Abstract
Objectives Working memory performances are based on brain functional connectivity, so that connectivity may be deranged in individuals with mild cognitive impairment (MCI) and patients with dementia due to Alzheimer’s disease (ADD). Here we tested the hypothesis of abnormal functional connectivity as revealed by the imaginary part of coherency (ICoh) at electrode pairs from event-related electroencephalographic oscillations in ADD and MCI patients. Methods The study included 43 individuals with MCI, 43 with ADD, and 68 demographically matched healthy controls (HC). Delta, theta, alpha, beta, and gamma bands event-related ICoh was measured during an oddball paradigm. Inter-hemispheric, midline, and intra-hemispheric ICoh values were compared in ADD, MCI, and HC groups. Results The main results of the present study can be summarized as follows: (1) A significant increase of midline frontal and temporal theta coherence in the MCI group as compared to the HC group; (2) A significant decrease of theta, delta, and alpha intra-hemispheric coherence in the ADD group as compared to the HC and MCI groups; (3) A significant decrease of theta midline coherence in the ADD group as compared to the HC and MCI groups; (4) Normal inter-hemispheric coherence in the ADD and MCI groups. Conclusions Compared with the MCI and HC, the ADD group showed disrupted event-related intra-hemispheric and midline low-frequency band coherence as an estimate of brain functional dysconnectivity underlying disabilities in daily living. Brain functional connectivity during attention and short memory demands is relatively resilient in elderly subjects even with MCI (with preserved abilities in daily activities), and it shows reduced efficiency at multiple operating oscillatory frequencies only at an early stage of ADD.
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Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
References
Ahnaou A, Moechars D, Raeymaekers L, Biermans R, Manyakov NV, Bottelbergs A et al (2017) Emergence of early alterations in network oscillations and functional connectivity in a tau seeding mouse model of Alzheimer’s disease pathology. Sci Rep 7(1):14189. https://doi.org/10.1038/s41598-017-13839-6
Albert MS, DeKosky ST, Dickson D, Dubois B, Feldman HH, Fox NC et al (2011) The diagnosis of mild cognitive impairment due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 7(3):270–279. https://doi.org/10.1016/j.jalz.2011.03.008
Babiloni C, Binetti G, Cassetta E, Dal Forno G, Del Percio C, Ferreri F et al (2006) Sources of cortical rhythms change as a function of cognitive impairment in pathological aging: a multicenter study. Clin Neurophysiol 117(2):252–268
Babiloni C, Blinowska K, Bonanni L, Cichocki A, De Haan W, Del Percio C et al (2020) What electrophysiology tells us about Alzheimer’s disease: a window into the synchronization and connectivity of brain neurons. Neurobiol Aging 85:58–73. https://doi.org/10.1016/j.neurobiolaging.2019.09.008
Başar E, Güntekin B, Tülay E, Yener GG (2010) Evoked and event related coherence of Alzheimer patients manifest differentiation of sensory-cognitive networks. Brain Res 1357:79–90. https://doi.org/10.1016/j.brainres.2010.08.054
Başar E, Başar-Eroğlu C, Güntekin B, Yener GG (2013a) Brain’s alpha, beta, gamma, delta, and theta oscillations in neuropsychiatric diseases: proposal for biomarker strategies. Suppl Clin Neurophysiol 62:19–54. https://doi.org/10.1016/b978-0-7020-5307-8.00002-8
Başar E, Başar-Eroğlu C, Ozerdem A, Rossini PM, Yener GG (2013b) Application of brain oscillations to neuropsychiatric diseases: a new land? Preface Suppl Clin Neurophysiol 62:v–vi. https://doi.org/10.1016/b978-0-7020-5307-8.09984-1
