Abstract
The activity patterns adopted by brain neuronal populations differ dramatically between wakefulness and sleep. However, these vigilance states are not independent and they reciprocally interact. Here, we provide evidence that in humans, regional brain activity during wakefulness is influenced by sleep regulation, namely by the interaction between sleep homeostasis and circadian signals. We also show that, by contrast, regional brain activity during sleep is influenced by the experience acquired during the preceding waking period. These data reveal the dynamic interactions by which the succession of vigilance states support normal brain function and human cognition.
Similar content being viewed by others
References
Archer SN, Robilliard DL, Skene DJ, Smits M, Williams A, Arendt J, von Schantz M (2003) A length polymorphism in the circadian clock gene Per3 is linked to delayed sleep phase syndrome and extreme diurnal preference. Sleep 26(4):413–415
Aston-Jones G (2005) Brain structures and receptors involved in alertness. Sleep Med 6(Suppl 1):S3–S7
Basheer R, Strecker RE, Thakkar MM, McCarley RW (2004) Adenosine and sleep–wake regulation. Prog Neurobiol 73(6):379–396. doi:10.1016/j.pneurobio.2004.06.004
Borbely AA (1982) A two process model of sleep regulation. Hum Neurobiol 1(3):195–204
Born J, Diekelmann S, Wilhelm I (2009) The whats and whens of sleep-dependent memory consolidation. Sleep Med Rev 13(5):309–321. doi:10.1016/j.smrv.2008.08.002
Braun AR, Balkin TJ, Wesenten NJ, Carson RE, Varga M, Baldwin P, Selbie S, Belenky G, Herscovitch P (1997) Regional cerebral blood flow throughout the sleep-wake cycle. An H2(15)O PET study. Brain 120(Pt 7):1173–1197
Buchsbaum MS, Gillin JC, Wu J, Hazlett E, Sicotte N, Dupont RM, Bunney WE Jr (1989) Regional cerebral glucose metabolic rate in human sleep assessed by positron emission tomography. Life Sci 45(15):1349–1356
Dang-Vu TT, Schabus M, Desseilles M, Albouy G, Boly M, Darsaud A, Gais S, Rauchs G, Sterpenich V, Vandewalle G, Carrier J, Moonen G, Balteau E, Degueldre C, Luxen A, Phillips C, Maquet P (2008) Spontaneous neural activity during human slow wave sleep. Proc Natl Acad Sci U S A 105(39):15160–15165. doi:10.1073/pnas.0801819105
Destexhe A, Hughes SW, Rudolph M, Crunelli V (2007) Are corticothalamic 'up' states fragments of wakefulness? Trends Neurosci 30(7):334–342. doi:10.1016/j.tins.2007.04.006
Diekelmann S, Born J (2010) The memory function of sleep. Nat Rev Neurosci 11(2):114–126. doi:10.1038/nrn2762
Dijk DJ, Archer SN (2010) PERIOD3, circadian phenotypes, and sleep homeostasis. Sleep Med Rev 14(3):151–160. doi:10.1016/j.smrv.2009.07.002
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(5 Pt 1):3526–3538
Dijk DJ, Duffy JF, Czeisler CA (1992) Circadian and sleep/wake dependent aspects of subjective alertness and cognitive performance. J Sleep Res 1(2):112–117
Dijk DJ, von Schantz M (2005) Timing and consolidation of human sleep, wakefulness, and performance by a symphony of oscillators. J Biol Rhythms 20(4):279–290. doi:10.1177/0748730405278292
Dinges DPJ (1985) Microcomputer analyses of performance on a portable, simple visual rt task during sustained operations. Behav Res Methods Instrum Comput 17:652–655
Drummond SP, Meloy MJ, Yanagi MA, Orff HJ, Brown GG (2005) Compensatory recruitment after sleep deprivation and the relationship with performance. Psychiatry Res 140(3):211–223. doi:10.1016/j.pscychresns.2005.06.007
