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Brain Topography

, Volume 30, Issue 6, pp 757–773 | Cite as

Resisting Sleep Pressure: Impact on Resting State Functional Network Connectivity

  • Laura Tüshaus
  • Joshua Henk Balsters
  • Anthony Schläpfer
  • Daniel Brandeis
  • Ruth O’Gorman Tuura
  • Peter Achermann
Original Paper

Abstract

In today’s 24/7 society, sleep restriction is a common phenomenon which leads to increased levels of sleep pressure in daily life. However, the magnitude and extent of impairment of brain functioning due to increased sleep pressure is still not completely understood. Resting state network (RSN) analyses have become increasingly popular because they allow us to investigate brain activity patterns in the absence of a specific task and to identify changes under different levels of vigilance (e.g. due to increased sleep pressure). RSNs are commonly derived from BOLD fMRI signals but studies progressively also employ cerebral blood flow (CBF) signals. To investigate the impact of sleep pressure on RSNs, we examined RSNs of participants under high (19 h awake) and normal (10 h awake) sleep pressure with three imaging modalities (arterial spin labeling, BOLD, pseudo BOLD) while providing confirmation of vigilance states in most conditions. We demonstrated that CBF and pseudo BOLD signals (measured with arterial spin labeling) are suited to derive independent component analysis based RSNs. The spatial map differences of these RSNs were rather small, suggesting a strong biological substrate underlying these networks. Interestingly, increased sleep pressure, namely longer time awake, specifically changed the functional network connectivity (FNC) between RSNs. In summary, all FNCs of the default mode network with any other network or component showed increasing effects as a function of increased ‘time awake’. All other FNCs became more anti-correlated with increased ‘time awake’. The sensorimotor networks were the only ones who showed a within network change of FNC, namely decreased connectivity as function of ‘time awake’. These specific changes of FNC could reflect both compensatory mechanisms aiming to fight sleep as well as a first reduction of consciousness while becoming drowsy. We think that the specific changes observed in functional network connectivity could imply an impairment of information transfer between the affected RSNs.

Keywords

BOLD Pseudo BOLD Arterial spin labeling Cerebral blood flow Time awake Independent component analysis Vigilance Imaging modality 

Notes

Acknowledgements

This study was supported by the Swiss National Science Foundation grant CRSII3_136249. We thank Drs. Andrea Federspiel, Philipp Stämpfli, Roger Lüchinger, Kay Jann, Roland Dürr, Thomas Rusterholz for technical support and Drs. Thomas Koenig, Mara Kottlow, Lars Michels and Leila Tarokh for fruitful discussions. We also would like to thank Ximena Omlin, Angela Aeschbach, Claudia Aschmann, Daniela Buser, Angela Escobar, Lukas Fürer, Jolanda Müller, Johanna Scherer, Nina Schumacher, Michelle Steinemann, Sarah Untersander and Katharina Wellstein for help with the data acquisition.

Funding

This work was supported by the Swiss National Science Foundation Sinergia grant #136249.

Author Contributions

LT, AS, DB, ROT and PA designed the experiment. LT and AS performed the experiment. LT, JB and PA analyzed the data. LT and PA wrote the manuscript. All authors approved the final version.

Compliance with Ethical Standards

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Supplementary material

10548_2017_575_MOESM1_ESM.pdf (547 kb)
Supplementary material 1 (PDF 548 KB)

