Sleep deprivation leads to a loss of functional connectivity in frontal brain regions
The restorative effect of sleep on waking brain activity remains poorly understood. Previous studies have compared overall neural network characteristics after normal sleep and sleep deprivation. To study whether sleep and sleep deprivation might differentially affect subsequent connectivity characteristics in different brain regions, we performed a within-subject study of resting state brain activity using the graph theory framework adapted for the individual electrode level.
In balanced order, we obtained high-density resting state electroencephalography (EEG) in 8 healthy participants, during a day following normal sleep and during a day following total sleep deprivation. We computed topographical maps of graph theoretical parameters describing local clustering and path length characteristics from functional connectivity matrices, based on synchronization likelihood, in five different frequency bands. A non-parametric permutation analysis with cluster correction for multiple comparisons was applied to assess significance of topographical changes in clustering coefficient and path length.
Significant changes in graph theoretical parameters were only found on the scalp overlying the prefrontal cortex, where the clustering coefficient (local integration) decreased in the alpha frequency band and the path length (global integration) increased in the theta frequency band. These changes occurred regardless, and independent of, changes in power due to the sleep deprivation procedure.
The findings indicate that sleep deprivation most strongly affects the functional connectivity of prefrontal cortical areas. The findings extend those of previous studies, which showed sleep deprivation to predominantly affect functions mediated by the prefrontal cortex, such as working memory. Together, these findings suggest that the restorative effect of sleep is especially relevant for the maintenance of functional connectivity of prefrontal brain regions.
- Gujar N, Yoo SS, Hu P, Walker MP: The unrested resting brain: sleep deprivation alters activity within the default-mode network. J Cogn Neurosci 2010, 22:1637–1648. 10.1162/jocn.2009.21331 CrossRef
- Chee MWL, Chuah LYM: Functional neuroimaging insights into how sleep and sleep deprivation affect memory and cognition. Curr Opin Neurol 2008, 21:417–423. CrossRef
- De Havas JA, Parimal S, Soon CS, Chee MW: Sleep deprivation reduces default mode network connectivity and anti-correlation during rest and task performance. NeuroImage 2012, 59:1745–1751. 10.1016/j.neuroimage.2011.08.026 CrossRef
- Koenis MM, Romeijn N, Piantoni G, Verweij I, van der Werf YD, van Someren EJW, Stam CJ: Does sleep restore the topology of functional brain networks? Hum Brain Mapp 2013, 34:487–500. 10.1002/hbm.21455 CrossRef
- Horovitz SG, Braun AR, Carr WS, Picchioni D, Balkin TJ, Fukunaga M, Duyn JH: Decoupling of the brain’s default mode network during deep sleep. Proc Natl Acad Sci U S A 2009, 106:11376–11381. 10.1073/pnas.0901435106 CrossRef
- Horovitz SG, Fukunaga M, de Zwart JA, van Gelderen P, Fulton SC, Balkin TJ, Duyn JH: Low frequency BOLD fluctuations during resting wakefulness and light sleep: a simultaneous EEG-fMRI study. Hum Brain Mapp 2008, 29:671–682. 10.1002/hbm.20428 CrossRef
- Shao Y, Wang L, Ye E, Jin X, Ni W, Yang Y, Wen B, Hu D, Yang Z: Decreased thalamocortical functional connectivity after 36 hours of total sleep deprivation: evidence from resting state fMRI. Plos One 2013, 8:e78830. 10.1371/journal.pone.0078830 CrossRef
- Watts DJ, Strogatz SH: Collective dynamics of ‘small-world’ networks. Nature 1998, 393:440–442. 10.1038/30918 CrossRef
- Bullmore E, Sporns O: Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 2009, 10:186–198. 10.1038/nrn2575 CrossRef
- Latora V, Marchiori M: Efficient behavior of small-world networks. Phys Rev Lett 2001, 87:198701. CrossRef
- Reijneveld JC, Ponten SC, Berendse HW, Stam CJ: The application of graph theoretical analysis to complex networks in the brain. Clin Neurophysiol 2007, 118:2317–2331. 10.1016/j.clinph.2007.08.010 CrossRef
- Ferri R, Rundo F, Bruni O, Terzano MG, Stam CJ: The functional connectivity of different EEG bands moves towards small-world network organization during sleep. Clin Neurophysiol 2008, 119:2026–2036. 10.1016/j.clinph.2008.04.294 CrossRef
- Tononi G, Cirelli C: Sleep and synaptic homeostasis: a hypothesis. Brain Res Bull 2003, 62:143–150. 10.1016/j.brainresbull.2003.09.004 CrossRef
- Tononi G, Cirelli C: Sleep function and synaptic homeostasis. Sleep Med Rev 2006, 10:49–62. 10.1016/j.smrv.2005.05.002 CrossRef
- Samann PG, Tully C, Spoormaker VI, Wetter TC, Holsboer F, Wehrle R, Czisch ML: Increased sleep pressure reduces resting state functional connectivity. MAGMA 2010, 23:375–389. 10.1007/s10334-010-0213-z CrossRef
- Buckner RL, Andrews-Hanna JR, Schacter DL: The brain’s default network - Anatomy, function, and relevance to disease. Ann N Y Acad Sci 2008, 1124:1–38. 10.1196/annals.1440.011 CrossRef
- Harrison Y, Horne JA, Rothwell A: Prefrontal neuropsychological effects of sleep deprivation in young adults - a model for healthy aging? Sleep 2000, 23:1067–1073.