Başar E, Femir B, Emek-Savaş DD, Güntekin B, Yener GG (2017) Increased long distance event-related gamma band connectivity in Alzheimer’s disease. Neuroimage Clin 14:580–590. https://doi.org/10.1016/j.nicl.2017.02.021
Başar E, Schürmann M, Demiralp T, Başar-Eroglu C, Ademoglu A (2001) Event-related oscillations are 'real brain responses'--wavelet analysis and new strategies. Int J Psychophysiol 39(2-3):91-127. https://doi.org/10.1016/s0167-8760(00)00135-5
Brier MR, Thomas JB, Ances BM (2014) Network dysfunction in Alzheimer’s disease: refining the disconnection hypothesis. Brain Connect 4(5):299–311
Brunia CH (1999) Neural aspects of anticipatory behavior. Acta Psychol (amst) 101(2–3):213–242. https://doi.org/10.1016/s0001-6918(99)00006-2
Caravaglios G, Costanzo E, Palermo F, Muscoso EG (2008) Decreased amplitude of auditory event-related delta responses in Alzheimer’s disease. Int J Psychophysiol 70(1):23–32. https://doi.org/10.1016/j.ijpsycho.2008.04.004
Caravaglios G, Castro G, Muscoso EG, Crivelli D, Balconi M (2018) Beta Responses in healthy elderly and in patients with amnestic mild cognitive impairment during a task of temporal orientation of attention. Clin EEG Neurosci 49(4):258–271. https://doi.org/10.1177/1550059416676144
Cashdollar N, Malecki U, Rugg-Gunn FJ, Duncan JS, Lavie N, Duzel E (2009) Hippocampus-dependent and -independent theta-networks of active maintenance. Proc Natl Acad Sci U S A 106(48):20493–20498. https://doi.org/10.1073/pnas.0904823106
Chan HL, Chu JH, Fung HC, Tsai YT, Meng LF, Huang CC et al (2013) Brain connectivity of patients with Alzheimer’s disease by coherence and cross mutual information of electroencephalograms during photic stimulation. Med Eng Phys 35(2):241–252. https://doi.org/10.1016/j.medengphy.2011.10.005
Cloud BS, Swenson R, Malamut BL, Kaplan E, Sands LP, Gitlin HL et al (1994) The Boston revision of the Wechsler memory scale-mental control subtest. Poster presented at the 22nd annual meeting of the International Neuropsychological Society, Cincinnati, OH
Cohen AD, Price JC, Weissfeld LA, James J, Rosario BL, Bi W et al (2009) Basal cerebral metabolism may modulate the cognitive effects of Abeta in mild cognitive impairment: an example of brain reserve. J Neurosci 29(47):14770–14778. https://doi.org/10.1523/JNEUROSCI.3669-09.2009
Colgin LL (2016) Rhythms of the hippocampal network. Nat Rev Neurosci 17(4):239–249. https://doi.org/10.1038/nrn.2016.21
Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215
Corbetta M, Kincade JM, Ollinger JM, McAvoy MP, Shulman GL (2000) Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nat Neurosci 3(3):292–297. https://doi.org/10.1038/73009
Dauwels J, Vialatte F, Musha T, Cichocki A (2010) A comparative study of synchrony measures for the early diagnosis of Alzheimer’s disease based on EEG. Neuroimage 49(1):668–693
Dickerson BC, Sperling RA (2008) Functional abnormalities of the medial temporal lobe memory system in mild cognitive impairment and Alzheimer’s disease: insights from functional MRI studies. Neuropsychologia 46(6):1624–1635. https://doi.org/10.1016/j.neuropsychologia.2007.11.030
Dickerson BC, Salat DH, Greve DN, Chua EF, Rand-Giovannetti E, Rentz DM et al (2005) Increased hippocampal activation in mild cognitive impairment compared to normal aging and AD. Neurology 65(3):404–411. https://doi.org/10.1212/01.wnl.0000171450.97464.49
Düzel E, Penny WD, Burgess N (2010) Brain oscillations and memory. Curr Opin Neurobiol 20(2):143–149. https://doi.org/10.1016/j.conb.2010.01.004
Dziewczapolski G, Glogowski CM, Masliah E, Heinemann SF (2009) Deletion of the α7 nicotinic acetylcholine receptor gene improves cognitive deficits and synaptic pathology in a mouse model of Alzheimer’s disease. J Neurosci 29(27):8805–8815. https://doi.org/10.1523/JNEUROSCI.6159-08.2009
