006.04.007
Duffy J.F. Dijk D.J. Getting Through to Circadian Oscillators: Why Use Constant Routines? J. Biol. Rhythms 2002 17 4 13 10.1177/074873002129002294
McMahon W.R. Ftouni S. Phillips A.J.K. Beatty C. Lockley S.W. Rajaratnam S.M.W. Maruff P. Drummond S.P.A. Anderson C. The Impact of Structured Sleep Schedules Prior to an In-Laboratory Study: Individual Differences in Sleep and Circadian Timing PLoS ONE 2020 15 e0236566 10.1371/journal.pone.0236566
Buysse D.J. Monk T.H. Carrier J. Begley A. Circadian Patterns of Sleep, Sleepiness, and Performance in Older and Younger Adults Sleep 2005 28 1365 1376 10.1093/sleep/28.11.1365
Deantoni M. Reyt M. Berthomier C. Muto V. Hammad G. De Haan S. Dourte M. Taillard J. Lambot E. Cajochen C. et al. Association between Circadian Sleep Regulation and Cortical Gyrification in Young and Older Adults Sleep 2023 46 zsad094 10.1093/sleep/zsad094 37010079
Maire M. Reichert C.F. Gabel V. Viola A.U. Phillips C. Krebs J. Scheffler K. Klarhöfer M. Strobel W. Cajochen C. et al. Fighting Sleep at Night: Brain Correlates and Vulnerability to Sleep Loss Ann. Neurol. 2015 78 235 247 10.1002/ana.24434 25940842
Münch M. Knoblauch V. Blatter K. Schröder C. Schnitzler C. Kräuchi K. Wirz-Justice A. Cajochen C. Age-Related Attenuation of the Evening Circadian Arousal Signal in Humans Neurobiol. Aging 2005 26 1307 1319 10.1016/j.neurobiolaging.2005.03.004
Abel J.H. Lecamwasam K. St Hilaire M.A. Klerman E.B. Recent Advances in Modeling Sleep: From the Clinic to Society and Disease Curr. Opin. Physiol. 2020 15 37 46 10.1016/j.cophys.2019.12.001 34485783
Postnova S. Sleep Modelling across Physiological Levels Clocks Sleep 2019 1 166 184 10.3390/clockssleep1010015 33089162
Skeldon A.C. Dijk D.-J. Derks G. Mathematical Models for Sleep-Wake Dynamics: Comparison of the Two-Process Model and a Mutual Inhibition Neuronal Model PLoS ONE 2014 9 e103877 10.1371/journal.pone.0103877
Borbély A.A. Achermann P. Sleep Homeostasis and Models of Sleep Regulation J. Biol. Rhythms 1999 14 557 568 10.1177/074873099129000894
Behn C.D. Brown E.N. Scammell T.E. Kopell N. A Mathematical Model of Network Dynamics Governing Sleep-Wake Patterns in Mice J. Neurophysiol. 2007 97 3828 3840 10.1152/jn.01184.2006
Booth V. Diniz Behn C.G. Physiologically-Based Modeling of Sleep–Wake Regulatory Networks Math. Biosci. 2014 250 54 68 10.1016/j.mbs.2014.01.012 24530893
Phillips A.J.K. Czeisler C.A. Klerman E.B. Revisiting Spontaneous Internal Desynchrony Using a Quantitative Model of Sleep Physiology J. Biol. Rhythms 2011 26 441 453 10.1177/0748730411414163
Phillips A.J.K. Robinson P.A. A Quantitative Model of Sleep-Wake Dynamics Based on the Physiology of the Brainstem Ascending Arousal System J. Biol. Rhythms 2007 22 167 179 10.1177/0748730406297512 17440218
Postnova S. Lockley S.W. Robinson P.A. Sleep Propensity under Forced Desynchrony in a Model of Arousal State Dynamics J. Biol. Rhythms 2016 31 498 508 10.1177/0748730416658806 27432116
