Clinical Implications of EEG and ERP as Biological Markers for Alzheimer's Disease and Mild Cognitive Impairment

경도인지장애와 알츠하이머병 치매의 생물학적 표지자로서 뇌파와 사건유발전위의 임상적 의미

  • Kim, Chang Gyu (Clinical Emotion and Cognition Research Laboratory (CEC Lab), Inje University) ;
  • Kim, Hyun-Taek (Department of Psychology, Korea University) ;
  • Lee, Seung-Hwan (Clinical Emotion and Cognition Research Laboratory (CEC Lab), Inje University)
  • 김창규 (인제대학교 임상감정인지기능연구소) ;
  • 김현택 (고려대학교 심리학과) ;
  • 이승환 (인제대학교 임상감정인지기능연구소)
  • Received : 2013.08.08
  • Accepted : 2013.09.30
  • Published : 2013.11.30

Abstract

Objectives Memory impairment is a very important mental health issue for elderly and adults. Mild cognitive impairment (MCI) is a prodromal stage of Alzheimer's disease (AD). Early detection of the prodromal stage of patients with AD is an important topic of interest for both mental health clinicians and policy makers. Methods Electroencephalograpgy (EEG) has been used as a possible biological marker for patients with MCI, and AD. In this review, we will summarize the clinical implications of EEG and ERP as a biological marker for AD and MCI. Results EEG power density, functional coupling, spectral coherence, synchronization, and connectivity were analyzed and proved their clinical efficacy in patients with the prodromal stage of AD. Serial studies on late event-related potentials (ERPs) were also conducted in MCI patients as well as healthy elders. Even though these EEG and ERP studies have some limitations for their design and method, their clinical implications are increasing rapidly. Conclusion EEG and ERP can be used as biological markers of AD and MCI. Also they can be used as useful tools for early detection of AD and MCI patients. They are useful and sensitive research tools for AD and MCI patients. However, some problems remain to be solved until they can be practical measures in clinical setting.

Keywords

References

  1. Basar E, Guntekin B. A review of brain oscillations in cognitive disorders and the role of neurotransmitters. Brain Res 2008;1235:172- 193. https://doi.org/10.1016/j.brainres.2008.06.103
  2. Ferri CP, Prince M, Brayne C, Brodaty H, Fratiglioni L, Ganguli M, et al. Global prevalence of dementia: a Delphi consensus study. Lancet 2005;366:2112-2117. https://doi.org/10.1016/S0140-6736(05)67889-0
  3. Clark CM, DeCarli C, Mungas D, Chui HI, Higdon R, Nunez J, et al. Earlier onset of Alzheimer disease symptoms in latino individuals compared with anglo individuals. Arch Neurol 2005;62:774-778. https://doi.org/10.1001/archneur.62.5.774
  4. Waldemar G, Dubois B, Emre M, Georges J, McKeith IG, Rossor M, et al. Recommendations for the diagnosis and management of Alzheimer' s disease and other disorders associated with dementia: EFNS guideline. Eur J Neurol 2007;14:e1-e26.
  5. Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E. Mild cognitive impairment: clinical characterization and outcome. Arch Neurol 1999;56:303-308. https://doi.org/10.1001/archneur.56.3.303
  6. Larrieu S, Letenneur L, Orgogozo JM, Fabrigoule C, Amieva H, Le Carret N, et al. Incidence and outcome of mild cognitive impairment in a population-based prospective cohort. Neurology 2002;59:1594- 1599. https://doi.org/10.1212/01.WNL.0000034176.07159.F8
  7. Petersen RC, Doody R, Kurz A, Mohs RC, Morris JC, Rabins PV, et al. Current concepts in mild cognitive impairment. Arch Neurol 2001;58:1985-1992. https://doi.org/10.1001/archneur.58.12.1985
  8. Wilson RS, Leurgans SE, Boyle PA, Bennett DA. Cognitive decline in prodromal Alzheimer disease and mild cognitive impairment. Arch Neurol 2011;68:351-356.