References

  1. Aguirre GK, Detre JA, Zarahn E, Alsop DC (2002) Experimental design and the relative sensitivity of BOLD and perfusion fMRI. Neuroimage 15:488–500CrossRefPubMedGoogle Scholar
  2. Åkerstedt T, Gillberg M (1990) Subjective and objective sleepiness in the active individual. Int J Neurosci 52:29–37CrossRefPubMedGoogle Scholar
  3. Allen PJ, Polizzi G, Krakow K, Fish DR, Lemieux L (1998) Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction. Neuroimage 8:229–239CrossRefPubMedGoogle Scholar
  4. Allen PJ, Josephs O, Turner R (2000) A method for removing imaging artifact from continuous EEG recorded during functional MRI. Neuroimage 12:230–239CrossRefPubMedGoogle Scholar
  5. Allen EA et al (2011a) A baseline for the multivariate comparison of resting-state networks Frontiers in Systems. Neuroscience 5:1–23Google Scholar
  6. Allen EA, Erhardt EB, Yonghua W, Eichele T, Calhoun VD (2011b) Capturing inter-subject variability with group independent component analysis of fMRI data: a simulation study. Neuroimage 59:4141–4159. doi: 10.1016/j.neuroimage.2011.10.010 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Aslan S, Xu F, Wang PL, Uh J, Yezhuvath US, van Osch M, Lu H (2010) Estimation of labeling efficiency in Pseudocontinuous arterial spin labeling. Magn Reson Med 63:765–771CrossRefPubMedPubMedCentralGoogle Scholar
  8. Banks S, Dinges DF (2007) Behavioral and physiological consequences of sleep restriction. J Clin Sleep Med 3:519–528PubMedPubMedCentralGoogle Scholar
  9. Basner M, Rao H, Goel N, Dinges DF (2013) Sleep deprivation and neurobehavioral dynamics. Curr Opin Neurobiol 23:854–863CrossRefPubMedPubMedCentralGoogle Scholar
  10. Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360:1001–1013CrossRefPubMedPubMedCentralGoogle Scholar
  11. Berger RJ, Oswald I (1962) Effects of sleep deprivation on behaviour, subsequent sleep, and dreaming. Br J Psychiatry 108:457–465CrossRefGoogle Scholar
  12. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541CrossRefPubMedGoogle Scholar
  13. Blautzik J et al (2013) Classifying fMRI-derived resting-state connectivity patterns according to their daily rhythmicity. Neuroimage 71:298–306CrossRefPubMedGoogle Scholar
  14. Braun AR et al (1997) Regional cerebral blood flow throughout the sleep–wake cycle An H2(15)O PET study. Brain 120:1173–1197CrossRefPubMedGoogle Scholar
  15. Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain’s default network: anatomy, function, and relevance to disease. Ann NY Acad Sci 1124:1–38CrossRefPubMedGoogle Scholar
  16. Bunge S, Hazeltine E, Scanlon M, Rosen A, Gabrieli J (2002) Dissociable contributions of prefrontal and parietal cortices to response selection. Neuroimage 17:1562–1571. doi: 10.1006/nimg.2002.1252 CrossRefPubMedGoogle Scholar
  17. Buxton RB (2002) Introduction to Functional Magnetic Resonance Imaging: Principles and Techniques. Cambridge University Press, Cambridge, NYGoogle Scholar
  18. Buzsáki G, Logothetis N, Singer W (2013) Scaling brain size, keeping timing: evolutionary preservation of brain rhythms. Neuron 80:751–764. doi: 10.1016/j.neuron.2013.10.002 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Calhoun VD, Adali T, Pearlson GD, Pekar JJ (2001) A method for making group inferences from functional MRI data using independent component analysis. Hum Brain Mapp 14:140–151CrossRefPubMedGoogle Scholar
  20. Chee MWL, Choo W (2004) Functional imaging of working memory after 24 h of total sleep deprivation. J Neurosci 24:4560–4567CrossRefPubMedGoogle Scholar
