DOI QR코드

DOI QR Code

Computational electroencephalography analysis for characterizing brain networks

  • Sunwoo, Jun-Sang (Department of Neurosurgery, Seoul National University Hospital) ;
  • Cha, Kwang Su (Department of Neurology, Seoul National University Hospital) ;
  • Jung, Ki-Young (Department of Neurology, Seoul National University Hospital)
  • Received : 2020.08.26
  • Accepted : 2020.09.14
  • Published : 2020.10.31

Abstract

Electroencephalography (EEG) produces time-series data of neural oscillations in the brain, and is one of the most commonly used methods for investigating both normal brain functions and brain disorders. Quantitative EEG analysis enables identification of frequencies and brain activity that are activated or impaired. With studies on the structural and functional networks of the brain, the concept of the brain as a complex network has been fundamental to understand normal brain functions and the pathophysiology of various neurological disorders. Functional connectivity is a measure of neural synchrony in the brain network that refers to the statistical interdependency between neural oscillations over time. In this review, we first discuss the basic methods of EEG analysis, including preprocessing, spectral analysis, and functional-connectivity and graph-theory measures. We then review previous EEG studies of brain network characterization in several neurological disorders, including epilepsy, Alzheimer's disease, dementia with Lewy bodies, and idiopathic rapid eye movement sleep behavior disorder. Identifying the EEG-based network characteristics might improve the understanding of disease processes and aid the development of novel therapeutic approaches for various neurological disorders.