Ertan T, Eker E, Şar V (1997) Geriatric depression scale: validity and reliability of the Turkish elderly population. Arch Neuropsychiatry 34(1):62–71
Ferretti A, Rogers-Healion K, Fotros A (2022) The therapeutic potential of restoring gamma oscillations in Alzheimer’s disease. Adv Psychiatry Behav Health 2(1):47–55. https://doi.org/10.1016/j.ypsc.2022.05.002
Fodor Z, Sirály E, Horváth A, Salacz P, Hidasi Z, Csibri É et al (2018) Decreased event-related beta synchronization during memory maintenance marks early cognitive decline in mild cognitive impairment. J Alzheimers Dis 63(2):489–502. https://doi.org/10.3233/JAD-171079
Gour N, Ranjeva JP, Ceccaldi M, Confort-Gouny S, Barbeau E, Soulier E et al (2011) Basal functional connectivity within the anterior temporal network is associated with performance on declarative memory tasks. Neuroimage 58(2):687–697. https://doi.org/10.1016/j.neuroimage.2011.05.090
Grady CL, Furey ML, Pietrini P, Horwitz B, Rapoport SI (2001) Altered brain functional connectivity and impaired short-term memory in Alzheimer’s disease. Brain 124(Pt 4):739–756. https://doi.org/10.1093/brain/124.4.739
Grieder M, Wang DJJ, Dierks T, Wahlund LO, Jann K (2018) Default mode network complexity and cognitive decline in mild Alzheimer’s disease. Front Neurosci 12:770. https://doi.org/10.3389/fnins.2018.00770
Güngen C, Ertan T, Eker E, Yaşar R, Engin F (2002) Standardize Mini Mental test'in türk toplumunda hafif demans tanisinda geçerlik ve güvenilirliği [Reliability and validity of the standardized Mini Mental State Examination in the diagnosis of mild dementia in Turkish population]. Turk Psikiyatri Derg 13(4):273–81. Turkish
Güntekin B, Saatçi E, Yener G (2008) Decrease of evoked delta, theta and alpha coherence in Alzheimer patients during a visual oddball paradigm. Brain Res 1235:109–116
Harris AZ, Gordon JA (2015) Long-range neural synchrony in behavior. Annu Rev Neurosci 38:171–194. https://doi.org/10.1146/annurev-neuro-071714-034111
Hillary FG, Grafman JH (2017) Injured brains and adaptive networks: the benefits and costs of hyperconnectivity. Trends Cogn Sci 21(5):385–401. https://doi.org/10.1016/j.tics.2017.03.003
Hogan MJ, Swanwick GR, Kaiser J, Rowan M, Lawlor B (2003) Memory-related EEG power and coherence reductions in mild Alzheimer’s disease. Int J Psychophysiol 49(2):147–163. https://doi.org/10.1016/s0167-8760(03)00118-1
Hoover WB, Vertes RP (2007) Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 212(2):149–179. https://doi.org/10.1007/s00429-007-0150-4
Jack CR Jr, Bennett DA, Blennow K, Carrillo MC, Dunn B, Haeberlein SB et al (2018) NIA-AA research framework: toward a biological definition of Alzheimer’s disease. Alzheimers Dement 14(4):535–562. https://doi.org/10.1016/j.jalz.2018.02.018
Jiang ZY (2005) Abnormal cortical functional connections in Alzheimer’s disease: analysis of inter- and intra-hemispheric EEG coherence. J Zhejiang Univ Sci B 6(4):259–264. https://doi.org/10.1631/jzus.2005.B0259
Jiang ZY, Zheng LL (2006) Inter- and intra-hemispheric EEG coherence in patients with mild cognitive impairment at rest and during working memory task. J Zhejiang Univ Sci B 7(5):357–364. https://doi.org/10.1631/jzus.2006.B0357
Johnson JD (2006) The conversational brain: fronto-hippocampal interaction and disconnection. Med Hypotheses 67(4):759–764. https://doi.org/10.1016/j.mehy.2006.04.031
Jones MW, Wilson MA (2005) Phase precession of medial prefrontal cortical activity relative to the hippocampal theta rhythm. Hippocampus 15(7):867–873. https://doi.org/10.1002/hipo.20119
Kaplan E, Goodglass H, Weintraub S (2001) Boston naming test. Pro-Ed. https://doi.org/10.1016/j.clinph.2005.07.005
Koch K, Myers NE, Göttler J, Pasquini L, Grimmer T, Förster S et al (2015) Disrupted intrinsic networks link amyloid-β pathology and impaired cognition in prodromal Alzheimer’s disease. Cereb Cortex 25(12):4678–4688. https://doi.org/10.1093/cercor/bhu151