  21. Chee MWL, Tan JC (2010) Lapsing when sleep deprived: neural activation characteristics of resistant and vulnerable individuals. Neuroimage 51:835–843CrossRefPubMedGoogle Scholar
  22. Chee MWL, Chuah L, Venkatraman V, Chan W, Philip P, Dinges D (2006) Functional imaging of working memory following normal sleep and after 24 and 35 h of sleep deprivation: correlations of fronto-parietal activation with performance. Neuroimage 31:419–428CrossRefPubMedGoogle Scholar
  23. Chee MWL, Tan J, Zheng H, Parimal S, Weissmann D, Zagorodnov V, Dinges DF (2008) Lapsing during sleep deprivation is associated with distributed changes in brain activation. J Neurosci 28:5519–5528. doi: 10.1523/JNEUROSCI.0733-08.2008 CrossRefPubMedGoogle Scholar
  24. Chee MWL, Tan J, Parimal S, Zagorodnov V (2010) Sleep deprivation and its effects on object-selective attention. Neuroimage 49:1903–1910. doi: 10.1016/j.neuroimage.2009.08.067 CrossRefPubMedGoogle Scholar
  25. Chen JJ, Jann K, Wang DJJ (2015) Characterizing resting-state brain function using arterial-spin labeling. Brain Connect 5:527–542CrossRefPubMedPubMedCentralGoogle Scholar
  26. Choo W-C, Lee W-W, Venkatraman V, Sheu F-S, Chee MWL (2005) Dissociation of cortical regions modulated by both working memory load and sleep deprivation and by sleep deprivation alone. Neuroimage 25:579–587CrossRefPubMedGoogle Scholar
  27. Czisch M, Wehrle R, Harsay H, Wetter TC, Holsboer F, Sämann PG, Drummond SPA (2012) On the need of objective vigilance monitoring: effects of sleep loss on target detection and task-negative activity using combined EEG/fMRI. Front Neurol 3:67. doi: 10.3389/fneur.2012.00067 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Damoiseaux JS, Rombouts SARB, Barkhof F, Scheltens P, Stam CJ, Smith SM, Beckmann CF (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103:13848–13853CrossRefPubMedPubMedCentralGoogle Scholar
  29. De Luca M, Beckmann CF, De Stefano N, Matthews PM, Smith SM (2006) fMRI resting state networks define distinct modes of long-distance interactions in the human brain. Neuroimage 29:1359–1367CrossRefPubMedGoogle Scholar
  30. De Havas JA, Parimal S, Soon CS, Chee MWL (2012) Sleep deprivation reduces default mode network connectivity and anti-correlation during rest and task performance. Neuroimage 59:1745–1751CrossRefPubMedGoogle Scholar
  31. Dehaene S, Sergent C, Changeaux J-P (2003) A neuronal network model linking subjective reports and objective physiological data during conscious perception. Proc Natl Acad Sci USA 100:8520–8525CrossRefPubMedPubMedCentralGoogle Scholar
  32. Deibler AR, Pollock JM, Kraft RA, Tan H, Burdette JH, Maldjian JA (2008) Arterial spin-labeling in routine clinical practice, Part 1: technique and artifacts. AJNR Am J Neuroradiol 29:1228–1234CrossRefPubMedPubMedCentralGoogle Scholar
  33. Dinges DF et al (1997) Cumulative sleepiness, mood disturbance, and psychomotor vigilance performance decrements during a week of sleep restricted to 4–5 h per night. Sleep 20:267–277PubMedGoogle Scholar
  34. Drummond S, Gillin J, Brown G (2001) Increased cerebral response during a divided attention task following sleep deprivation. J Sleep Res 10:85–92CrossRefPubMedGoogle Scholar
  35. Drummond SPA, Brown GG, Salamat JS, Gillin JC (2004) Increasing task difficulty facilitates the cerebral compensatory response to total sleep deprivation. Sleep 27:445–451PubMedGoogle Scholar
  36. Drummond S, Bischoff-Grethe A, Dinges D, Ayalon L, Mednick S, Meloy M (2005) The neural basis of the psychomotor vigilance task. Sleep 28:1059–1068PubMedGoogle Scholar