Euston DR, Tatsuno M, McNaughton BL (2007) Fast-forward playback of recent memory sequences in prefrontal cortex during sleep. Science 318(5853):1147–1150. doi:10.1126/science.1148979
Frankland PW, Bontempi B (2005) The organization of recent and remote memories. Nat Rev Neurosci 6(2):119–130. doi:10.1038/nrn1607
Gais S, Albouy G, Boly M, Dang-Vu TT, Darsaud A, Desseilles M, Rauchs G, Schabus M, Sterpenich V, Vandewalle G, Maquet P, Peigneux P (2007) Sleep transforms the cerebral trace of declarative memories. Proc Natl Acad Sci U S A 104(47):18778–18783. doi:10.1073/pnas.0705454104
Groeger JA, Viola AU, Lo JC, von Schantz M, Archer SN, Dijk DJ (2008) Early morning executive functioning during sleep deprivation is compromised by a PERIOD3 polymorphism. Sleep 31(8):1159–1167
Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O (2008) Mapping the structural core of human cerebral cortex. PLoS Biol 6(7):e159. doi:10.1371/journal.pbio.0060159
Hofle N, Paus T, Reutens D, Fiset P, Gotman J, Evans AC, Jones BE (1997) Regional cerebral blood flow changes as a function of delta and spindle activity during slow wave sleep in humans. J Neurosci 17(12):4800–4808
Huber R, Esser SK, Ferrarelli F, Massimini M, Peterson MJ, Tononi G (2007) TMS-induced cortical potentiation during wakefulness locally increases slow wave activity during sleep. PLoS One 2(3):e276. doi:10.1371/journal.pone.0000276
Huber R, Ghilardi MF, Massimini M, Tononi G (2004) Local sleep and learning. Nature 430(6995):78–81. doi:10.1038/nature02663
Huber R, Maatta S, Esser SK, Sarasso S, Ferrarelli F, Watson A, Ferreri F, Peterson MJ, Tononi G (2008) Measures of cortical plasticity after transcranial paired associative stimulation predict changes in electroencephalogram slow-wave activity during subsequent sleep. J Neurosci 28(31):7911–7918. doi:10.1523/JNEUROSCI.1636-08.2008
Isomura Y, Sirota A, Ozen S, Montgomery S, Mizuseki K, Henze DA, Buzsaki G (2006) Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron 52(5):871–882. doi:10.1016/j.neuron.2006.10.023
Ji D, Wilson MA (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10(1):100–107. doi:10.1038/nn1825
Kajimura N, Uchiyama M, Takayama Y, Uchida S, Uema T, Kato M, Sekimoto M, Watanabe T, Nakajima T, Horikoshi S, Ogawa K, Nishikawa M, Hiroki M, Kudo Y, Matsuda H, Okawa M, Takahashi K (1999) Activity of midbrain reticular formation and neocortex during the progression of human non-rapid eye movement sleep. J Neurosci 19(22):10065–10073
Kattler H, Dijk DJ, Borbely AA (1994) Effect of unilateral somatosensory stimulation prior to sleep on the sleep EEG in humans. J Sleep Res 3(3):159–164
Krueger JM (2008) The role of cytokines in sleep regulation. Curr Pharm Des 14(32):3408–3416
Laureys S, Peigneux P, Phillips C, Fuchs S, Degueldre C, Aerts J, Del Fiore G, Petiau C, Luxen A, van der Linden M, Cleeremans A, Smith C, Maquet P (2001) Experience-dependent changes in cerebral functional connectivity during human rapid eye movement sleep. Neuroscience 105(3):521–525
Louie K, Wilson MA (2001) Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29(1):145–156
Madsen PL, Holm S, Vorstrup S, Friberg L, Lassen NA, Wildschiodtz G (1991) Human regional cerebral blood flow during rapid-eye-movement sleep. J Cereb Blood Flow Metab 11(3):502–507. doi:10.1038/jcbfm.1991.94
