Skip to main content
Log in

Mapping Slow Waves by EEG Topography and Source Localization: Effects of Sleep Deprivation

  • Original Paper
  • Published:
Brain Topography Aims and scope Submit manuscript

Abstract

Slow waves are a salient feature of the electroencephalogram (EEG) during non-rapid eye movement (non-REM) sleep. The aim of this study was to assess the topography of EEG power and the activation of brain structures during slow wave sleep under normal conditions and after sleep deprivation. Sleep EEG recordings during baseline and recovery sleep after 40 h of sustained wakefulness were analyzed (eight healthy young men, 27 channel EEG). Power maps were computed for the first non-REM sleep episode (where sleep pressure is highest) in baseline and recovery sleep, at frequencies between 0.5 and 2 Hz. Power maps had a frontal predominance at all frequencies between 0.5 and 2 Hz. An additional occipital focus of activity was observed below 1 Hz. Power maps ≤ 1 Hz were not affected by sleep deprivation, whereas an increase in power was observed in the maps ≥ 1.25 Hz. Based on the response to sleep deprivation, low-delta (0.5–1 Hz) and mid-delta activity (1.25–2 Hz) were dissociated. Electrical sources within the cortex of low- and mid-delta activity were estimated using eLORETA. Source localization revealed a predominantly frontal distribution of activity for low-delta and mid-delta activity. Sleep deprivation resulted in an increase in source strength only for mid-delta activity, mainly in parietal and frontal regions. Low-delta activity dominated in occipital and temporal regions and mid-delta activity in limbic and frontal regions independent of the level of sleep pressure. Both, power maps and electrical sources exhibited trait-like aspects.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Sources of baseline and recovery of single individuals form a cluster indicated by different colors. (Color figure online)

Fig. 6

Sources in the two bands were normalized (activity across all voxels equals one) and the difference between low- and mid-delta activity was calculated (top row). Bottom row: significant log of F ratio at p < 0.05 (yellow areas correspond to low-delta > mid-delta activity; blue areas correspond to mid-delta activity > low-delta activity). Please note that the first panel of the statistics is a view from bottom and not from top. L left, R right, A anterior, S superior. (Color figure online)

Similar content being viewed by others

Abbreviations

EEG:

Electroencephalogram,

LORETA:

Low resolution brain electromagnetic tomography,

non-REM:

Non-rapid eye movement (sleep),

REM:

Rapid eye movement (sleep),

SEM:

Standard error of mean,

SWA:

Slow-wave activity (EEG power in 0.75–4.5 Hz range),

SWS:

Slow wave sleep

References

  • Achermann P, Borbély AA (1997) Low-frequency (< 1 Hz) oscillations in the human sleep electroencephalogram. Neuroscience 81:213–222

    Article  CAS  PubMed  Google Scholar 

  • Achermann P, Borbély AA (1998a) Coherence analysis of the human sleep electroencephalogram. Neuroscience 85:1195–1208

    Article  CAS  PubMed  Google Scholar 

  • Achermann P, Borbély AA (1998b) Temporal evolution of coherence and power in the human sleep electroencephalogram. J Sleep Res 7(Suppl 1):36–41

    Article  PubMed  Google Scholar 

  • Achermann P, Borbély AA (2017) Sleep homeostasis and models of sleep regulation. In: Kryger MH, Roth T, Dement W (eds) Principles and practice of sleep medicine, 6th edn., Elsevier, Philadelphia, PA, pp 377–387

    Chapter  Google Scholar 

  • Achermann P, Finelli LA, Borbely AA (2001) Unihemispheric enhancement of delta power in human frontal sleep EEG by prolonged wakefulness. Brain Res 913:220–223

    Article  CAS  PubMed  Google Scholar 

  • Adamczyk M, Ambrosius U, Lietzenmaier S, Wichniak A, Holsboer F, Friess E (2015) Genetics of rapid eye movement sleep in humans. Transl Psychiatry 5:e598. doi:10.1038/tp.2015.85