Puckeridge M. Fulcher B.D. Phillips A.J.K. Robinson P.A. Incorporation of Caffeine into a Quantitative Model of Fatigue and Sleep J. Theor. Biol. 2011 273 44 54 10.1016/j.jtbi.2010.12.018 21176782
Rempe M.J. Best J. Terman D. A Mathematical Model of the Sleep/Wake Cycle J. Math. Biol. 2010 60 615 644 10.1007/s00285-009-0276-5 19557415
Knock S.A. Magee M. Stone J.E. Ganesan S. Mulhall M.D. Lockley S.W. Howard M.E. Rajaratnam S.M.W. Sletten T.L. Postnova S. Prediction of Shiftworker Alertness, Sleep, and Circadian Phase Using a Model of Arousal Dynamics Constrained by Shift Schedules and Light Exposure Sleep 2021 44 zsab146 10.1093/sleep/zsab146 34111278
Fulcher B.D. Phillips A.J.K. Robinson P.A. Quantitative Physiologically Based Modeling of Subjective Fatigue during Sleep Deprivation J. Theor. Biol. 2010 264 407 419 10.1016/j.jtbi.2010.02.028
Phillips A.J.K. Robinson P.A. Sleep Deprivation in a Quantitative Physiologically Based Model of the Ascending Arousal System J. Theor. Biol. 2008 255 413 423 10.1016/j.jtbi.2008.08.022 18805427
Skeldon A.C. Derks G. Dijk D.-J. Modelling Changes in Sleep Timing and Duration across the Lifespan: Changes in Circadian Rhythmicity or Sleep Homeostasis? Sleep Med. Rev. 2016 28 96 107 10.1016/j.smrv.2015.05.011 26545247
Van Dongen H.P.A. Maislin G. Mullington J.M. Dinges D.F. The Cumulative Cost of Additional Wakefulness: Dose-Response Effects on Neurobehavioral Functions and Sleep Physiology From Chronic Sleep Restriction and Total Sleep Deprivation Sleep 2003 26 117 126 10.1093/sleep/26.2.117
Piltz S.H. Diniz Behn C.G. Booth V. Habitual Sleep Duration Affects Recovery from Acute Sleep Deprivation: A Modeling Study J. Theor. Biol. 2020 504 110401 10.1016/j.jtbi.2020.110401 32663506
Phillips A.J.K. Chen P.Y. Robinson P.A. Probing the Mechanisms of Chronotype Using Quantitative Modeling J. Biol. Rhythms 2010 25 217 227 10.1177/0748730410369208
Phillips A.J.K. Robinson P.A. Kedziora D.J. Abeysuriya R.G. Mammalian Sleep Dynamics: How Diverse Features Arise from a Common Physiological Framework PLoS Comput. Biol. 2010 6 e1000826 10.1371/journal.pcbi.1000826 20585613
Roenneberg T. Chronobiology: The Human Sleep Project Nature 2013 498 10.1038/498427a 23803826
Rajaratnam S.M.W. Middleton B. Stone B.M. Arendt J. Dijk D.-J. Melatonin Advances the Circadian Timing of EEG Sleep and Directly Facilitates Sleep without Altering Its Duration in Extended Sleep Opportunities in Humans J. Physiol. 2004 561 339 351 10.1113/jphysiol.2004.073742
Wehr T.A. Moul D.E. Barbato G. Giesen H.A. Seidel J.A. Barker C. Bender C. Conservation of Photoperiod-Responsive Mechanisms in Humans Am. J. Physiol.-Regul. Integr. Comp. Physiol. 1993 265 R846 R857 10.1152/ajpregu.1993.265.4.R846 8238456
Carskadon M.A. Brown E.D. Dement W.C. Sleep Fragmentation in the Elderly: Relationship to Daytime Sleep Tendency Neurobiol. Aging 1982 3 321 327 10.1016/0197-4580(82)90020-3 7170049
Klerman E.B. Dijk D.-J. Age-Related Reduction in the Maximal Capacity for Sleep--Implications for Insomnia Curr. Biol. CB 2008 18 1118 1123 10.1016/j.cub.2008.06.047
