Abstract
Alzheimer’s disease (AD) is an important brain disease associated with aging. It involves various functional and structural changes which alter the EEG characteristics. Although numerous studies have found changes in delta, theta, alpha, and beta power, fewer studies have looked at the changes in the resting state EEG gamma activity characteristics in AD. This study aimed to investigate the alterations in the frequency and power values of AD patients’ resting-state EEG gamma oscillations compared with healthy elderly and young subjects. We performed Fast Fourier Transform (FFT) on the resting state EEG data from 179 participants, including 59 early stage AD patients, 60 healthy elderly, and 60 healthy young subjects. We averaged FFT performed epochs to investigate the power values in the gamma frequency range (28–48 Hz). We then sorted the peaks of power values in the gamma frequency range, and the average of the identified highest three values was named as the gamma dominant peak frequency. The gamma dominant peak frequency of AD patients (Meyes−opened = 33.4 Hz, Meyes−closed = 32.7 Hz) was lower than healthy elderly (Meyes−opened = 35.5 Hz, Meyes−closed = 35.0 Hz) and healthy young subjects (Meyes−opened = 37.2 Hz, Meyes−closed = 37.0 Hz). These results could be related to AD progression and therefore critical for the recent findings regarding the 40 Hz gamma entrainment because it seems they entrain the gamma frequency of AD towards that of healthy young.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The data supporting the findings of the article is available in the Resting-state EEG Gamma in Alzheimer at https://osf.io/5sfa4/ (Güntekin et al. 2022).
Abbreviations
- AD:
-
Alzheimer’s disease.
- CDR:
-
clinical dementia rating.
- EC:
-
eyes-closed.
- EO:
-
eyes-opened.
- EOG:
-
electro-oculogram.
- EEG:
-
electroencephalogram.
- FFT:
-
Fast Fourier Transform.
- HE:
-
Healthy elderly.
- HY:
-
Healthy young.
- MCI:
-
Mild Cognitive Impairment.
- MMSE:
-
mini-mental state examination.
- MRI:
-
magnetic resonance imaging.
- PV cells:
-
parvalbumin positive inhibitory interneurons.
- rsEEG:
-
resting-state electroencephalography.
References
Adaikkan C, Middleton SJ, Marco A, Pao PC, Mathys H, Kimu DNW, Gao F, Young JZ, Suk HJ, Boyden ES, McHugh TJ, Tsai LH (2019) Gamma Entrainment Binds Higher-Order Brain Regions and Offers Neuroprotection. Neuron 102(5):929–943e8. https://doi.org/10.1016/J.NEURON.2019.04.011
Adaikkan C, Tsai LH (2020) Gamma Entrainment: Impact on Neurocircuits, Glia, and Therapeutic Opportunities. Trends Neurosci 43(1):24–41. https://doi.org/10.1016/J.TINS.2019.11.001
Alekseichuk I, Turi Z, Amador de Lara G, Antal A, Paulus W (2016) Spatial Working Memory in Humans Depends on Theta and High Gamma Synchronization in the Prefrontal Cortex. Curr Biol 26(12):1513–1521. https://doi.org/10.1016/J.CUB.2016.04.035
American Psychiatric Association (2000) Diagnostic and statistical manual of mental disorders. 4th Edition. Washington, D.C.: American Psychiatric Association
Amieva H, Jacqmin-Gadda H, Orgogozo JM, Le Carret N, Helmer C, Letenneur L, Barberger-Gateau P, Fabrigoule C, Dartigues JF (2005) The 9 year cognitive decline before dementia of the Alzheimer type: a prospective population-based study. Brain 128(5):1093–1101. https://doi.org/10.1093/BRAIN/AWH451
Ao Y, Kou J, Yang C, Wang Y, Huang L, Jing X, Chen J (2022) The temporal dedifferentiation of global brain signal fluctuations during human brain ageing. Sci Rep 12(1):1–8
Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger CE, Fell J (2010) Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc Natl Acad Sci USA 107(7):3228–3233. https://doi.org/10.1073/PNAS.0911531107
Ayton S, Lei P, Bush AI (2013) Metallostasis in Alzheimer’s disease. Free Radic Biol Med 62:76–89. https://doi.org/10.1016/J.FREERADBIOMED.2012.10.558
Babiloni C (2021) Cortical Sources of Resting State EEG Rhythms in Alzheimer’s, Parkinson’s, and Lewy Body Diseases. Int J Psychophysiol 168:S22. https://doi.org/10.1016/J.IJPSYCHO.2021.07.065