  9. Karrasch M, Sinervä E, Grönholm P, Rinne J, Laine M. CERAD test performances in amnestic mild cognitive impairment and Alzheimer' s disease. Acta Neurol Scand 2005;111:172-179. https://doi.org/10.1111/j.1600-0404.2005.00380.x
  10. Forlenza OV, Diniz BS, Gattaz WF. Diagnosis and biomarkers of predementia in Alzheimer' s disease. BMC Med 2010;8:89. https://doi.org/10.1186/1741-7015-8-89
  11. Drago V, Babiloni C, Bartrés-Faz D, Caroli A, Bosch B, Hensch T, et al. Disease tracking markers for Alzheimer' s disease at the prodromal (MCI) stage. J Alzheimers Dis 2011;26 Suppl 3:159-199.
  12. van Harten AC, Visser PJ, Pijnenburg YA, Teunissen CE, Blankenstein MA, Scheltens P, et al. Cerebrospinal fluid A$\beta$42 is the best predictor of clinical progression in patients with subjective complaints. Alzheimers Dement 2013;9:481-487. https://doi.org/10.1016/j.jalz.2012.08.004
  13. Shim YS, Morris JC. Biomarkers predicting Alzheimer' s disease in cognitively normal aging. J Clin Neurol 2011;7:60-68. https://doi.org/10.3988/jcn.2011.7.2.60
  14. Fagan AM, Roe CM, Xiong C, Mintun MA, Morris JC, Holtzman DM. Cerebrospinal fluid tau/beta-amyloid(42) ratio as a prediction of cognitive decline in nondemented older adults. Arch Neurol 2007; 64:343-349. https://doi.org/10.1001/archneur.64.3.noc60123
  15. Rossini PM, Dal Forno G. Integrated technology for evaluation of brain function and neural plasticity. Phys Med Rehabil Clin N Am 2004;15:263-306. https://doi.org/10.1016/S1047-9651(03)00124-4
  16. Celesia GG, Kaufman D, Cone S. Effects of age and sex on pattern electroretinograms and visual evoked potentials. Electroencephalogr Clin Neurophysiol 1987;68:161-171. https://doi.org/10.1016/0168-5597(87)90023-2
  17. Rossini PM. Implications of brain plasticity to brain-machine interfaces operation a potential paradox? Int Rev Neurobiol 2009;86:81- 90. https://doi.org/10.1016/S0074-7742(09)86006-6
  18. Klimesch W. EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Brain Res Rev 1999;29:169-195. https://doi.org/10.1016/S0165-0173(98)00056-3
  19. Klimesch W, Doppelmayr M, Schimke H, Ripper B. Theta synchronization and alpha desynchronization in a memory task. Psychophysiology 1997;34:169-176. https://doi.org/10.1111/j.1469-8986.1997.tb02128.x
  20. Klimesch W, Schimke H, Schwaiger J. Episodic and semantic memory: an analysis in the EEG theta and alpha band. Electroencephalogr Clin Neurophysiol 1994;91:428-441. https://doi.org/10.1016/0013-4694(94)90164-3
  21. Sauseng P, Klimesch W, Doppelmayr M, Pecherstorfer T, Freunberger R, Hanslmayr S. EEG alpha synchronization and functional coupling during top-down processing in a working memory task. Hum Brain Mapp 2005;26:148-155. https://doi.org/10.1002/hbm.20150
  22. Yordanova JY, Kolev VN, Başar E. EEG theta and frontal alpha oscillations during auditory processing change with aging. Electroencephalogr Clin Neurophysiol 1998;108:497-505. https://doi.org/10.1016/S0168-5597(98)00028-8
  23. Yordanova J, Rosso OA, Kolev V. A transient dominance of theta event-related brain potential component characterizes stimulus processing in an auditory oddball task. Clin Neurophysiol 2003;114: 529-540. https://doi.org/10.1016/S1388-2457(02)00415-7
  24. Kim SP, Kang JH, Choe SH, Jeong JW, Kim HT, Yun K, et al. Modulation of theta phase synchronization in the human electroencephalogram during a recognition memory task. Neuroreport 2012;23: 637-641. https://doi.org/10.1097/WNR.0b013e328354afed
  25. Stam CJ. Brain dynamics in theta and alpha frequency bands and working memory performance in humans. Neurosci Lett 2000;286: 115-118. https://doi.org/10.1016/S0304-3940(00)01109-5
  26. Weiss S, Rappelsberger P. Long-range EEG synchronization during word encoding correlates with successful memory performance. Brain Res Cogn Brain Res 2000;9:299-312. https://doi.org/10.1016/S0926-6410(00)00011-2