- Yoo SS, Gujar N, Hu P, Jolesz FA, Walker MP: The human emotional brain without sleep - a prefrontal amygdala disconnect. Curr Biol 2007, 17:R877-R878. 10.1016/j.cub.2007.08.007 CrossRef
- Spreng RN, Stevens WD, Chamberlain JP, Gilmore AW, Schacter D: Default network activity, coupled with the frontoparietal control network, supports goal-directed cognition. Neuroimage 2010, 53:303–317. 10.1016/j.neuroimage.2010.06.016 CrossRef
- Vincent JL, Kahn I, Snyder AZ, Raichle ME, Buckner RL: Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. J Neurophysiol 2008, 100:3328–3342. 10.1152/jn.90355.2008 CrossRef
- Cajochen C, Foy R, Dijk DJ: Frontal predominance of a relative increase in sleep delta and theta EEG activity after sleep loss in humans. Sleep Res Online 1999, 2:65–69.
- Finelli LA, Baumann H, Borbely AA, Achermann P: Dual electroencephalogram markers of human sleep homeostasis: correlation between theta activity in waking and slow-wave activity in sleep. Neurosci 2000, 101:523–529. 10.1016/S0306-4522(00)00409-7 CrossRef
- Strijkstra AM, Beersma DG, Drayer B, Halbesma N, Daan S: Subjective sleepiness correlates negatively with global alpha (8–12 Hz) and positively with central frontal theta (4–8 Hz) frequencies in the human resting awake electroencephalogram. Neurosci Lett 2003, 340:17–20. 10.1016/S0304-3940(03)00033-8 CrossRef
- Goncalves SI, de Munck JC, Pouwels PJ, Schoonhoven R, Kuijer JP, Maurits NM, Hoogduin JM, van Someren EJ, Heethaar RM, da Silva FH L: Correlating the alpha rhythm to BOLD using simultaneous EEG/fMRI: inter-subject variability. Neuroimage 2006, 30:203–213. 10.1016/j.neuroimage.2005.09.062 CrossRef
- Laufs H, Holt JL, Elfont R, Krams M, Paul JS, Krakow K, Kleinschmidt A: Where the BOLD signal goes when alpha EEG leaves. Neuroimage 2006, 31:1408–1418. 10.1016/j.neuroimage.2006.02.002 CrossRef
- Scheeringa R, Bastiaansen MCM, Petersson KM, Oostenveld R, Norris DG, Hagoort P: Frontal theta EEG activity correlates negatively with the default mode network in resting state. Int J Psychophysiol 2008, 67:242–251. 10.1016/j.ijpsycho.2007.05.017 CrossRef
- Riedner BA, Vyazovskiy VV, Huber R, Massimini M, Esser S, Murphy M, Tononi G: Sleep homeostasis and cortical synchronization: III. A high-density EEG study of sleep slow waves in humans. Sleep 2007, 30:1643–1657.
- Maquet P, Degueldre C, Delfiore G, Aerts J, Péters JM, Luxen A, Franck G: Functional neuroanatomy of human slow wave sleep. J Neurosci 1997, 17:2807–2812.