Kurt P, Emek-Savaş DD, Batum K, Turp B, Güntekin B, Karşıdağ S et al (2014) Patients with mild cognitive impairment display reduced auditory event-related delta oscillatory responses. Behav Neurol 2014:268967. https://doi.org/10.1155/2014/268967
Liu CJ, Huang CF, Chou CY, Kuo WJ, Lin YT, Hung CM, Chen TC, Ho MC (2012) Age- and disease-related features of task-related brain oscillations by using mutual information. Brain Behav 2(6):754–762. https://doi.org/10.1002/brb3.93
López ME, Garcés P, Cuesta P, Castellanos NP, Aurtenetxe S, Bajo R et al (2014) Synchronization during an internally directed cognitive state in healthy aging and mild cognitive impairment: a MEG study. Age (dordr) 36(3):9643. https://doi.org/10.1007/s11357-014-9643-2
Manos PJ, Wu R (1994) The ten-point clock test: a quick screen and grading method for cognitive impairment in medical and surgical patients. Int J Psychiatry Med 24(3):229–244
Mantini D, Perrucci MG, Del Gratta C, Romani GL, Corbetta M (2007) Electrophysiological signatures of resting state networks in the human brain. Proc Natl Acad Sci U S A 104(32):13170–13175. https://doi.org/10.1073/pnas.0700668104
McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR Jr, Kawas CH et al (2011) The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 7(3):263–269. https://doi.org/10.1016/j.jalz.2011.03.005
Moretti DV, Frisoni GB, Fracassi C, Pievani M, Geroldi C, Binetti G et al (2011) MCI patients’ EEGs show group differences between those who progress and those who do not progress to AD. Neurobiol Aging 32(4):563–571. https://doi.org/10.1016/j.neurobiolaging.2009.04.003
Morison G, Kilborn K, Tieges Z (2011) Decrease in event-related EEG coherence in Alzheimer’s patients during an episodic memory paradigm. Alzheimer’s Dement. https://doi.org/10.1016/j.jalz.2011.05.2124
Morris JC (1993) The clinical dementia rating (CDR): current version and scoring rules. Neurology 43(11):2412–2414. https://doi.org/10.1212/wnl.43.11.2412-a
Nolte G, Bai O, Wheaton L, Mari Z, Vorbach S, Hallett M (2004) Identifying true brain interaction from EEG data using the imaginary part of coherency. Clin Neurophysiol 115(10):2292–2307. https://doi.org/10.1016/j.clinph.2004.04.029
Nunez PL, Srinivasan R (2006) A theoretical basis for standing and traveling brain waves measured with human EEG with implications for an integrated consciousness. Clin Neurophysiol 117(11):2424–2435. https://doi.org/10.1016/j.clinph.2006.06.754
Palop JJ, Mucke L (2016) Network abnormalities and interneuron dysfunction in Alzheimer disease. Nat Rev Neurosci 17(12):777–792. https://doi.org/10.1038/nrn.2016.141
Pearson RCA, Esiri MM, Hiorns RW, Wilcock GK, Powell TPS (1985) Anatomical correlates of the distribution of the pathological changes in the neocortex in Alzheimer’s disease. Proceed Natl Acad Sci USA 82:4531–4534
Pereira JB, Cavallin L, Spulber G, Aguilar C, Mecocci P, Vellas B et al (2014) Influence of age, disease onset and ApoE4 on visual medial temporal lobe atrophy cut-offs. J Intern Med 275(3):317–330. https://doi.org/10.1111/joim.12148
Pfurtscheller G, Da Silva FL (1999) Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 110(11):1842–1857
Picton TW (1992) The P300 wave of the human event-related potential. J Clin Neurophysiol 9(4):456–479
Pievani M, de Haan W, Wu T, Seeley WW, Frisoni GB (2011) Functional network disruption in the degenerative dementias. Lancet Neurol 10(9):829–843. https://doi.org/10.1016/S1474-4422(11)70158-2
Reiman EM, Jagust WJ (2012) Brain imaging in the study of Alzheimer’s disease. Neuroimage 61:505–516