  27. Petsche H. [The EEG and thinking]. EEG EMG Z Elektroenzephalogr Elektromyogr Verwandte Geb 1990;21:207-218.
  28. Demiralp T, Bayraktaroglu Z, Lenz D, Junge S, Busch NA, Maess B, et al. Gamma amplitudes are coupled to theta phase in human EEG during visual perception. Int J Psychophysiol 2007;64:24-30. https://doi.org/10.1016/j.ijpsycho.2006.07.005
  29. Deiber MP, Missonnier P, Bertrand O, Gold G, Fazio-Costa L, Ibanez V, et al. Distinction between perceptual and attentional processing in working memory tasks: a study of phase-locked and induced oscillatory brain dynamics. J Cogn Neurosci 2007;19:158-172. https://doi.org/10.1162/jocn.2007.19.1.158
  30. Jensen O, Tesche CD. Frontal theta activity in humans increases with memory load in a working memory task. Eur J Neurosci 2002; 15:1395-1399. https://doi.org/10.1046/j.1460-9568.2002.01975.x
  31. Dujardin K, Bourriez JL, Guieu JD. Event-related desynchronization (ERD) patterns during verbal memory tasks: effect of age. Int J Psychophysiol 1994;16:17-27. https://doi.org/10.1016/0167-8760(94)90038-8
  32. Dujardin K, Bourriez JL, Guieu JD. Event-related desynchronization (ERD) patterns during memory processes: effects of aging and task difficulty. Electroencephalogr Clin Neurophysiol 1995;96:169- 182. https://doi.org/10.1016/0168-5597(94)00284-L
  33. Klass DW, Brenner RP. Electroencephalography of the elderly. J Clin Neurophysiol 1995;12:116-131. https://doi.org/10.1097/00004691-199503000-00002
  34. Babiloni C, Binetti G, Cassarino A, Dal Forno G, Del Percio C, Ferreri F, et al. Sources of cortical rhythms in adults during physiological aging: a multicentric EEG study. Hum Brain Mapp 2006;27: 162-172. https://doi.org/10.1002/hbm.20175
  35. Jelic V, Johansson SE, Almkvist O, Shigeta M, Julin P, Nordberg A, et al. Quantitative electroencephalography in mild cognitive impairment: longitudinal changes and possible prediction of Alzheimer' s disease. Neurobiol Aging 2000;21:533-540. https://doi.org/10.1016/S0197-4580(00)00153-6
  36. Coben LA, Danziger W, Storandt M. A longitudinal EEG study of mild senile dementia of Alzheimer type: changes at 1 year and at 2.5 years. Electroencephalogr Clin Neurophysiol 1985;61:101-112. https://doi.org/10.1016/0013-4694(85)91048-X
  37. Soininen H, Partanen J, Laulumaa V, Helkala EL, Laakso M, Riekkinen PJ. Longitudinal EEG spectral analysis in early stage of Alzheimer' s disease. Electroencephalogr Clin Neurophysiol 1989;72: 290-297. https://doi.org/10.1016/0013-4694(89)90064-3
  38. Luckhaus C, Grass-Kapanke B, Blaeser I, Ihl R, Supprian T, Winterer G, et al. Quantitative EEG in progressing vs stable mild cognitive impairment (MCI): results of a 1-year follow-up study. Int J Geriatr Psychiatry 2008;23:1148-1155. https://doi.org/10.1002/gps.2042
  39. Huang C, Wahlund L, Dierks T, Julin P, Winblad B, Jelic V. Discrimination of Alzheimer' s disease and mild cognitive impairment by equivalent EEG sources: a cross-sectional and longitudinal study. Clin Neurophysiol 2000;111:1961-1967. https://doi.org/10.1016/S1388-2457(00)00454-5