- Mander BA, Reid KJ, Baron KG, Tjoa T, Parrish TB, Paller KA, Gitelman DR, Zee PC: EEG measures index neural and cognitive recovery from sleep deprivation. J Neurosci 2010, 30:2686–2693. 10.1523/JNEUROSCI.4010-09.2010 CrossRef
- Huber R, Ghilardi MF, Massimini M, Tononi G: Local sleep and learning. Nature 2004, 430:78–81. 10.1038/nature02663 CrossRef
- 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: Spontaneous neural activity during human slow wave sleep. Proc Natl Acad Sci U S A 2008, 105:15160–15165. 10.1073/pnas.0801819105 CrossRef
- Van Der Werf YD, Altena E, Schoonheim MM, Sanz-Arigita EJ, Vis JC, De Rijke W, Van Someren EJ: Sleep benefits subsequent hippocampal functioning. Nat Neurosci 2009, 12:122–123. 10.1038/nn.2253 CrossRef
- Romeijn N, Raymann RJEM, Møst E, Te Lindert B, Van Der Meijden WP, Fronczek R, Gomez-Herrero G, Van Someren EJ: Sleep, vigilance, and thermosensitivity. Pflug Arch Eur J Phy 2012, 463:169–176. 10.1007/s00424-011-1042-2 CrossRef
- Delorme A, Makeig S: EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 2004, 134:9–21. 10.1016/j.jneumeth.2003.10.009 CrossRef
- Oostenveld R, Fries P, Maris E, Schoffelen JM: FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011, 2011:156869.
- Jung TP, Makeig S, Humphries C, Lee TW, McKeown MJ, Iragui V, Sejnowski TJ: Removing electroencephalographic artifacts by blind source separation. Psychophysiology 2000, 37:163–178. 10.1016/S0167-8760(00)00088-X CrossRef
- Stam CJ, van Dijk BW: Synchronization Likelihood: an unbiased measure of generalized synchronization in multivariate datasets. Physica D 2002, 163:236–251. 10.1016/S0167-2789(01)00386-4 CrossRef
- Bartolomei F, Bosma I, Klein M, Baayen JC, Reijneveld JC, Postma TJ, Heimans JJ, van Dijk BW, de Munck JC, de Jongh A, Cover KS, Stam CJ: Disturbed functional connectivity in brain tumour patients: evaluation by graph analysis of synchronization matrices. Clin Neurophysiol 2006, 117:2039–2049. 10.1016/j.clinph.2006.05.018 CrossRef
- Smit DJA, Stam CJ, Posthuma D, Boomsma DI, De Geus EJC: Heritability of ‘small-world’ networks in the brain: a graph theoretical analysis of resting-state EEG functional connectivity. Behav Genet 2007, 37:794–795.
- Montez T, Linkenkaer-Hansen K, van Dijk BW, Stam CJ: Synchronization likelihood with explicit time-frequency priors. Neuroimage 2006, 33:1117–1125. 10.1016/j.neuroimage.2006.06.066 CrossRef
- Newman MEJ: The structure and function of complex networks. Siam Review 2003, 45:167–256. 10.1137/S003614450342480 CrossRef
- Maris E, Oostenveld R: Nonparametric statistical testing of EEG- and MEG-data. J Neurosci Methods 2007, 163:161–175. 10.1016/j.jneumeth.2007.02.011 CrossRef
- Nolte G, Bai O, Wheaton L, Mari Z, Vorbach S, Hallett M: Identifying true brain interaction from EEG data using the imaginary part of coherency. Clin Neurophysiol 2004, 115:2292–2307. 10.1016/j.clinph.2004.04.029 CrossRef
- Sobel ME: Asymptotic intervals for indirect effects in structural equations models. In Sociological methodology. Edited by: Leinhart S. Washington, DC: American Sociological Association; 1982:290–312.
- Bates D, Maechler M, Bolker B: lme4: linear mixed-effects models using S4 classes. 2011.
- R Development Core Team: R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2013. URL http://www.R-project.org
- Welch PD: Use of fast fourier transform for estimation of power spectra: a method based on time averaging over short modified periodograms. IEEE T Audio Electroacustics 1967, Au15:70–73. CrossRef
- Tadel F, Baillet S, MOsher JC, Pantazis D, Leahy RM: Brainstorm: a user-friendly application for MEG/EEG analysis. Comput Intell Neurosci 2011, 2011:879716.
- Sleep deprivation leads to a loss of functional connectivity in frontal brain regions
- Open Access
- Available under Open Access This content is freely available online to anyone, anywhere at any time.
- Online Date
- July 2014
- Online ISSN
- BioMed Central
- Additional Links
- Sleep deprivation
- Brain connectivity
- Graph theory
- EEG analysis
- Small-world networks
- Author Affiliations
- 1. Netherlands Institute for Neuroscience, an Institute of the Royal Netherlands Academy of Arts and Sciences, Meibergdreef 47, 1105 BA, Amsterdam, the Netherlands
- 2. Department of Psychology, VU University, Amsterdam, the Netherlands
- 3. Department of Integrative Neurophysiology, Faculty of Earth and Life Sciences, VU University, Amsterdam, the Netherlands
- 4. Department of Medical Psychology, VU University Medical Centre, Amsterdam, the Netherlands
- 5. Department of Anatomy and Neurosciences, VU University Medical Centre, Amsterdam, the Netherlands