Madsen PL, Schmidt JF, Holm S, Vorstrup S, Lassen NA, Wildschiodtz G (1991) Cerebral oxygen metabolism and cerebral blood flow in man during light sleep (stage 2). Brain Res 557(1–2):217–220
Maquet P (2000) Functional neuroimaging of normal human sleep by positron emission tomography. J Sleep Res 9(3):207–231
Maquet P, Degueldre C, Delfiore G, Aerts J, Peters JM, Luxen A, Franck G (1997) Functional neuroanatomy of human slow wave sleep. J Neurosci 17(8):2807–2812
Maquet P, Dive D, Salmon E, Sadzot B, Franco G, Poirrier R, Franck G (1992) Cerebral glucose utilization during stage 2 sleep in man. Brain Res 571(1):149–153
Maquet P, Dive D, Salmon E, Sadzot B, Franco G, Poirrier R, von Frenckell R, Franck G (1990) Cerebral glucose utilization during sleep-wake cycle in man determined by positron emission tomography and [18F]2-fluoro-2-deoxy-D-glucose method. Brain Res 513(1):136–143
Maquet P, Laureys S, Peigneux P, Fuchs S, Petiau C, Phillips C, Aerts J, Del Fiore G, Degueldre C, Meulemans T, Luxen A, Franck G, Van Der Linden M, Smith C, Cleeremans A (2000) Experience-dependent changes in cerebral activation during human REM sleep. Nat Neurosci 3(8):831–836. doi:10.1038/77744
Maquet P, Peters J, Aerts J, Delfiore G, Degueldre C, Luxen A, Franck G (1996) Functional neuroanatomy of human rapid-eye-movement sleep and dreaming. Nature 383(6596):163–166. doi:10.1038/383163a0
Maquet P, Ruby P, Maudoux A, Albouy G, Sterpenich V, Dang-Vu T, Desseilles M, Boly M, Perrin F, Peigneux P, Laureys S (2005) Human cognition during REM sleep and the activity profile within frontal and parietal cortices: a reappraisal of functional neuroimaging data. Prog Brain Res 150:219–227. doi:10.1016/S0079-6123(05)50016-5
Marr D (1970) A theory for cerebral neocortex. Proc R Soc Lond B Biol Sci 176(43):161–234
Mongrain V, Carrier J, Dumont M (2006) Circadian and homeostatic sleep regulation in morningness–eveningness. J Sleep Res 15(2):162–166. doi:10.1111/j.1365-2869.2006.00532.x
Murphy M, Riedner BA, Huber R, Massimini M, Ferrarelli F, Tononi G (2009) Source modeling sleep slow waves. Proc Natl Acad Sci U S A 106(5):1608–1613. doi:10.1073/pnas.0807933106
Nadasdy Z, Hirase H, Czurko A, Csicsvari J, Buzsaki G (1999) Replay and time compression of recurring spike sequences in the hippocampus. J Neurosci 19(21):9497–9507
Nofzinger EA, Mintun MA, Wiseman M, Kupfer DJ, Moore RY (1997) Forebrain activation in REM sleep: an FDG PET study. Brain Res 770(1–2):192–201
Peigneux P, Laureys S, Fuchs S, Collette F, Perrin F, Reggers J, Phillips C, Degueldre C, Del Fiore G, Aerts J, Luxen A, Maquet P (2004) Are spatial memories strengthened in the human hippocampus during slow wave sleep? Neuron 44(3):535–545. doi:10.1016/j.neuron.2004.10.007
Pennartz CM, Lee E, Verheul J, Lipa P, Barnes CA, McNaughton BL (2004) The ventral striatum in off-line processing: ensemble reactivation during sleep and modulation by hippocampal ripples. J Neurosci 24(29):6446–6456. doi:10.1523/JNEUROSCI.0575-04.2004
Peyrache A, Khamassi M, Benchenane K, Wiener SI, Battaglia FP (2009) Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat Neurosci 12(7):919–926. doi:10.1038/nn.2337
Qin YL, McNaughton BL, Skaggs WE, Barnes CA (1997) Memory reprocessing in corticocortical and hippocampocortical neuronal ensembles. Philos Trans R Soc Lond B Biol Sci 352(1360):1525–1533. doi:10.1098/rstb.1997.0139