  40. 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
  41. Jeong J, Gore JC, Peterson BS. Mutual information analysis of the EEG in patients with Alzheimer' s disease. Clin Neurophysiol 2001; 112:827-835. https://doi.org/10.1016/S1388-2457(01)00513-2
  42. Jeong J, Chae JH, Kim SY, Han SH. Nonlinear dynamic analysis of the EEG in patients with Alzheimer' s disease and vascular dementia. J Clin Neurophysiol 2001;18:58-67. https://doi.org/10.1097/00004691-200101000-00010
  43. Babiloni C, Binetti G, Cassetta E, Dal Forno G, Del Percio C, Ferreri F, et al. Sources of cortical rhythms change as a function of cognitive impairment in pathological aging: a multicenter study. Clin Neurophysiol 2006;117:252-268. https://doi.org/10.1016/j.clinph.2005.09.019
  44. Babiloni C, Frisoni GB, Pievani M, Vecchio F, Lizio R, Buttiglione M, et al. Hippocampal volume and cortical sources of EEG alpha rhythms in mild cognitive impairment and Alzheimer disease. Neuroimage 2009;44:123-135. https://doi.org/10.1016/j.neuroimage.2008.08.005
  45. Babiloni C, Frisoni GB, Vecchio F, Pievani M, Geroldi C, De Carli C, et al. Global functional coupling of resting EEG rhythms is related to white-matter lesions along the cholinergic tracts in subjects with amnesic mild cognitive impairment. J Alzheimers Dis 2010; 19:859-871. https://doi.org/10.3233/JAD-2010-1290
  46. Babiloni C, Ferri R, Binetti G, Cassarino A, Dal Forno G, Ercolani M, et al. Fronto-parietal coupling of brain rhythms in mild cognitive impairment: a multicentric EEG study. Brain Res Bull 2006;69:63-73. https://doi.org/10.1016/j.brainresbull.2005.10.013
  47. Lee SH, Park YM, Kim DW, Im CH. Global synchronization index as a biological correlate of cognitive decline in Alzheimer' s disease. Neurosci Res 2010;66:333-339. https://doi.org/10.1016/j.neures.2009.12.004
  48. Park YM, Che HJ, Im CH, Jung HT, Bae SM, Lee SH. Decreased EEG synchronization and its correlation with symptom severity in Alzheimer' s disease. Neurosci Res 2008;62:112-117. https://doi.org/10.1016/j.neures.2008.06.009
  49. Babiloni C, Binetti G, Cassetta E, Cerboneschi D, Dal Forno G, Del Percio C, et al. Mapping distributed sources of cortical rhythms in mild Alzheimer' s disease. A multicentric EEG study. Neuroimage 2004;22:57-67. https://doi.org/10.1016/j.neuroimage.2003.09.028
  50. Kim JS, Lee SH, Park G, Kim S, Bae SM, Kim DW, et al. Clinical implications of quantitative electroencephalography and current source density in patients with Alzheimer' s disease. Brain Topogr 2012;25: 461-474. https://doi.org/10.1007/s10548-012-0234-1
  51. Papaliagkas V, Kimiskidis V, Tsolaki M, Anogianakis G. Usefulness of event-related potentials in the assessment of mild cognitive impairment. BMC Neurosci 2008;9:107. https://doi.org/10.1186/1471-2202-9-107
  52. Pogarell O, Mulert C, Hegerl U. Event related potentials and fMRI in neuropsychopharmacology. Clin EEG Neurosci 2006;37:99-107. https://doi.org/10.1177/155005940603700207
