[en] Sleep is regulated in a time-of-day dependent manner and profits working memory. However, the impact of the circadian timing system as well as contributions of specific sleep properties to this beneficial effect remains largely unexplored. Moreover, it is unclear to which extent inter-individual differences in sleep-wake regulation depend on circadian phase and modulate the association between sleep and working memory. Here, sleep electroencephalography (EEG) was recorded during a 40-h multiple nap protocol, and working memory performance was assessed by the n-back task 10 times before and after each scheduled nap sleep episode. Twenty-four participants were genotyped regarding a functional polymorphism in adenosine deaminase (rs73598374, 12 G/A-, 12 G/G-allele carriers), previously associated with differences in sleep-wake regulation. Our results indicate that genotype-driven differences in sleep depend on circadian phase: heterozygous participants were awake longer and slept less at the end of the biological day, while they exhibited longer non rapid eye movement (NREM) sleep and slow wave sleep concomitant with reduced power between 8-16 Hz at the end of the biological night. Slow wave sleep and NREM sleep delta EEG activity covaried positively with overall working memory performance, independent of circadian phase and genotype. Moreover, REM sleep duration benefitted working memory particularly when occurring in the early morning hours and specifically in heterozygous individuals. Even though based on a small sample size and thus requiring replication, our results suggest genotype-dependent differences in circadian sleep regulation. They further indicate that REM sleep, being under strong circadian control, boosts working memory performance according to genotype in a time-of-day dependent manner. Finally, our data provide first evidence that slow wave sleep and NREM sleep delta activity, majorly regulated by sleep homeostatic mechanisms, is linked to working memory independent of the timing of the sleep episode within the 24-h cycle.
Disciplines :
Neurosciences & behavior
Author, co-author :
Reichert, Carolin F.
Maire, Micheline
Gabel, Virginie
Hofstetter, Marcel
Viola, Antoine U.
Kolodyazhniy, Vitaliy
Strobel, Werner
Goetz, Thomas
Bachmann, Valerie
Landolt, Hans-Peter
Cajochen, Christian
Schmidt, Christina ; Université de Liège > Département de Psychologie : cognition et comportement > Neuropsychologie
Language :
English
Title :
The circadian regulation of sleep: impact of a functional ADA-polymorphism and its association to working memory improvements.
Publication date :
2014
Journal title :
PLoS ONE
eISSN :
1932-6203
Publisher :
Public Library of Science, United States - California
Dijk DJ, Czeisler CA (1994) Paradoxical timing of the circadian rhythm of sleep propensity serves to consolidate sleep and wakefulness in humans. Neurosci Lett 166: 63-68.
Dijk DJ, Shanahan TL, Duffy JF, Ronda JM, Czeisler CA (1997) Variation of electroencephalographic activity during non-rapid eye movement and rapid eye movement sleep with phase of circadian melatonin rhythm in humans. J Physiol 505 (Pt 3): 851-858.
Edgar DM, Dement WC, Fuller CA (1993) Effect of SCN lesions on sleep in squirrel monkeys: evidence for opponent processes in sleep-wake regulation. J Neurosci 13: 1065-1079.
Dijk DJ, Edgar DM (1999) Circadian and homoestatic control of wakefulness and sleep. In: Turek FW, Zee PC, editors. Regulation of Sleep and Wakefulness. New York, NY: Marcel Dekker, Inc. pp. 111-147.
Strogatz SH, Kronauer RE, Czeisler CA (1987) Circadian pacemaker interferes with sleep onset at specific times each day: role in insomnia. Am J Physiol 253: R172-178.
Dijk DJ, Czeisler CA (1995) Contribution of the circadian pacemaker and the sleep homeostat to sleep propensity, sleep structure, electroencephalographic slow waves, and sleep spindle activity in humans. J Neurosci 15: 3526-3538.
Landolt HP (2011) Genetic determination of sleep EEG profiles in healthy humans. Prog Brain Res 193: 51-61.