  37. Erhardt EB, Rachakonda S, Bedrick E, Allen EA, Adali T, Calhoun VD (2011) Comparison of multi-subject ICA methods for analysis of fMRI data. Hum Brain Mapp 32:2075–2095. doi: 10.1002/hbm.21170 CrossRefPubMedGoogle Scholar
  38. Fan J, McCandliss BD, Fossella J, Flombaum JI, Posner MI (2005) The activation of attention networks. Neuroimage 26:471–479CrossRefPubMedGoogle Scholar
  39. Filippi M, Valsasina P, Misci P, Falini A, Comi G, Rocca MA (2013) The organization of intrinsic brain activity differs between genders: a resting-state fMRI study in a large cohort of young healthy subjects. Hum Brain Mapp 34:1330–1343. doi: 10.1002/hbm.21514 CrossRefPubMedGoogle Scholar
  40. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA 102:9673–9678CrossRefPubMedPubMedCentralGoogle Scholar
  41. Franco A, Mannell M, Calhoun VD, Mayer AR (2013) Impact of analysis methods on the reproducibility and reliability of resting-state networks. Brain Connect 3:363–374 doi: 10.1089/brain.2012.0134 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Heine L et al (2012) Resting state networks and consciousness Alterations of multiple resting state network connectivity in physiological, pharmacological, and pathological consciousness states. Front Psychol 3:295. doi: 10.3389/fpsyg.2012.00295 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Hjelmervik H, Hausmann M, Osnes B, Westerhausen R, Specht K (2014) Resting states are resting traits—an fMRI Study of sex differences and menstrual cycle effects in resting state cognitive control networks. PLoS ONE 9:e103492. doi: 10.1371/journal.pone.0103492 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Hockey GRJ, Wastell DG, Sauer J (1998) Effects of sleep deprivation and user interface on complex performance: a multilevel analysis of compensatory control. Hum Factors 40:233–253CrossRefPubMedGoogle Scholar
  45. Horne JA, Pettitt AN (1985) High incentive effects on vigilance performance during 72 h of total sleep deprivation. Acta Psychol 58:123–139CrossRefGoogle Scholar
  46. Horovitz SG, Fukunaga M, de Zwart JA, van Gelderen P, Fulton SC, Balkin TJ, Duyn JH (2008) Low frequency BOLD fluctuations during resting wakefulness and light sleep: a simultaneous EEG-fMRI study. Hum Brain Mapp 29:671–682CrossRefPubMedGoogle Scholar
  47. Horovitz SG, Braun AR, Carr WS, Picchioni D, Balkin TJ, Fukunaga M, Duyn JH (2009) Decoupling of the brain}s default mode network during deep sleep. Proc Natl Acad Sci USA 106:11376–11381CrossRefPubMedPubMedCentralGoogle Scholar
  48. Iannaccone R, Hauser T, Staempfli P, Walitza S, Brandeis D, Brem S (2015) Conflict monitoring and error processing: new insights from simultaneous EEG-fMRI. Neuroimage 105:395–407. doi: 10.1016/j.neuroimage.2014.10.028 CrossRefPubMedGoogle Scholar
  49. Iber C, Ancoli-Israel S, Chesson Jr AL, Quan SF (2007) The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications, 1st edn. American Academy of Sleep Medicine, WestchesterGoogle Scholar
  50. Jackson ML et al (2011) The effect of sleep deprivation on BOLD activity elicited by a divided attention task. Brain Imag Behav 5:97–108. doi: 10.1007/s11682-011-9115-6 CrossRefGoogle Scholar
  51. Jackson ML, Gunzelmann G, Whitney P, Hinson JM, Belenky G, Rabat A, Van Dongen HPA (2013) Deconstructing and reconstructing cognitive performance in sleep deprivation. Sleep Med Rev 17:215–225CrossRefPubMedGoogle Scholar
  52. Jann K, Orosz A, Dierks T, Wang DJJ, Wiest R, Federspiel A (2013) Quantification of network perfusion in ASL cerebral blood flow data with seed based and ICA approaches. Brain Topogr 26:569–580CrossRefPubMedGoogle Scholar