  53. Meador KJ, Loring DW, Davis HC, Sethi KD, Patel BR, Adams RJ, et al. Cholinergic and serotonergic effects on the P3 potential and recent memory. J Clin Exp Neuropsychol 1989;11:252-260. https://doi.org/10.1080/01688638908400887
  54. Neshige R, Barrett G, Shibasaki H. Auditory long latency event-related potentials in Alzheimer' s disease and multi-infarct dementia. J Neurol Neurosurg Psychiatry 1988;51:1120-1125. https://doi.org/10.1136/jnnp.51.9.1120
  55. Onofrj M, Thomas A, Luciano AL, Iacono D, Di Rollo A, D' Andreamatteo G, et al. Donepezil versus vitamin E in Alzheimer' s disease: Part 2: mild versus moderate-severe Alzheimer' s disease. Clin Neuropharmacol 2002;25:207-215. https://doi.org/10.1097/00002826-200207000-00004
  56. Reeves RR, Struve FA, Patrick G, Booker JG, Nave DW. The effects of donepezil on the P300 auditory and visual cognitive evoked potentials of patients with Alzheimer' s disease. Am J Geriatr Psychiatry 1999;7:349-352.
  57. Thomas A, Iacono D, Bonanni L, D' Andreamatteo G, Onofrj M. Donepezil, rivastigmine, and vitamin E in Alzheimer disease: a combined P300 event-related potentials/neuropsychologic evaluation over 6 months. Clin Neuropharmacol 2001;24:31-42. https://doi.org/10.1097/00002826-200101000-00007
  58. Werber AE, Klein C, Rabey JM. Evaluation of cholinergic treatment in demented patients by P300 evoked related potentials. Neurol Neurochir Pol 2001;35 Suppl 3:37-43.
  59. Werber EA, Gandelman-Marton R, Klein C, Rabey JM. The clinical use of P300 event related potentials for the evaluation of cholinesterase inhibitors treatment in demented patients. J Neural Transm 2003; 110:659-669. https://doi.org/10.1007/s00702-003-0817-9
  60. Golob EJ, Ringman JM, Irimajiri R, Bright S, Schaffer B, Medina LD, et al. Cortical event-related potentials in preclinical familial Alzheimer disease. Neurology 2009;73:1649-1655. https://doi.org/10.1212/WNL.0b013e3181c1de77
  61. Green J, Levey AI. Event-related potential changes in groups at increased risk for Alzheimer disease. Arch Neurol 1999;56:1398-1403. https://doi.org/10.1001/archneur.56.11.1398
  62. Portaccio E, Zipoli V, Goretti B, Hakiki B, Nacmias B, Siracusa G, et al. ApolipoproteinE epsilon 4 allele is not associated with disease course and severity in multiple sclerosis. Acta Neurol Scand 2009; 120:439-441. https://doi.org/10.1111/j.1600-0404.2009.01278.x
  63. Chapman RM, McCrary JW, Gardner MN, Sandoval TC, Guillily MD, Reilly LA, et al. Brain ERP components predict which individuals progress to Alzheimer' s disease and which do not. Neurobiol Aging 2011;32:1742-1755. https://doi.org/10.1016/j.neurobiolaging.2009.11.010
  64. Gironell A, García-Sánchez C, Estévez-González A, Boltes A, Kulisevsky J. Usefulness of p300 in subjective memory complaints: a prospective study. J Clin Neurophysiol 2005;22:279-284. https://doi.org/10.1097/01.WNP.0000173559.60113.AB