Maire M, Reichert C, Schmidt C (2013) Current and Future Perspectives in Sleep and Circadian Rhythms Research. Journal of Cognitive and Behavioral Psychotherapies.
Bachmann V, Klaus F, Bodenmann S, Schafer N, Brugger P, et al. (2012) Functional ADA Polymorphism Increases Sleep Depth and Reduces Vigilant Attention in Humans. Cerebral Cortex 22: 962-970.
Battistuzzi G, Iudicone P, Santolamazza P, Petrucci R (1981) Activity of adenosine deaminase allelic forms in intact erythrocytes and in lymphocytes. Ann Hum Genet 45: 15-19.
Landolt HP (2008) Sleep homeostasis: a role for adenosine in humans? Biochem Pharmacol 75: 2070-2079.
Retey JV, Adam M, Honegger E, Khatami R, Luhmann UF, et al. (2005) A functional genetic variation of adenosine deaminase affects the duration and intensity of deep sleep in humans. Proc Natl Acad Sci U S A 102: 15676-15681.
Riksen NP, Franke B, van den Broek P, Naber M, Smits P, et al. (2008) The 22G>A polymorphism in the adenosine deaminase gene impairs catalytic function but does not affect reactive hyperaemia in humans in vivo. Pharmacogenet Genomics 18: 843-846.
Porkka-Heiskanen T, Kalinchuk AV (2011) Adenosine, energy metabolism and sleep homeostasis. Sleep Med Rev 15: 123-135.
Mazzotti DR, Guindalini C, de Souza AA, Sato JR, Santos-Silva R, et al. (2012) Adenosine deaminase polymorphism affects sleep EEG spectral power in a large epidemiological sample. PLoS ONE 7: e44154.
Mazzotti DR, Guindalini C, Pellegrino R, Barrueco KF, Santos-Silva R, et al. (2011) Effects of the adenosine deaminase polymorphism and caffeine intake on sleep parameters in a large population sample. Sleep 34: 399-402.
Reichert CF, Maire M, Gabel V, Viola AU, Kolodyazhniy V, et al. (2014) Insights into Behavioral Vulnerability to Differential Sleep Pressure and Circadian Phase from a Functional ADA Polymorphism. J Biol Rhythms 92: 119-130.
Shochat T, Luboshitzky R, Lavie P (1997) Nocturnal melatonin onset is phase locked to the primary sleep gate. Am J Physiol 273: R364-370.
Dijk DJ, Duffy JF, Czeisler CA (1992) Circadian and sleep/wake dependent aspects of subjective alertness and cognitive performance. J Sleep Res 1: 112-117.
Wyatt JK, Ritz-De Cecco A, Czeisler CA, Dijk DJ (1999) Circadian temperature and melatonin rhythms, sleep, and neurobehavioral function in humans living on a 20-h day. Am J Physiol 277: R1152-1163.
Jaeggi SM, Buschkuehl M, Jonides J, Perrig WJ (2008) Improving fluid intelligence with training on working memory. Proc Natl Acad Sci U S A 105: 6829-6833.
Kuriyama K, Honma M, Shimazaki M, Horie M, Yoshiike T, et al. (2011) An N-methyl-D-aspartate receptor agonist facilitates sleep-independent synaptic plasticity associated with working memory capacity enhancement. Sci Rep 1: 127.
Kuriyama K, Mishima K, Suzuki H, Aritake S, Uchiyama M (2008) Sleep accelerates the improvement in working memory performance. J Neurosci 28: 10145-10150.
Cajochen C, Knoblauch V, Wirz-Justice A, Krauchi K, Graw P, et al. (2004) Circadian modulation of sequence learning under high and low sleep pressure conditions. Behav Brain Res 151: 167-176.
Wright KP Jr, Hull JT, Hughes RJ, Ronda JM, Czeisler CA (2006) Sleep and wakefulness out of phase with internal biological time impairs learning in humans. J Cogn Neurosci 18: 508-521.