  53. Jann K, Gee DG, Kilroy E, Schwab S, Smith RX, Cannon TD, Wang DJJ (2015) Functional connectivity in BOLD and CBF data: similarity and reliability of resting brain networks. Neuroimage 106:111–122CrossRefPubMedGoogle Scholar
  54. Johns MW (1991) A new method for measuring daytime sleepiness: the epworth sleepiness scale. Sleep 14:540–545CrossRefPubMedGoogle Scholar
  55. Kaplan GB, Greenblatt DJ, Ehrenberg BL, Goddard JE, Cotreau MM, Harmatz JS, Shader RI (1997) Dose-dependent pharmacokinetics and psychomotor effects of caffeine in humans. Pharmcokinetics Pharmacodyn 37:693–703Google Scholar
  56. Kaufmann T et al (2016) The brain functional connectome is robustly altered by lack of sleep. Neuroimage 127:324–332CrossRefPubMedGoogle Scholar
  57. Kong D, Soon C, Chee MWL (2012) Functional imaging correlates of impaired distractor suppression following sleep deprivation. Neuroimage 61:50–55CrossRefPubMedGoogle Scholar
  58. Kopp B, Rist F, Mattler U (1996) N200 in the flanker task as a neurobehavioral tool for investigating executive control. Psychophysiology 33:282–294CrossRefPubMedGoogle Scholar
  59. Laird AR et al (2011) Behavioral interpretations of intrinsic connectivity networks. J Cogn Neurosci 23:4022–4037CrossRefPubMedPubMedCentralGoogle Scholar
  60. Landolt H-P, Rétey JV, Tönz K, Gottselig JM, Khatami R, Isabelle B, Achermann P (2004) Caffeine attenuates waking and sleep electroencephalographic markers of sleep homeostasis in humans. Neuropsychopharmacology 29:1933–1939CrossRefPubMedGoogle Scholar
  61. Larson-Prior LJ, Zempel JM, Nolan TS, Prior FW, Snyder AZ, Raichle ME (2009) Cortical network functional connectivity in the descent to sleep. Proc Natl Acad Sci USA 106:4489–4494CrossRefPubMedPubMedCentralGoogle Scholar
  62. Li YO, Adali T, Calhoun VD (2007) Estimating the number of independent components for functional magnetic resonance imaging data. Hum Brain Mapp 28:1251–1266CrossRefPubMedGoogle Scholar
  63. Lim J, Choo W, Chee MWL (2007) Reproducibility of changes in behaviour and fMRI activation associated with sleep deprivation in a working memory task. Sleep 30:61–70CrossRefPubMedGoogle Scholar
  64. Lim J, Tan J, Parimal S, Dinges DF, Chee MWL (2010) Sleep deprivation impairs object-selective attention: a view from the ventral visual cortex. PLoS ONE 5:e9087. doi: 10.1371/journal.pone.0009087 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Liu TT, Wong EC (2005) A signal processing model for arterial spin labeling functional MRI. Neuroimage 24:207–215CrossRefPubMedGoogle Scholar
  66. Logothetis N, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150–157. doi: 10.1038/35084005 CrossRefPubMedGoogle Scholar
  67. Ma N, Dinges DF, Basner M, Rao H (2015) How acute total sleep loss affects the attending brain: a meta-analysis of neuroimaging studies. Sleep 38:233–240CrossRefPubMedPubMedCentralGoogle Scholar
  68. Magri C, Schridde U, Murayama Y, Panzeri S, Logothetis N (2012) The amplitude and timing of the BOLD signal reflects the relationship between local field potential power at different frequencies. J Neurosci 32:1395–1407. doi: 10.1523/JNEUROSCI.3985-11.2012 CrossRefPubMedGoogle Scholar
  69. Mander B et al (2008) Sleep deprivation alters functioning within the neural network underlying the covert orienting of attention. Brain Res 1217:148–156. doi: 10.1016/j.brainres.2008.04.030 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Mantini D, Perrucci MG, Cugini S, Ferretti A, Romani GL, Del Gratta C (2007) Complete artifact removal for EEG recorded during continuous fMRI using independent component analysis. Neuroimage 34:598–607CrossRefPubMedGoogle Scholar