  65. Golob EJ, Irimajiri R, Starr A. Auditory cortical activity in amnestic mild cognitive impairment: relationship to subtype and conversion to dementia. Brain 2007;130(Pt 3):740-752. https://doi.org/10.1093/brain/awl375
  66. Olichney JM, Taylor JR, Gatherwright J, Salmon DP, Bressler AJ, Kutas M, et al. Patients with MCI and N400 or P600 abnormalities are at very high risk for conversion to dementia. Neurology 2008; 70(19 Pt 2):1763-1770. https://doi.org/10.1212/01.wnl.0000281689.28759.ab
  67. Lee MS, Lee SH, Moon EO, Moon YJ, Kim S, Kim SH, et al. Neuropsychological correlates of the P300 in patients with Alzheimer' s disease. Prog Neuropsychopharmacol Biol Psychiatry 2013;40:62-69. https://doi.org/10.1016/j.pnpbp.2012.08.009
  68. Watts DJ, Strogatz SH. Collective dynamics of 'small-world' networks. Nature 1998;393:440-442. https://doi.org/10.1038/30918
  69. Rubinov M, Sporns O. Complex network measures of brain connectivity: uses and interpretations. Neuroimage 2010;52:1059-1069. https://doi.org/10.1016/j.neuroimage.2009.10.003
  70. Stam CJ, Jones BF, Nolte G, Breakspear M, Scheltens P. Small-world networks and functional connectivity in Alzheimer' s disease. Cereb Cortex 2007;17:92-99.
  71. 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
  72. de Haan W, Pijnenburg YA, Strijers RL, van der Made Y, van der Flier WM, Scheltens P, et al. Functional neural network analysis in frontotemporal dementia and Alzheimer' s disease using EEG and graph theory. BMC Neurosci 2009;10:101. https://doi.org/10.1186/1471-2202-10-101
  73. Ahmadlou M, Adeli H, Adeli A. New diagnostic EEG markers of the Alzheimer' s disease using visibility graph. J Neural Transm 2010; 117:1099-1109. https://doi.org/10.1007/s00702-010-0450-3
  74. Lai CL, Lin RT, Liou LM, Liu CK. The role of event-related potentials in cognitive decline in Alzheimer' s disease. Clin Neurophysiol 2010; 121:194-199. https://doi.org/10.1016/j.clinph.2009.11.001
  75. Papaliagkas VT, Kimiskidis VK, Tsolaki MN, Anogianakis G. Cognitive event-related potentials: longitudinal changes in mild cognitive impairment. Clin Neurophysiol 2011;122:1322-1326. https://doi.org/10.1016/j.clinph.2010.12.036
  76. Ball SS, Marsh JT, Schubarth G, Brown WS, Strandburg R. Longitudinal P300 latency changes in Alzheimer' s disease. J Gerontol 1989;44:M195-M200. https://doi.org/10.1093/geronj/44.6.M195
  77. Onofrj M, Gambi D, Del Re ML, Fulgente T, Bazzano S, Colamartino P, et al. Mapping of event-related potentials to auditory and visual odd-ball paradigms in patients affected by different forms of dementia. Eur Neurol 1991;31:259-269. https://doi.org/10.1159/000116687
  78. St Clair D, Blackburn I, Blackwood D, Tyrer G. Measuring the course of Alzheimer' s disease. A longitudinal study of neuropsychological function and changes in P3 event-related potential. Br J Psychiatry 1988;152:48-54. https://doi.org/10.1192/bjp.152.1.48
  79. Swanwick GR, Rowan MJ, Coen RF, Lawlor BA, Coakley D. Measuring cognitive deterioration in Alzheimer' s disease. Br J Psychiatry 1997;170:580.