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ambrosius U et al (2008) Heritability of sleep electroencephalogram. Biol Psychiatry 64:344–348

    Article  PubMed  Google Scholar 

  • Amzica F, Steriade M (1998) Electrophysiological correlates of sleep delta waves. Electroencephalogr Clin Neurophysiol 107:69–83

    Article  CAS  PubMed  Google Scholar 

  • Bersagliere A, Achermann P (2010) Slow oscillations in human non-rapid eye movement sleep electroencephalogram: effects of increased sleep pressure. J Sleep Res 19:228–237

    Article  PubMed  Google Scholar 

  • Buckelmüller J, Landolt HP, Stassen HH, Achermann P (2006) Trait-like individual differences in the human sleep electroencephalogram. Neuroscience 138:351–356

    Article  PubMed  Google Scholar 

  • Cao L, Thut G, Gross J (2017) The role of brain oscillations in predicting self-generated sounds. Neuroimage 147:895–903. doi:10.1016/j.neuroimage.2016.11.001

    Article  PubMed  PubMed Central  Google Scholar 

  • Cash SS et al (2009) The human K-complex represents an isolated cortical down-state. Science 324:1084–1087

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clancy K, Ding M, Bernat E, Schmidt NB, Li W (2017) Restless ‘rest’: intrinsic sensory hyperactivity and disinhibition in post-traumatic stress disorder. Brain 140:2041–2050. doi:10.1093/brain/awx116

    Article  PubMed  Google Scholar 

  • Coatanhay A, Soufflet L, Staner L, Boeijinga P (2002) EEG source identification: frequency analysis during sleep. C R Biol 325:273–282

    Article  PubMed  Google Scholar 

  • Crunelli V, David F, Lorincz ML, Hughes SW (2015) The thalamocortical network as a single slow wave-generating unit. Curr Opin Neurobiol 31:72–80. doi:10.1016/j.conb.2014.09.001

    Article  CAS  PubMed  Google Scholar 

  • Csercsa R et al (2010) Laminar analysis of slow wave activity in humans. Brain 133:2814–2829

    Article  PubMed  PubMed Central  Google Scholar 

  • Dang-Vu TT et al (2008) Spontaneous neural activity during human slow wave sleep. Proc Natl Acad Sci USA 105:15160–15165. doi:10.1073/pnas.0801819105

    Article  PubMed  PubMed Central  Google Scholar 

  • De Gennaro L et al (2008) The electroencephalographic fingerprint of sleep is genetically determined: a twin study. Ann Neurol 64:455–460

    Article  PubMed  Google Scholar 

  • Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21

    Article  PubMed  Google Scholar 

  • Dierks T et al (2000) Spatial pattern of cerebral glucose metabolism (PET) correlates with localization of intracerebral EEG-generators in Alzheimer’s disease. Clin Neurophysiol 111:1817–1824

    Article  CAS  PubMed  Google Scholar 

  • Esser SK, Hill SL, Tononi G (2007) Sleep homeostasis and cortical synchronization: I. Modeling the effects of synaptic strength on sleep slow waves. Sleep 30:1617–1630

    Article  PubMed  PubMed Central  Google Scholar 

  • Finelli LA (2001) Functional mapping of the human brain during sleep and sleep deprivation Dissertation ETH no 14251

  • Finelli LA, Baumann H, Borbély AA, Achermann P (2000) Dual electroencephalogram markers of human sleep homeostasis: correlation between theta activity in waking and slow-wave activity in sleep. Neuroscience 101:523–529

    Article  CAS  PubMed  Google Scholar 

  • Finelli LA, Achermann P, Borbély AA (2001a) Individual ‘fingerprints’ in human sleep EEG topography. Neuropsychopharmacology 25:S57–S62

    Article  Google Scholar 

  • Finelli LA, Borbély AA, Achermann P (2001b) Functional topography of the human nonREM sleep electroencephalogram. Eur J Neurosci 13:2282–2290