  71. Mason MF, Norton MI, Van Horn JD, Wegner DM, Grafton ST, Macrae CN (2007) Wandering minds: the default network and stimulus-independent thought. Science 315:393–395CrossRefPubMedPubMedCentralGoogle Scholar
  72. Michels L, Bucher K, Lüchinger R, Klaver P, Martin E, Jeanmonod D, Brandeis D (2010) Simultaneous EEG-fMRI during a working memory task: modulations in low and high frequency bands. PloS One 5:e10298. doi: 10.1371/journal.pone.0010298 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Mu Q et al (2005) Decreased cortical response to verbal working memory following sleep deprivation. Sleep 28:55–67CrossRefPubMedGoogle Scholar
  74. Muto V et al (2012) Influence of acute sleep loss on the neural correlates of alerting, orientating and executive attention components. J Sleep Res 21:648–658. doi: 10.1111/j.1365-2869.2012.01020.x CrossRefPubMedGoogle Scholar
  75. Nuwer MR et al (1998) IFCN Standards—IFCN standards for digital recording of clinical EEG. Electroencephalogr Clin Neurophysiol 106:259–261. doi: 10.1016/S0013-4694(97)00106-5 CrossRefPubMedGoogle Scholar
  76. Ong J, Kong D, Chia T, Tandi J, Yeo BTT, Chee MWL (2015) Co-activated yet disconnected—Neural correlates of eye closures when trying to stay awake. Neuroimage 118:553–562. doi: 10.1016/j.neuroimage.2015.03.085 CrossRefPubMedGoogle Scholar
  77. Portas CM, Howseman AM, Josephs O, Turner R, Frith CD (1998) A specific role for the thalamus in mediating the interaction of attention and arousal in humans. J Neurosci 18:8979–8989PubMedGoogle Scholar
  78. Poudel GR, Innes CRH, Jones RD (2012) Cerebral perfusion differences between drowsy and nondrowsy individuals after acute sleep restriction. Sleep 35:1085–1096CrossRefPubMedPubMedCentralGoogle Scholar
  79. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012) Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 59:2142–2154CrossRefPubMedGoogle Scholar
  80. Raichle ME (2011) The restless brain. Brain Connect 1:3–12CrossRefPubMedPubMedCentralGoogle Scholar
  81. Rechtschaffen A, Kales A (1968) A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. U. S. Department of Health, Education. and Welfare, Public Health Service - National Institutes of Health, National Institute of Neurological Diseases and Blindness, Neurological Information Network, Bethesda, Maryland 20014Google Scholar
  82. Roenneberg T, Wirz-Justice A, Merrow M (2003) Life between clocks: daily temporal patterns of human chronotypes. J Biol Rhythms 18:80–90CrossRefPubMedGoogle Scholar
  83. Rubia K, Smith A, Brammer M, Taylor E (2003) Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection. Neuroimage 20:351–358CrossRefPubMedGoogle Scholar
  84. Sämann PG, Tully C, Spoormaker VI, Wetter TC, Holsboer F, Wehrle R, Czisch M (2010) Increased sleep pressure reduces resting state functional connectivity. Magn Reson Mater Phys Biol Med 23:375–389CrossRefGoogle Scholar
  85. Sämann PG et al (2011) Development of the brain’s default mode network from wakefulness to slow wave sleep. Cereb Cortex 21:2082–2093CrossRefPubMedGoogle Scholar
  86. Smith SM et al (2009) Correspondence of the brain}s functional architecture during activation and rest. Proc Natl Acad Sci USA 106:13040–13045CrossRefPubMedPubMedCentralGoogle Scholar
  87. Sternberg S (1966) High-speed scanning in human memory. Science 153:652–654CrossRefPubMedGoogle Scholar
  88. Tomasi D et al (2009) Impairment of attentional networks after 1 night of sleep deprivation. Cereb Cortex 19:233–240. doi: 10.1093/cercor/bhn073 CrossRefPubMedGoogle Scholar