Mander B.A. Winer J.R. Walker M.P. Sleep and Human Aging Neuron 2017 94 19 36 10.1016/j.neuron.2017.02.004
Okamoto-Mizuno K. Mizuno K. Effects of Thermal Environment on Sleep and Circadian Rhythm J. Physiol. Anthropol. 2012 31 14 10.1186/1880-6805-31-14 22738673
Johns M.W. Sleep Propensity Varies with Behaviour and the Situation in Which It Is Measured: The Concept of Somnificity J. Sleep Res. 2002 11 61 67 10.1046/j.1365-2869.2002.00274.x 11869428
Rial R.V. Canellas F. Gamundí A. Akaârir M. Nicolau M.C. Pleasure: The Missing Link in the Regulation of Sleep Neurosci. Biobehav. Rev. 2018 88 141 154 10.1016/j.neubiorev.2018.03.012
Reichert C.F. Maire M. Gabel V. Viola A.U. Kolodyazhniy V. Strobel W. Götz T. Bachmann V. Landolt H.-P. Cajochen C. et al. Insights into Behavioral Vulnerability to Differential Sleep Pressure and Circadian Phase from a Functional ADA Polymorphism J. Biol. Rhythms 2014 29 119 130 10.1177/0748730414524898
Reyt M. Deantoni M. Baillet M. Lesoinne A. Laloux S. Lambot E. Demeuse J. Calaprice C. LeGoff C. Collette F. et al. Daytime Rest: Association with 24-h Rest-Activity Cycles, Circadian Timing and Cognition in Older Adults J. Pineal Res. 2022 73 e12820 10.1111/jpi.12820 35906192
Van Someren E.J.W. Nagtegaal E. Improving Melatonin Circadian Phase Estimates Sleep Med. 2007 8 590 601 10.1016/j.sleep.2007.03.012 17493871
Berry R.B. Gamaldo C.E. Harding S.M. Brooks R. Lloyd R.M. Vaughn B.V. Marcus C.L. AASM Scoring Manual Version 2.2 Updates: New Chapters for Scoring Infant Sleep Staging and Home Sleep Apnea Testing J. Clin. Sleep Med. JCSM 2015 11 1253 1254 10.5664/jcsm.5176 26446251
Berthomier C. Drouot X. Herman-Stoïca M. Berthomier P. Prado J. Bokar-Thire D. Benoit O. Mattout J. d’Ortho M.-P. Automatic Analysis of Single-Channel Sleep EEG: Validation in Healthy Individuals Sleep 2007 30 1587 1595 10.1093/sleep/30.11.1587
Berthomier C. Muto V. Schmidt C. Vandewalle G. Jaspar M. Devillers J. Gaggioni G. Chellappa S.L. Meyer C. Phillips C. et al. Exploring Scoring Methods for Research Studies: Accuracy and Variability of Visual and Automated Sleep Scoring J. Sleep Res. 2020 29 e12994 10.1111/jsr.12994
Chylinski D. Berthomier C. Lambot E. Frenette S. Brandewinder M. Carrier J. Vandewalle G. Muto V. Variability of Sleep Stage Scoring in Late Midlife and Early Old Age J. Sleep Res. 2022 31 e13424 10.1111/jsr.13424 34169604
Deantoni M. Reyt M. Baillet M. Dourte M. De Haan S. Lesoinne A. Vandewalle G. Maquet P. Berthomier C. Muto V. et al. Napping and Circadian Sleep-Wake Regulation during Healthy Aging Sleep 2023 zsad287 10.1093/sleep/zsad287 37943833
Saper C.B. Scammell T.E. Lu J. Hypothalamic Regulation of Sleep and Circadian Rhythms Nature 2005 437 1257 1263 10.1038/nature04284 16251950
Abeysuriya R.G. Lockley S.W. Robinson P.A. Postnova S. A Unified Model of Melatonin, 6-sulfatoxymelatonin, and Sleep Dynamics J. Pineal Res. 2018 64 10.1111/jpi.12474 29437238