    Article  CAS  PubMed  Google Scholar 

  • Frackowiak RSJ (ed) (2004) Human brain function. 2nd edn., Academic Press, London

    Google Scholar 

  • Frei E, Gamma A, Pascual-Marqui R, Lehmann D, Hell D, Vollenweider FX (2001) Localization of MDMA-induced brain activity in healthy volunteers using low resolution brain electromagnetic tomography (LORETA). Hum Brain Mapp 14:152–165

    Article  CAS  PubMed  Google Scholar 

  • Fuchs M, Kastner J, Wagner M, Hawes S, Ebersole JS (2002) A standardized boundary element method volume conductor model. Clin Neurophysiol 113:702–712

    Article  PubMed  Google Scholar 

  • Geiger A, Huber R, Kurth S, Ringli M, Jenni OG, Achermann P (2011) The sleep EEG as a marker of intellectual ability in school age children. Sleep 34:181–189

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin FH, Witzel T, Ahlfors SP, Stufflebeam SM, Belliveau JW, Hämäläinen MS (2006) Assessing and improving the spatial accuracy in MEG source localization by depth-weighted minimum-norm estimates. Neuroimage 31:160–171. doi:10.1016/j.neuroimage.2005.11.054

    Article  PubMed  Google Scholar 

  • Liu Q, Farahibozorg S, Porcaro C, Wenderoth N, Mantini D (2017) Detecting large-scale networks in the human brain using high-density electroencephalography. Hum Brain Mapp. doi:10.1002/hbm.23688

    Google Scholar 

  • Mander BA et al (2015) Beta-amyloid disrupts human NREM slow waves and related hippocampus-dependent memory consolidation. Nat Neurosci 18:1051–1057. doi:10.1038/nn.4035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maris E, Oostenveld R (2007) Nonparametric statistical testing of EEG- and MEG-data. J Neurosci Methods 164:177–190

    Article  PubMed  Google Scholar 

  • Marzano C, Ferrara M, Curcio G, De Gennaro L (2010) The effects of sleep deprivation in humans: topographical electroencephalogram changes in non-rapid eye movement (NREM) sleep versus REM sleep. J Sleep Res 19:260–268

    Article  PubMed  Google Scholar 

  • Massimini M, Huber R, Ferrarelli F, Hill S, Tononi G (2004) The sleep slow oscillation as a traveling wave. J Neurosci 24:6862–6870

    Article  CAS  PubMed  Google Scholar 

  • Massimini M, Ferrarelli F, Huber R, Esser SK, Singh H, Tononi G (2005) Breakdown of cortical effective connectivity during sleep. Science 309:2228–2232

    Article  CAS  PubMed  Google Scholar 

  • Mazziotta J et al (2001) A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos Trans R Soc Lond B Biol Sci 356:1293–1322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moroni F et al (2007) Sleep in the human hippocampus: a stereo-EEG study. PLoS ONE 2:e867

    Article  PubMed  PubMed Central  Google Scholar 

  • Mulert C et al (2004) Integration of fMRI and simultaneous EEG: towards a comprehensive understanding of localization and time-course of brain activity in target detection. Neuroimage 22:83–94

    Article  PubMed  Google Scholar 

  • Murphy M, Riedner BA, Huber R, Massimini M, Ferrarelli F, Tononi G (2009) Source modeling sleep slow waves. Proc Natl Acad Sci USA 106:1608–1613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15:1–25

    Article  PubMed  Google Scholar 

  • Nir Y, Staba RJ, Andrillon T, Vyazovskiy VV, Cirelli C, Fried I, Tononi G (2011) Regional slow waves and spindles in human sleep. Neuron 70:153–169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parrino L, Spaggiari MC, Boselli M, Barusi R, Terzano MG (1993) Effects of prolonged wakefulness on cyclic alternating pattern (Cap) during sleep recovery at different circadian phases. J Sleep Res 2:91–95