Ribeiro S, Gervasoni D, Soares ES, Zhou Y, Lin SC, Pantoja J, Lavine M, Nicolelis MA (2004) Long-lasting novelty-induced neuronal reverberation during slow-wave sleep in multiple forebrain areas. PLoS Biol 2(1):E24. doi:10.1371/journal.pbio.0020024
Schabus M, Dang-Vu TT, Albouy G, Balteau E, Boly M, Carrier J, Darsaud A, Degueldre C, Desseilles M, Gais S, Phillips C, Rauchs G, Schnakers C, Sterpenich V, Vandewalle G, Luxen A, Maquet P (2007) Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc Natl Acad Sci U S A 104(32):13164–13169. doi:10.1073/pnas.0703084104
Schmidt C, Collette F, Leclercq Y, Sterpenich V, Vandewalle G, Berthomier P, Berthomier C, Phillips C, Tinguely G, Darsaud A, Gais S, Schabus M, Desseilles M, Dang-Vu TT, Salmon E, Balteau E, Degueldre C, Luxen A, Maquet P, Cajochen C, Peigneux P (2009) Homeostatic sleep pressure and responses to sustained attention in the suprachiasmatic area. Science 324(5926):516–519. doi:10.1126/science.1167337
Schmidt C, Peigneux P, Maquet P, Phillips C (2010) Response to comment on "Homeostatic sleep pressure and responses to sustained attention in the suprachiasmatic area". Science 316:309c-
Steriade MM, McCarley RW (eds) (2005) Brain control of wakefulness and sleep. Plenum, New York
Takahashi K (1989) Regional cerebral blood flow and oxygen consumption during normal human sleep. No To Shinkei 41(9):919–925
Tononi G, Cirelli C (2003) Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull 62(2):143–150
Tononi G, Cirelli C (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10(1):49–62. doi:10.1016/j.smrv.2005.05.002
Van Dongen HP, Baynard MD, Maislin G, Dinges DF (2004) Systematic interindividual differences in neurobehavioral impairment from sleep loss: evidence of trait-like differential vulnerability. Sleep 27(3):423–433
Vandewalle G, Archer SN, Wuillaume C, Balteau E, Degueldre C, Luxen A, Maquet P, Dijk DJ (2009) Functional magnetic resonance imaging-assessed brain responses during an executive task depend on interaction of sleep homeostasis, circadian phase, and PER3 genotype. J Neurosci 29(25):7948–7956. doi:10.1523/JNEUROSCI.0229-09.2009
Viola AU, Archer SN, James LM, Groeger JA, Lo JC, Skene DJ, von Schantz M, Dijk DJ (2007) PER3 polymorphism predicts sleep structure and waking performance. Curr Biol 17(7):613–618. doi:10.1016/j.cub.2007.01.073
Wierzynski CM, Lubenov EV, Gu M, Siapas AG (2009) State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron 61(4):587–596. doi:10.1016/j.neuron.2009.01.011
Acknowledgments
Personal research reported in this review was supported by the Belgian Fonds National de la Recherche Scientifique (F.N.R.S), Fondation Médicale Reine Elisabeth (FMRE), Research Fund of the University of Liège (ULg), and “Interuniversity Attraction Poles Programme–Belgian State–Belgian Science Policy.” VM is supported by the ULg. ZJ, LaM, CK, AF, AS, GV, and PM are supported by the F.N.R.S.
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is published as part of the Special Issue on Sleep.
Rights and permissions
About this article
Cite this article
Jedidi, Z., Rikir, E., Muto, V. et al. Functional neuroimaging of the reciprocal influences between sleep and wakefulness. Pflugers Arch - Eur J Physiol 463, 103–109 (2012). https://doi.org/10.1007/s00424-011-1016-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00424-011-1016-4