Rhodius-Meester HFM, Benedictus MR, Wattjes MP, Barkhof F, Scheltens P, Muller M et al (2017) MRI visual ratings of brain atrophy and white matter hyperintensities across the spectrum of cognitive decline are differently affected by age and diagnosis. Front Aging Neurosci 9:117. https://doi.org/10.3389/fnagi.2017.00117
Ruiz-Gomez SJ, Gomez C, Poza J, Maturana-Candelas A, Rodriguez-Gonzalez V, Garcia M et al (2019) Analysis of volume conduction effects on different functional connectivity metrics: application to Alzheimer’s disease EEG signals. Annu Int Conf IEEE Eng Med Biol Soc 2019:6434–6437. https://doi.org/10.1109/EMBC.2019.8856548
Sadaghiani S, Scheeringa R, Lehongre K, Morillon B, Giraud AL, Kleinschmidt A (2010) Intrinsic connectivity networks, alpha oscillations, and tonic alertness: a simultaneous electroencephalography/functional magnetic resonance imaging study. J Neurosci 30(30):10243–10250. https://doi.org/10.1523/JNEUROSCI.1004-10.2010
Sanchez Bornot JM, Wong-Lin K, Ahmad AL, Prasad G (2018) Robust EEG/MEG based functional connectivity with the envelope of the imaginary coherence: sensor space analysis. Brain Topogr 31(6):895–916. https://doi.org/10.1007/s10548-018-0640-0
Sarnthein J, Petsche H, Rappelsberger P, Shaw GL, von Stein A (1998) Synchronization between prefrontal and posterior association cortex during human working memory. PNAS 95(12):7092–7096. https://doi.org/10.1073/pnas.95.12.7092
Sauseng P, Klimesch W, Stadler W, Schabus M, Doppelmayr M, Hanslmayr S et al (2005) A shift of visual spatial attention is selectively associated with human EEG alpha activity. Eur J Neurosci 22(11):2917–2926. https://doi.org/10.1111/j.1460-9568.2005.04482.x
Scheltens P, Leys D, Barkhof F, Huglo D, Weinstein HC, Vermersch P et al (1992) Atrophy of medial temporal lobes on MRI in “probable” Alzheimer’s disease and normal ageing: diagnostic value and neuropsychological correlates. J Neurol Neurosurg Psychiatry 55(10):967–972. https://doi.org/10.1136/jnnp.55.10.967
Siapas AG, Lubenov EV, Wilson MA (2005) Prefrontal phase locking to hippocampal theta oscillations. Neuron 46(1):141–151. https://doi.org/10.1016/j.neuron.2005.02.028
Sperling RA, Dickerson BC, Pihlajamaki M, Vannini P, LaViolette PS, Vitolo OV et al (2010) Functional alterations in memory networks in early Alzheimer’s disease. NeuroMol Med 12(1):27–43
Srinivasan R, Winter WR, Ding J, Nunez PL (2007) EEG and MEG coherence: measures of functional connectivity at distinct spatial scales of neocortical dynamics. J Neurosci Methods 166(1):41–52
Stroop JR (1935) Studies of interference in serial verbal reactions. J Exp Psychol 18(6):643–662. https://doi.org/10.1037/h0054651
Tanör ÖÖ (2011) Öktem sözel bellek süreçleri testi. (Öktem-SBST) el kitabı
Thatcher RW (2012) Coherence, phase differences, phase shift, and phase lock in EEG/ERP analyses. Dev Neuropsychol 37(6):476–496. https://doi.org/10.1080/87565641.2011.619241
Torso M, Bozzali M, Zamboni G, Jenkinson M, Chance SA (2021) Alzheimers disease neuroimage initiative detection of Alzheimer’s disease using cortical diffusion tensor imaging. Hum Brain Mapp 42(4):967–977. https://doi.org/10.1002/hbm.25271
Tülay EE, Güntekin B, Yener G, Bayram A, Başar-Eroğlu C, Demiralp T (2020) Evoked and induced EEG oscillations to visual targets reveal a differential pattern of change along the spectrum of cognitive decline in Alzheimer’s Disease. Int J Psychophysiol 155:41–48. https://doi.org/10.1016/j.ijpsycho.2020.06.001
Tumaç A (1997) The effect of age and education on performance in some tests that are sensitive to frontal damage in normal subjects. Department of Psychology, Institute of Social Sciences, Istanbul University. (Unpublished Master Thesis)
van der Hiele K, Vein AA, Reijntjes RH, Westendorp RG, Bollen EL, van Buchem MA et al (2007) EEG correlates in the spectrum of cognitive decline. Clin Neurophysiol 118(9):1931–1939. https://doi.org/10.1016/j.clinph.2007.05.070