    Article  CAS  PubMed  Google Scholar 

  • Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24(Suppl D):5–12

    PubMed  Google Scholar 

  • Pascual-Marqui RD (2007) Discrete, 3D distributed, linear imaging methods of electric neuronal activity. Part 1: exact, zero error localization. arXiv:07103341 [math-ph], http://arxiv.org/pdf/07103341

  • Pascual-Marqui RD (2009) Theory of the EEG inverse problem. In: Tong S, Thakor N (eds) Quantitative EEG analysis: methods and applications, Artech House, Boston, pp 121–140

    Google Scholar 

  • Pascual-Marqui RD, Michel CM, Lehmann D (1994) Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. Int J Psychophysiol 18:49–65

    Article  CAS  PubMed  Google Scholar 

  • Pascual-Marqui RD et al (2011) Assessing interactions in the brain with exact low resolution electromagnetic tomography (eLORETA). Philos Trans A Math Phys Eng Sci 369:3768–3784. doi: 10.1098/rsta.2011.0081

    Article  PubMed  Google Scholar 

  • Plummer C et al (2010) Clinical utility of distributed source modelling of interictal scalp EEG in focal epilepsy. Clin Neurophysiol 121:1726–1739

    Article  CAS  PubMed  Google Scholar 

  • Poryazova R, Werth E, Parrino L, Terzano MG, Bassetti CL (2011) Cyclic alternating pattern in narcolepsy patients and healthy controls after partial and total sleep deprivation. Clin Neurophysiol 122:1788–1793. doi:10.1016/j.clinph.2011.02.028

    Article  PubMed  Google Scholar 

  • Rechtschaffen A, Kales A (1968) A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. National Institutes of Health, Bethesda, Maryland

    Google Scholar 

  • Riedner BA, Vyazovskiy VV, Huber R, Massimini M, Esser S, Murphy M, Tononi G (2007) Sleep homeostasis and cortical synchronization: III. A high-density EEG study of sleep slow waves in humans. Sleep 30:1643–1657

    Article  PubMed  PubMed Central  Google Scholar 

  • Saletin JM, van der Helm E, Walker MP (2013) Structural brain correlates of human. sleep oscillations. Neuroimage 83:658–668. doi:10.1016/j.neuroimage.2013.06.021

    Article  PubMed  PubMed Central  Google Scholar 

  • Steriade M, McCormick DA, Sejnowski TJ (1993a) Thalamocortical oscillations in the sleeping and aroused brain. Science 262:679–685

    Article  CAS  PubMed  Google Scholar 

  • Steriade M, Nuñez A, Amzica F (1993b) A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13:3252–3265

    CAS  PubMed  Google Scholar 

  • Steriade M, Nuñez A, Amzica F (1993c) Intracellular analysis of relations between the slow (< 1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram. J Neurosci 13:3266–3283

    CAS  PubMed  Google Scholar 

  • Tan HR, Gross J, Uhlhaas PJ (2015) MEG-measured auditory steady-state oscillations show high test-retest reliability: a sensor and source-space. analysis. Neuroimage 122:417–426. doi:10.1016/j.neuroimage.2015.07.055

    Article  PubMed  Google Scholar 

  • Tarokh L, Carskadon MA, Achermann P (2011) Trait-like characteristics of the sleep EEG across adolescent development. J Neurosci 31:6371–6378. doi:10.1523/JNEUROSCI.5533-10.2011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tarokh L, Rusterholz T, Achermann P, Van Dongen HP (2015) The spectrum of the non-rapid eye movement sleep electroencephalogram following total sleep deprivation is trait-like. J Sleep Res 24:360–363. doi:10.1111/jsr.12279

    Article  PubMed  Google Scholar 

  • Terzano MG et al (2002) Atlas, rules, and recording techniques for the scoring of cyclic alternating pattern (CAP) in human sleep. Sleep Med 3:187–199. doi:10.1016/S1389-9457(02)00003-5

    Article  PubMed  Google Scholar 

  • Tononi G, Cirelli C (2006) Sleep function and synaptic homeostasis. Sleep Med Rev 10:49–62