  89. Wang C, Ong J, Patanaik A, Zhou J, Chee M (2016) Spontaneous eyelid closures link vigilance fluctuation with fMRI dynamic connectivity states. Proc Natl Acad Sci USA 113:9653–9658CrossRefPubMedPubMedCentralGoogle Scholar
  90. Webb WB, Levy CM (1984) Effects of spaced and repeated total sleep deprivation. Ergon 27:45–58CrossRefGoogle Scholar
  91. Weissman-Fogel I, Moayedi M, Taylor KS, Pope G, Davis KD (2010) Cognitive and default-mode resting state networks: do male and female brains “rest” differently? Hum Brain Mapp 31:1713–1726. doi: 10.1002/hbm.20968 PubMedGoogle Scholar
  92. Wilkinson RT (1961) Interaction of lack of sleep with knowledge of results, repeated testing and individual differences. J Exp Psychol 62:263–271CrossRefPubMedGoogle Scholar
  93. Williams DS, Detre JA, Leigh JS, Koretsky AP (1992) Magnetic resonance imaging of perfusion using spin inversion of arterial water. Proc Natl Acad Sci USA 89:212–216CrossRefPubMedPubMedCentralGoogle Scholar
  94. Wittmann M, Dinich J, Merrow M, Roenneberg T (2006) Social jetlag: misalignment of biological and social time. Chronobiol Int 23:497–509CrossRefPubMedGoogle Scholar
  95. Wong EC, Buxton RB, Frank LR (1997) Implementation of quantitative perfusion imaging techniques for functional brain mapping using pulsed arterial spin labeling. NMR Biomed 10:237–249CrossRefPubMedGoogle Scholar
  96. Wu JC et al (2006) Frontal lobe metabolic decreases with sleep deprivation not totally reversed by recovery sleep. Neuropsychopharmacology 31:2783–2792CrossRefPubMedGoogle Scholar
  97. Wu W-C, St Lawrence KS, Licht DJ, Wang DJJ (2010) Quantification issues in arterial spin labeling perfusion magnetic resonance imaging. Top Magn Reson Imaging 21:65–73CrossRefPubMedGoogle Scholar
  98. Wu W-C, Lien S-H, Chang J-H, Yang S-C (2014) Caffeine alters resting-state functional connectivity measured by blood oxygenation level-dependent MRI. NMR Biomed 27:444–452CrossRefPubMedPubMedCentralGoogle Scholar
  99. Xu F, Liu P, Pekar JJ, Lu H (2015) Does acute caffeine ingestion alter brain metabolism in young adults? Neuroimage 110:39–47CrossRefPubMedPubMedCentralGoogle Scholar
  100. Yeo BTT, Tandi J, Chee MWL (2015) Functional connectivity during rested wakefulness predicts vulnerability to sleep deprivation. Neuroimage 111:147–158CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Laura Tüshaus
    • 1
    • 2
    • 3
  • Joshua Henk Balsters
    • 4
  • Anthony Schläpfer
    • 2
    • 5
  • Daniel Brandeis
    • 2
    • 5
    • 6
    • 7
  • Ruth O’Gorman Tuura
    • 7
    • 8
  • Peter Achermann
    • 1
    • 2
    • 3
    • 7
  1. 1.Chronobiology and Sleep Research, Institute of Pharmacology and ToxicologyUniversity of ZurichZurichSwitzerland
  2. 2.Neuroscience Center ZurichUniversity of Zurich and ETH ZurichZurichSwitzerland
  3. 3.Zurich Center for Interdisciplinary Sleep ResearchUniversity of ZurichZurichSwitzerland
  4. 4.Neural Control of Movement Lab, Department of Health Sciences and TechnologyETH ZurichZurichSwitzerland
  5. 5.Department of Child and Adolescent Psychiatry and PsychotherapyUniversity of ZurichZurichSwitzerland
  6. 6.Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental HealthMedical Faculty Mannheim/Heidelberg UniversityMannheimGermany
  7. 7.Zurich Center for Integrative Human PhysiologyUniversity of ZurichZurichSwitzerland
  8. 8.Center for MR-ResearchUniversity Children’s Hospital ZurichZurichSwitzerland

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