Vossel S, Geng JJ, Fink GR (2014a) Dorsal and ventral attention systems distinct neural circuits but collaborative roles. Neuroscientist 20(2):150–159
Vossel S, Geng JJ, Friston KJ (2014b) Attention, predictions and expectations, and their violation: attentional control in the human brain. Front Hum Neurosci 8:490
Waser M, Garn H, Schmidt R, Benke T, Dal-Bianco P, Ransmayr G et al (2016) Quantifying synchrony patterns in the EEG of Alzheimer’s patients with linear and non-linear connectivity markers. J Neural Transm (vienna) 123(3):297–316. https://doi.org/10.1007/s00702-015-1461-x
Weiler M, de Campos BM, Teixeira CVL, Casseb RF, Carletti-Cassani AFMK, Vicentini JE et al (2017) Intranetwork and internetwork connectivity in patients with Alzheimer disease and the association with cerebrospinal fluid biomarker levels. J Psychiatry Neurosci 42(6):366–377. https://doi.org/10.1503/jpn.160190
Weschler D (1981) Weschler adult intelligence scale-revised manual. Psychological Corporation, New York
Yener G, Güntekin B, Başar E (2008) Event-related delta oscillatory responses of Alzheimer patients. Eur J Neurol 15(6):540–547. https://doi.org/10.1111/j.1468-1331.2008.02100.x
Yener GG, Kurt P, Emek-Savaş DD, Güntekin B, Başar E (2013) Reduced visual event-related δ oscillatory responses in amnestic mild cognitive impairment. J Alzheimers Dis 37(4):759–767. https://doi.org/10.3233/JAD-130569
Yener GG, Emek-Savaş DD, Lizio R, Çavuşoğlu B, Carducci F, Ada E et al (2016) Frontal delta event-related oscillations relate to frontal volume in mild cognitive impairment and healthy controls. Int J Psychophysiol 103:110–117. https://doi.org/10.1016/j.ijpsycho.2015.02.005
Yesavage JA, Brink TL, Rose TL, Lum O, Huang V, Adey M et al (1982) Development and validation of a geriatric depression screening scale: a preliminary report. J Psychiatr Res 17(1):37–49. https://doi.org/10.1016/0022-3956(82)90033-4
Zhang Z, Zheng H, Liang K, Wang H, Kong S, Hu J et al (2015) Functional degeneration in dorsal and ventral attention systems in amnestic mild cognitive impairment and Alzheimer’s disease: an fMRI study. Neurosci Lett 585:160–165. https://doi.org/10.1016/j.neulet.2014.11.050
Zheng LL, Jiang ZY, Yu EY (2007) Alpha spectral power and coherence in the patients with mild cognitive impairment during a three-level working memory task. J Zhejiang Univ Sci B 8(8):584–592
Zhou Y, Dougherty JH Jr, Hubner KF, Bai B, Cannon RL, Hutson RK (2008) Abnormal connectivity in the posterior cingulate and hippocampus in early Alzheimer’s disease and mild cognitive impairment. Alzheimers Dement 4(4):265–270. https://doi.org/10.1016/j.jalz.2008.04.006
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This article has been supported financially by a grant of the Scientific and Technological Research Council of Turkey (TÜBiTAK) (Grant number: 112S459), and Dokuz Eylul University, Department of Scientific Research Projects (Grant number: 2018.KB.SAG.084).
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Conceptualization: [Ezgi Fide] and [Görsev Yener]; Methodology: [Ezgi Fide] and [Deniz Yerlikaya]; Formal analysis and investigation: [Ezgi Fide]; Writing—original draft preparation: [Ezgi Fide]; Writing—review and editing: [Ezgi Fide], [Deniz Yerlikaya], [Görsev Yener], [Bahar Güntekin], and [Cludio Babiloni]; Supervision: [Görsev Yener], [Bahar Güntekin], and [Cludio Babiloni].
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Fide, E., Yerlikaya, D., Güntekin, B. et al. Coherence in event-related EEG oscillations in patients with Alzheimer’s disease dementia and amnestic mild cognitive impairment. Cogn Neurodyn 17, 1621–1635 (2023). https://doi.org/10.1007/s11571-022-09920-0
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DOI: https://doi.org/10.1007/s11571-022-09920-0