Keywords

References

  1. Hong SB, Jung KY. Basic electrophysiology of the electroencephalography. J Korean Neurol Assoc 2003;21:225-238.
  2. Buzsaki G, Anastassiou CA, Koch C. The origin of extracellular fields and currents--EEG, ECoG, LFP and spikes. Nat Rev Neurosci 2012;13:407-420. https://doi.org/10.1038/nrn3241
  3. Buzsaki G, Draguhn A. Neuronal oscillations in cortical networks. Science 2004;304:1926-1929. https://doi.org/10.1126/science.1099745
  4. Jensen O, Spaak E, Zumer JM. Human brain oscillations: from physiological mechanisms to analysis and cognition. In: Supek S, Aine CJ, eds. Magnetoencephalography: from signals to dynamic cortical networks. New York: Springer International Publishing, 2019;1-46.
  5. Jung KY. Characteristics and analysis methods of EEG signals. In: Korean EEG Study Group, ed. Art and application of EEG analysis: from basic to clinical research. Seoul: Daehan Medical Book Publishing, 2017;124-145.
  6. Stam CJ, van Straaten EC. The organization of physiological brain networks. Clin Neurophysiol 2012;123:1067-1087. https://doi.org/10.1016/j.clinph.2012.01.011
  7. Stam CJ. Modern network science of neurological disorders. Nat Rev Neurosci 2014;15:683-695. https://doi.org/10.1038/nrn3801
  8. 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. https://doi.org/10.1016/j.jneumeth.2003.10.009
  9. Makeig S, Bell AJ, Jung TP, Sejnowski TJ. Independent component analysis of electroencephalographic data. In: Mozer MC, Jordan MI, Petsche T, eds. Advances in Neural Information Processing Systems 9 (NIPS 1996). London: MIT Press, 1996;145-151.
  10. Jung TP, Makeig S, Humphries C, Lee TW, McKeown MJ, Iragui V, et al. Removing electroencephalographic artifacts by blind source separation. Psychophysiology 2000;37:163-178. https://doi.org/10.1016/S0167-8760(00)00088-X
  11. Crespo-Garcia M, Atienza M, Cantero JL. Muscle artifact removal from human sleep EEG by using independent component analysis. Ann Biomed Eng 2008;36:467-475. https://doi.org/10.1007/s10439-008-9442-y
  12. Polat K, Gunes S. Classification of epileptiform EEG using a hybrid system based on decision tree classifier and fast Fourier transform. Appl Math Comput 2007;187:1017-1026. https://doi.org/10.1016/j.amc.2006.09.022
  13. Mormann F, Lehnertz K, David P, Elger C. Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients. Physica D: Nonlinear Phenomena 2000;144:358-369. https://doi.org/10.1016/S0167-2789(00)00087-7
  14. Lachaux JP, Rodriguez E, Martinerie J, Varela FJ. Measuring phase synchrony in brain signals. Hum Brain Mapp 1999;8:194-208. https://doi.org/10.1002/(SICI)1097-0193(1999)8:4<194::AID-HBM4>3.0.CO;2-C
  15. Doesburg SM, Emberson LL, Rahi A, Cameron D, Ward LM. Asynchrony from synchrony: long-range gamma-band neural synchrony accompanies perception of audiovisual speech asynchrony. Exp Brain Res 2008;185:11-20. https://doi.org/10.1007/s00221-007-1127-5
  16. Vinck M, Oostenveld R, van Wingerden M, Battaglia F, Pennartz CM. An improved index of phase-synchronization for electrophysiological data in the presence of volume-conduction, noise and sample-size bias. Neuroimage 2011;55:1548-1565. https://doi.org/10.1016/j.neuroimage.2011.01.055
  17. Bullmore E, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 2009;10:186-198. https://doi.org/10.1038/nrn2575
  18. Stam CJ, Reijneveld JC. Graph theoretical analysis of complex networks in the brain. Nonlinear Biomed Phys 2007;1:3. https://doi.org/10.1186/1753-4631-1-3
  19. Fisher RS, Acevedo C, Arzimanoglou A, Bogacz A, Cross JH, Elger CE, et al. ILAE official report: a practical clinical definition of epilepsy. Epilepsia 2014;55:475-482. https://doi.org/10.1111/epi.12550
  20. Kramer MA, Cash SS. Epilepsy as a disorder of cortical network organization. Neuroscientist 2012;18:360-372. https://doi.org/10.1177/1073858411422754
  21. Bartolomei F, Wendling F, Regis J, Gavaret M, Guye M, Chauvel P. Pre-ictal synchronicity in limbic networks of mesial temporal lobe epilepsy. Epilepsy Res 2004;61:89-104. https://doi.org/10.1016/j.eplepsyres.2004.06.006
  22. Bettus G, Wendling F, Guye M, Valton L, Regis J, Chauvel P, et al. Enhanced EEG functional connectivity in mesial temporal lobe epilepsy. Epilepsy Res 2008;81:58-68. https://doi.org/10.1016/j.eplepsyres.2008.04.020
  23. Bernhardt B, Hong SJ, Bernasconi A, Bernasconi N. Imaging structural and functional brain networks in temporal lobe epilepsy. Front Hum Neurosci 2013;7:624. https://doi.org/10.3389/fnhum.2013.00624
  24. Bonilha L, Helpern JA, Sainju R, Nesland T, Edwards JC, Glazier SS, et al. Presurgical connectome and postsurgical seizure control in temporal lobe epilepsy. Neurology 2013;81:1704-1710. https://doi.org/10.1212/01.wnl.0000435306.95271.5f