Cajochen C, Knoblauch V, Krauchi K, Renz C, Wirz-Justice A (2001) Dynamics of frontal EEG activity, sleepiness and body temperature under high and low sleep pressure. Neuroreport 12: 2277-2281.
Munch M, Knoblauch V, Blatter K, Schroder C, Schnitzler C, et al. (2005) Age-related attenuation of the evening circadian arousal signal in humans. Neurobiol Aging 26: 1307-1319.
Sagaspe P, Taillard J, Amieva H, Beck A, Rascol O, et al. (2012) Influence of age, circadian and homeostatic processes on inhibitory motor control: a Go/Nogo task study. PLoS One 7: e39410.
Franken P, Dijk DJ (2009) Circadian clock genes and sleep homeostasis. Eur J Neurosci 29: 1820-1829.
Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ (1989) The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res 28: 193-213.
Ebrahim IO, Shapiro CM, Williams AJ, Fenwick PB (2013) Alcohol and sleep I: effects on normal sleep. Alcohol Clin Exp Res 37: 539-549.
James JE, Keane MA (2007) Caffeine, sleep and wakefulness: implications of new understanding about withdrawal reversal. Hum Psychopharmacol 22: 549-558.
Prat G, Adan A, Sanchez-Turet M (2009) Alcohol hangover: a critical review of explanatory factors. Hum Psychopharmacol 24: 259-267.
Rechtschaffen A, Kales AA (1968) A manual of standardized terminology, techniques and scoring system of sleep stages of human subjects. Bethesda, MD: US Dept of Health, Education, Welfare, Public Health Service.
Knoblauch V, Munch M, Blatter K, Martens WL, Schroder C, et al. (2005) Age-related changes in the circadian modulation of sleep-spindle frequency during nap sleep. Sleep 28: 1093-1101.
Snodgrass JG, Corwin J (1988) Pragmatics of measuring recognition memory: applications to dementia and amnesia. J Exp Psychol Gen 117: 34-50.
Collette F, Van der Linden M (2002) Brain imaging of the central executive component of working memory. Neurosci Biobehav Rev 26: 105-125.
Owen AM, McMillan KM, Laird AR, Bullmore E (2005) N-back working memory paradigm: a metaanalysis of normative functional neuroimaging studies. Hum Brain Mapp25: 46-59.
Jaeggi SM, Buschkuehl M, Perrig WJ, Meier B (2010) The concurrent validity of the N-back task as a working memory measure. Memory 18: 394-412.
Kane MJ, Conway AR, Miura TK, Colflesh GJ (2007) Working memory, attention control, and the N-back task: a question of construct validity. J Exp Psychol Learn Mem Cogn 33: 615-622.
Leonhart R (2004) Lehrbuch Statistik. Bern: Verlag Hans Huber.
Dinges DF, Powell JW (1985) Microcomputer analyses of performance on a portable, simple visual RT task during sustained operations. Behavior Research Methods, Instruments, & Computers: A Journal of the Psychonomic Society 17: 625-655.
Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53: 983-997.
Hayter AJ (1984) A proof of the conjecture that the Tukey-Kramer multiple comparisons procedure is conservative. The Annals of Statistics 12: 61-75.
Lo JC, Groeger JA, Santhi N, Arbon EL, Lazar AS, et al. (2012) Effects of partial and acute total sleep deprivation on performance across cognitive domains, individuals and circadian phase. PLoS ONE 7: e45987.
Curran-Everett D (2000) Multiple comparisons: philosophies and illustrations. Am J Physiol Regul Integr Comp Physiol 279: R1-8.
Lavie P (1986) Ultrashort sleep-waking schedule. III. 'Gates' and 'forbidden zones' for sleep. Electroencephalogr Clin Neurophysiol 63: 414-425.
Schmidt C, Collette F, Leclercq Y, Sterpenich V, Vandewalle G, et al. (2009) Homeostatic sleep pressure and responses to sustained attention in the suprachiasmatic area. Science 324: 516-519.