Babiloni C, Blinowska K, Bonanni L, Cichocki A, De Haan W, Del Percio C, Dubois B, Escudero J, Fernández A, Frisoni G, Guntekin B, Hajos M, Hampel H, Ifeachor E, Kilborn K, Kumar S, Johnsen K, Johannsson M, Jeong J, Randall F (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
Babiloni C, Lizio R, Marzano N, Capotosto P, Soricelli A, Triggiani AI, Cordone S, Gesualdo L, Del Percio C (2016) Brain neural synchronization and functional coupling in Alzheimer’s disease as revealed by resting state EEG rhythms. Int J Psychophysiol 103:88–102. https://doi.org/10.1016/J.IJPSYCHO.2015.02.008
Bartos M, Vida I, Jonas P (2007) Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Reviews Neurosci 2007 8(1):1. https://doi.org/10.1038/nrn2044
Başar E, Emek-Savaş DD, Güntekin B, Yener GG (2016) Delay of cognitive gamma responses in Alzheimer’s disease. NeuroImage: Clin 11:106–115. https://doi.org/10.1016/J.NICL.2016.01.015
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
Bhattacharya B, Sen, Coyle D, Maguire LP (2011) Alpha and Theta Rhythm Abnormality in Alzheimer’s Disease: A Study Using a Computational Model. Adv Exp Med Biol 718:57–73. https://doi.org/10.1007/978-1-4614-0164-3_6
Bokde ALW, Ewers M, Hampel H (2009) Assessing neuronal networks: Understanding Alzheimer’s disease. Prog Neurobiol 89(2):125–133. https://doi.org/10.1016/J.PNEUROBIO.2009.06.004
Böttger D, Herrmann CS, Von Cramon DY (2002) Amplitude differences of evoked alpha and gamma oscillations in two different age groups. Int J Psychophysiol 45(3):245–251. https://doi.org/10.1016/S0167-8760(02)00031-4
Brady DR, Mufson EJ (1997) Parvalbumin-immunoreactive neurons in the hippocampal formation of Alzheimer’s diseased brain. Neuroscience 80(4):1113–1125. https://doi.org/10.1016/S0306-4522(97)00068-7
Bush AI (2003) The metallobiology of Alzheimer’s disease. Trends Neurosci 26(4):207–214. https://doi.org/10.1016/S0166-2236(03)00067-5
Chan D, Suk HJ, Jackson B, Milman NP, Stark D, Beach SD, Tsai LH (2021) Induction of specific brain oscillations may restore neural circuits and be used for the treatment of Alzheimer’s disease. J Intern Med 290(5):993–1009. https://doi.org/10.1111/JOIM.13329
Coben LA, Danziger WL, Berg L (1983) Frequency analysis of the resting awake EEG in mild senile dementia of Alzheimer type. Electroencephalogr Clin Neurophysiol 55(4):372–380. https://doi.org/10.1016/0013-4694(83)90124-4
Dauwels J, Vialatte F, Cichocki A (2010) Diagnosis of Alzheimers Disease from EEG Signals: Where Are We Standing? Curr Alzheimer Res 7(6):487–505. https://doi.org/10.2174/156720510792231720
Frankó E, Joly O, Initiative, for the A. D. N (2013) Evaluating Alzheimer’s Disease Progression Using Rate of Regional Hippocampal Atrophy. PLoS ONE 8(8):e71354. https://doi.org/10.1371/JOURNAL.PONE.0071354
Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291(5508):1560–1563. https://doi.org/10.1126/SCIENCE.1055465/SUPPL_FILE/1055465S4_THUMB.GIF
Frisoni GB, Fox NC, Jack CR, Scheltens P, Thompson PM (2010) The clinical use of structural MRI in Alzheimer disease. Nat Reviews Neurol 2010 6(2):67–77. https://doi.org/10.1038/nrneurol.2009.215
Garza KM, Zhang L, Borron B, Wood LB, Singer AC (2020) Gamma Visual Stimulation Induces a Neuroimmune Signaling Profile Distinct from Acute Neuroinflammation. https://doi.org/10.1523/JNEUROSCI.1511-19.2019
Gaubert S, Raimondo F, Houot M, Corsi MC, Naccache L, Sitt JD, Hermann B, Oudiette D, Gagliardi G, Habert MO, Dubois B, De Vico Fallani F, Bakardjian H, Epelbaum S (2019) EEG evidence of compensatory mechanisms in preclinical Alzheimer’s disease. Brain 142(7):2096–2112. https://doi.org/10.1093/BRAIN/AWZ150
Gillespie AK, Jones EA, Lin YH, Karlsson MP, Kay K, Yoon SY, Tong LM, Nova P, Carr JS, Frank LM, Huang Y (2016) Apolipoprotein E4 Causes Age-Dependent Disruption of Slow Gamma Oscillations during Hippocampal Sharp-Wave Ripples. Neuron 90(4):740–751. https://doi.org/10.1016/J.NEURON.2016.04.009