  25. Lagarde S, Roehri N, Lambert I, Trebuchon A, McGonigal A, Carron R, et al. Interictal stereotactic-EEG functional connectivity in refractory focal epilepsies. Brain 2018;141:2966-2980. https://doi.org/10.1093/brain/awy214
  26. Horstmann MT, Bialonski S, Noennig N, Mai H, Prusseit J, Wellmer J, et al. State dependent properties of epileptic brain networks: comparative graph-theoretical analyses of simultaneously recorded EEG and MEG. Clin Neurophysiol 2010;121:172-185. https://doi.org/10.1016/j.clinph.2009.10.013
  27. Quraan MA, McCormick C, Cohn M, Valiante TA, McAndrews MP. Altered resting state brain dynamics in temporal lobe epilepsy can be observed in spectral power, functional connectivity and graph theory metrics. PLoS One 2013;8:e68609. https://doi.org/10.1371/journal.pone.0068609
  28. Wilke C, Worrell G, He B. Graph analysis of epileptogenic networks in human partial epilepsy. Epilepsia 2011;52:84-93. https://doi.org/10.1111/j.1528-1167.2010.02785.x
  29. Reitz C, Brayne C, Mayeux R. Epidemiology of Alzheimer disease. Nat Rev Neurol 2011;7:137-152. https://doi.org/10.1038/nrneurol.2011.2
  30. Jeong J. EEG dynamics in patients with Alzheimer's disease. Clin Neurophysiol 2004;115:1490-1505. https://doi.org/10.1016/j.clinph.2004.01.001
  31. Stam CJ, van der Made Y, Pijnenburg YA, Scheltens P. EEG synchronization in mild cognitive impairment and Alzheimer's disease. Acta Neurol Scand 2003;108:90-96. https://doi.org/10.1034/j.1600-0404.2003.02067.x
  32. Stam CJ, Montez T, Jones BF, Rombouts SA, van der Made Y, Pijnenburg YA, et al. Disturbed fluctuations of resting state EEG synchronization in Alzheimer's disease. Clin Neurophysiol 2005;116:708-715. https://doi.org/10.1016/j.clinph.2004.09.022
  33. Stam CJ, Jones BF, Nolte G, Breakspear M, Scheltens P. Smallworld networks and functional connectivity in Alzheimer's disease. Cereb Cortex 2007;17:92-99. https://doi.org/10.1093/cercor/bhj127
  34. Stam CJ, de Haan W, Daffertshofer A, Jones BF, Manshanden I, van Cappellen van Walsum AM, et al. Graph theoretical analysis of magnetoencephalographic functional connectivity in Alzheimer's disease. Brain 2009;132(Pt 1):213-224. https://doi.org/10.1093/brain/awn262
  35. McKeith IG, Boeve BF, Dickson DW, Halliday G, Taylor JP, Weintraub D, et al. Diagnosis and management of dementia with Lewy bodies: Fourth consensus report of the DLB Consortium. Neurology 2017;89:88-100. https://doi.org/10.1212/WNL.0000000000004058
  36. Briel RC, McKeith IG, Barker WA, Hewitt Y, Perry RH, Ince PG, et al. EEG findings in dementia with Lewy bodies and Alzheimer's disease. J Neurol Neurosurg Psychiatry 1999;66:401-403. https://doi.org/10.1136/jnnp.66.3.401
  37. Bonanni L, Thomas A, Tiraboschi P, Perfetti B, Varanese S, Onofrj M. EEG comparisons in early Alzheimer's disease, dementia with Lewy bodies and Parkinson's disease with dementia patients with a 2-year follow-up. Brain 2008;131(Pt 3):690-705. https://doi.org/10.1093/brain/awm322
  38. van Dellen E, de Waal H, van der Flier WM, Lemstra AW, Slooter AJ, Smits LL, et al. Loss of EEG network efficiency is related to cognitive impairment in dementia with lewy bodies. Mov Disord 2015;30:1785-1793. https://doi.org/10.1002/mds.26309
  39. McCann H, Stevens CH, Cartwright H, Halliday GM. ${\alpha}$-Synucleinopathy phenotypes. Parkinsonism Relat Disord 2014;20 Suppl 1:S62-S67. https://doi.org/10.1016/S1353-8020(13)70017-8
  40. You S, Jeon SM, Cho YW. Rapid eye movement sleep behavior disorder. J Sleep Med 2018;15:1-7. https://doi.org/10.13078/jsm.18001
  41. Postuma RB, Iranzo A, Hu M, Hogl B, Boeve BF, Manni R, et al. Risk and predictors of dementia and parkinsonism in idiopathic REM sleep behaviour disorder: a multicentre study. Brain 2019;142:744-759. https://doi.org/10.1093/brain/awz030
  42. Fantini ML, Gagnon JF, Petit D, Rompre S, Decary A, Carrier J, et al. Slowing of electroencephalogram in rapid eye movement sleep behavior disorder. Ann Neurol 2003;53:774-780. https://doi.org/10.1002/ana.10547
  43. Rodrigues Brazete J, Gagnon JF, Postuma RB, Bertrand JA, Petit D, Montplaisir J. Electroencephalogram slowing predicts neurodegeneration in rapid eye movement sleep behavior disorder. Neurobiol Aging 2016;37:74-81. https://doi.org/10.1016/j.neurobiolaging.2015.10.007
  44. Sunwoo JS, Lee S, Kim JH, Lim JA, Kim TJ, Byun JI, et al. Altered functional connectivity in idiopathic rapid eye movement sleep behavior disorder: a resting-state EEG study. Sleep 2017 Apr 18. [Epub]. DOI:10.1093/sleep/zsx058.
  45. Olde Dubbelink KT, Stoffers D, Deijen JB, Twisk JW, Stam CJ, Hillebrand A, et al. Resting-state functional connectivity as a marker of disease progression in Parkinson's disease: a longitudinal MEG study. Neuroimage Clin 2013;2:612-619. https://doi.org/10.1016/j.nicl.2013.04.003