  80. Polich J, Corey-Bloom J. Alzheimer' s disease and P300: review and evaluation of task and modality. Curr Alzheimer Res 2005;2:515-525. https://doi.org/10.2174/156720505774932214
  81. Polich J, Herbst KL. P300 as a clinical assay: rationale, evaluation, and findings. Int J Psychophysiol 2000;38:3-19. https://doi.org/10.1016/S0167-8760(00)00127-6
  82. Olichney JM, Hillert DG. Clinical applications of cognitive event-related potentials in Alzheimer' s disease. Phys Med Rehabil Clin N Am 2004;15:205-233. https://doi.org/10.1016/S1047-9651(03)00103-7
  83. Bennys K, Portet F, Touchon J, Rondouin G. Diagnostic value of event-related evoked potentials N200 and P300 subcomponents in early diagnosis of Alzheimer' s disease and mild cognitive impairment. J Clin Neurophysiol 2007;24:405-412. https://doi.org/10.1097/WNP.0b013e31815068d5
  84. Li X, Shao X, Wang N, Wang T, Chen G, Zhou H. Correlation of auditory event-related potentials and magnetic resonance spectroscopy measures in mild cognitive impairment. Brain Res 2010;1346: 204-212. https://doi.org/10.1016/j.brainres.2010.04.078
  85. Frodl T, Hampel H, Juckel G, Bürger K, Padberg F, Engel RR, et al. Value of event-related P300 subcomponents in the clinical diagnosis of mild cognitive impairment and Alzheimer' s Disease. Psychophysiology 2002;39:175-181. https://doi.org/10.1111/1469-8986.3920175
  86. van Deursen JA, Vuurman EF, Smits LL, Verhey FR, Riedel WJ. Response speed, contingent negative variation and P300 in Alzheimer' s disease and MCI. Brain Cogn 2009;69:592-599. https://doi.org/10.1016/j.bandc.2008.12.007
  87. Golob EJ, Johnson JK, Starr A. Auditory event-related potentials during target detection are abnormal in mild cognitive impairment. Clin Neurophysiol 2002;113:151-161. https://doi.org/10.1016/S1388-2457(01)00713-1
  88. Yener G, Güntekin B, Başar E. Event-related delta oscillatory responses of Alzheimer patients. Eur J Neurol 2008;15:540-547. https://doi.org/10.1111/j.1468-1331.2008.02100.x
  89. Güntekin B, Saatçi E, Yener G. Decrease of evoked delta, theta and alpha coherences in Alzheimer patients during a visual oddball paradigm. Brain Res 2008;1235:109-116. https://doi.org/10.1016/j.brainres.2008.06.028
  90. Jiang ZY. Abnormal cortical functional connections in Alzheimer' s disease: analysis of inter- and intra-hemispheric EEG coherence. J Zhejiang Univ Sci B 2005;6:259-264.
  91. Adler G, Brassen S, Jajcevic A. EEG coherence in Alzheimer' s dementia. J Neural Transm 2003;110:1051-1058. https://doi.org/10.1007/s00702-003-0024-8
  92. Dunkin JJ, Leuchter AF, Newton TF, Cook IA. Reduced EEG coherence in dementia: state or trait marker? Biol Psychiatry 1994;35: 870-879. https://doi.org/10.1016/0006-3223(94)90023-X
  93. Locatelli T, Cursi M, Liberati D, Franceschi M, Comi G. EEG coherence in Alzheimer' s disease. Electroencephalogr Clin Neurophysiol 1998;106:229-237. https://doi.org/10.1016/S0013-4694(97)00129-6
  94. Hogan MJ, Swanwick GR, Kaiser J, Rowan M, Lawlor B. Memoryrelated EEG power and coherence reductions in mild Alzheimer' s disease. Int J Psychophysiol 2003;49:147-163. https://doi.org/10.1016/S0167-8760(03)00118-1
  95. Besthorn C, Förstl H, Geiger-Kabisch C, Sattel H, Gasser T, Schreiter- Gasser U. EEG coherence in Alzheimer disease. Electroencephalogr Clin Neurophysiol 1994;90:242-245. https://doi.org/10.1016/0013-4694(94)90095-7