    Article  PubMed  Google Scholar 

  • Tononi G, Cirelli C (2014) Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation. and integration. Neuron 81:12–34. doi:10.1016/j.neuron.2013.12.025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tucker AM, Dinges DF, Van Dongen HP (2007) Trait interindividual differences in the sleep physiology of healthy young adults. J Sleep Res 16:170–180. doi:10.1111/j.1365-2869.2007.00594.x

    Article  PubMed  Google Scholar 

  • Vitacco D, Brandeis D, Pascual-Marqui R, Martin E (2002) Correspondence of event-related potential tomography and functional magnetic resonance imaging during language processing. Hum Brain Mapp 17:4–12

    Article  PubMed  Google Scholar 

  • Vyazovskiy VV, Harris KD (2013) Sleep and the single neuron: the role of global slow oscillations in individual cell rest. Nat Rev Neurosci 14:443–451. doi:10.1038/nrn3494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vyazovskiy VV, Riedner BA, Cirelli C, Tononi G (2007) Sleep homeostasis and cortical synchronization: II. A local field potential study of sleep slow waves in the rat. Sleep 30:1631–1642

    Article  PubMed  PubMed Central  Google Scholar 

  • Vyazovskiy VV, Faraguna U, Cirelli C, Tononi G (2009a) Triggering slow waves during NREM sleep in the rat by intracortical electrical stimulation: effects of sleep/wake history and background activity. J Neurophysiol 101:1921–1931

    Article  PubMed  PubMed Central  Google Scholar 

  • Vyazovskiy VV et al (2009b) Cortical firing sleep homeostasis. Neuron 63:865–878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Worrell GA, Lagerlund TD, Sharbrough FW, Brinkmann BH, Busacker NE, Cicora KM, O’Brien TJ (2000) Localization of the epileptic focus by low-resolution electromagnetic tomography in patients with a lesion demonstrated by MRI. Brain Topogr 12:273–282

    Article  CAS  PubMed  Google Scholar 

  • Yang L, Wilke C, Brinkmann B, Worrell GA, He B (2011) Dynamic imaging of ictal oscillations using non-invasive high-resolution EEG. Neuroimage 56:1908–1917. doi: 10.1016/j.neuroimage.2011.03.043

    Article  PubMed  PubMed Central  Google Scholar 

  • Zumsteg D, Wennberg RA, Treyer V, Buck A, Wieser HG (2005) H2 15O or 13NH3 PET and electromagnetic tomography (LORETA) during partial status epilepticus. Neurology 65:1657–1660

    Article  CAS  PubMed  Google Scholar 

  • Zumsteg D, Friedman A, Wieser HG, Wennberg RA (2006a) Propagation of interictal discharges in temporal lobe epilepsy: correlation of spatiotemporal mapping with intracranial foramen ovale electrode recordings. Clin Neurophysiol 117:2615–2626

    Article  PubMed  Google Scholar 

  • Zumsteg D, Lozano AM, Wennberg RA (2006b) Depth electrode recorded cerebral responses with deep brain stimulation of the anterior thalamus for epilepsy. Clin Neurophysiol 117:1602–1609

    Article  PubMed  Google Scholar 

  • Zumsteg D, Lozano AM, Wieser HG, Wennberg RA (2006c) Cortical activation with deep brain stimulation of the anterior thalamus for epilepsy. Clin Neurophysiol 117:192–207

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Dr. Alexander Borbély for comments on the manuscript. The study was supported by the Swiss National Science Foundation Grant 320030-130766 and 32003B_146643.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peter Achermann.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 551 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bersagliere, A., Pascual-Marqui, R.D., Tarokh, L. et al. Mapping Slow Waves by EEG Topography and Source Localization: Effects of Sleep Deprivation. Brain Topogr 31, 257–269 (2018). https://doi.org/10.1007/s10548-017-0595-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10548-017-0595-6

Keywords

Navigation