Mackiewicz M, Nikonova EV, Zimmerman JE, Galante RJ, Zhang L, et al. (2003) Enzymes of adenosine metabolism in the brain: diurnal rhythm and the effect of sleep deprivation. J Neurochem 85: 348-357.
Gorfine T, Zisapel N (2009) Late evening brain activation patterns and their relation to the internal biological time, melatonin, and homeostatic sleep debt. Hum Brain Mapp 30: 541-552.
Lavie P (1997) Melatonin: role in gating nocturnal rise in sleep propensity. J Biol Rhythms 12: 657-665.
Mistlberger RE (2005) Circadian regulation of sleep in mammals: role of the suprachiasmatic nucleus. Brain Res Brain Res Rev 49: 429-454.
De Gennaro L, Ferrara M (2003) Sleep spindles: an overview. Sleep Med Rev 7: 423-440.
Knoblauch V, Krauchi K, Renz C, Wirz-Justice A, Cajochen C (2002) Homeostatic control of slow-wave and spindle frequency activity during human sleep: effect of differential sleep pressure and brain topography. Cereb Cortex 12: 1092-1100.
Bonnet M, Carley D, Carskadon M, Easton P, Guilleminault C, et al. (1992) EEG arousals: scoring rules and examples: a preliminary report from the Sleep Disorders Atlas Task Force of the American Sleep Disorders Association. Sleep 15: 173-184.
Ehrhart J, Toussaint M, Simon C, Gronfier C, Luthringer R, et al. (2000) Alpha activity and cardiac correlates: three types of relationships during nocturnal sleep. Clin Neurophysiol 111: 940-946.
Tononi G, Cirelli C (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10: 49-62.
Rasch B, Born J (2013) About sleep's role in memory. Physiol Rev 93: 681-766.
Aeschbach D (2011) REM-sleep regulation: circadian, homeostatic, and non-REM sleep-dependent determinants. In: Mallick BN, Pandi-Perumal SR, McCarley RW, Morrison AR, editors. Rapid Eye Movement Sleep - Regulation and Function. New York: Cambridge University Press. pp. 80-88.
Smith C (1996) Sleep states, memory processes and synaptic plasticity. Behav Brain Res 78: 49-56.
Legault G, Smith CT, Beninger RJ (2006) Post-training intra-striatal scopolamine or flupenthixol impairs radial maze learning in rats. Behav Brain Res 170: 148-155.
Poe GR, Walsh CM, Bjorness TE (2010) Cognitive neuroscience of sleep. Prog Brain Res 185: 1-19.
Rasch B, Gais S, Born J (2009) Impaired off-line consolidation of motor memories after combined blockade of cholinergic receptors during REM sleep-rich sleep. Neuropsychopharmacology 34: 1843-1853.
Wallace TL, Bertrand D (2013) Importance of the nicotinic acetylcholine receptor system in the prefrontal cortex. Biochem Pharmacol 85: 1713-1720.
Buschkuehl M, Jaeggi SM, Jonides J (2012) Neuronal effects following working memory training. Dev Cogn Neurosci 2 Suppl 1: S167-179.
Scullin MK, Trotti LM, Wilson AG, Greer SA, Bliwise DL (2012) Nocturnal sleep enhances working memory training in Parkinson's disease but not Lewy body dementia. Brain 135: 2789-2797.
Fuxe K, Ferre S, Genedani S, Franco R, Agnati LF (2007) Adenosine receptor-dopamine receptor interactions in the basal ganglia and their relevance for brain function. Physiol Behav 92: 210-217.
Basheer R, Strecker RE, Thakkar MM, McCarley RW (2004) Adenosine and sleep-wake regulation. Prog Neurobiol 73: 379-396.
Ma WJ, Husain M, Bays PM (2014) Changing concepts of working memory. Nat Neurosci 17: 347-356.