Goodman MS, Kumar S, Zomorrodi R, Ghazala Z, Cheam ASM, Barr MS, Daskalakis ZJ, Blumberger DM, Fischer C, Flint A, Mah L, Herrmann N, Bowie CR, Mulsant BH, Rajji TK, Pollock BG, Lourenco L, Butters M, Gallagher D, Voineskos AN (2018) Theta-Gamma coupling and working memory in Alzheimer’s dementia and mild cognitive impairment. Front Aging Neurosci 10(APR):101. https://doi.org/10.3389/FNAGI.2018.00101/BIBTEX
Goutagny R, Krantic S (2013) Hippocampal oscillatory activity in Alzheimer’s disease: toward the identification of early biomarkers? Aging and disease 4(3):134
Güntekin B, Erdal F, Bölükbaş B, Hanoğlu L, Yener G, Duygun R(2022), March 22 Resting-state EEG Gamma in Alzheimer. Retrieved from osf.io/5sfa4
Güntekin B, Saatçi E, Yener G (2008) Decrease of evoked delta, theta and alpha coherences in Alzheimer patients during a visual oddball paradigm. Brain Res 1235:109–116. https://doi.org/10.1016/J.BRAINRES.2008.06.028
He BJ (2014) Scale-free brain activity: past, present, and future. Trends Cogn Sci 18(9):480–487
He Q, Colon-Motas KM, Pybus AF, Piendel L, Seppa JK, Walker ML, Manzanares CM, Qiu D, Miocinovic S, Wood LB, Levey AI, Lah JJ, Singer AC (2021) A feasibility trial of gamma sensory flicker for patients with prodromal Alzheimer’s disease. Alzheimer’s & Dementia: Translational Research & Clinical Interventions 7(1):e12178. https://doi.org/10.1002/TRC2.12178
Herrmann CS, Demiralp T (2005) Human EEG gamma oscillations in neuropsychiatric disorders. Clin Neurophysiol 116(12):2719–2733. https://doi.org/10.1016/J.CLINPH.2005.07.007
Hsiao FJ, Wang YJ, Yan SH, Chen WT, Lin YY (2013) Altered oscillation and synchronization of default-mode network activity in mild Alzheimer’s disease compared to mild cognitive impairment: an electrophysiological study. PLoS ONE 8(7):e68792. https://doi.org/10.1371/JOURNAL.PONE.0068792
Iaccarino HF, Singer AC, Martorell AJ, Rudenko A, Gao F, Gillingham TZ, Mathys H, Seo J, Kritskiy O, Abdurrob F, Adaikkan C, Canter RG, Rueda R, Brown EN, Boyden ES, Tsai LH (2016) Gamma frequency entrainment attenuates amyloid load and modifies microglia. Nat 2016 540(7632):230–235. https://doi.org/10.1038/nature20587
Ismail R, Hansen AK, Parbo P, Brændgaard H, Gottrup H, Brooks DJ, Borghammer P(2018) The Effect of 40-Hz Light Therapy on Amyloid Load in Patients with Prodromal and Clinical Alzheimer’s Disease. International Journal of Alzheimer’s Disease, 2018. https://doi.org/10.1155/2018/6852303
Jelic V, Johansson SE, Almkvist O, Shigeta M, Julin P, Nordberg A, Winblad B, Wahlund LO (2000) Quantitative electroencephalography in mild cognitive impairment: longitudinal changes and possible prediction of Alzheimer’s disease. Neurobiol Aging 21(4):533–540. https://doi.org/10.1016/S0197-4580(00)00153-6
Jensen O, Kaiser J, Lachaux JP (2007) Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci 30(7):317–324. https://doi.org/10.1016/J.TINS.2007.05.001
Jeong J (2004) EEG dynamics in patients with Alzheimer’s disease. Clin Neurophysiol 115(7):1490–1505. https://doi.org/10.1016/J.CLINPH.2004.01.001
Jones M, McDermott B, Oliveira BL, O’Brien A, Coogan D, Lang M, Moriarty N, Dowd E, Quinlan L, McGinley B, Dunne E, Newell D, Porter E, Elahi MA, O’Halloran M, Shahzad A (2019) Gamma Band Light Stimulation in Human Case Studies: Groundwork for Potential Alzheimer’s Disease Treatment. J Alzheimer’s Disease 70(1):171–185. https://doi.org/10.3233/JAD-190299
Keil A, Bernat EM, Cohen MX, Ding M, Fabiani M, Gratton G, Kappenman ES, Maris E, Mathewson KE, Ward RT, Weisz N (2022) Recommendations and publication guidelines for studies using frequency domain and time-frequency domain analyses of neural time series. Psychophysiology 59(5). https://doi.org/10.1111/psyp.14052
Kitchigina VF (2018) Alterations of Coherent Theta and Gamma Network Oscillations as an Early Biomarker of Temporal Lobe Epilepsy and Alzheimer’s Disease. Front Integr Nuerosci 12:36. https://doi.org/10.3389/FNINT.2018.00036/BIBTEX
Khan T (2016) Biomarkers in Alzheimer’s Disease. Academic Press, London
Koenig T, Prichep L, Dierks T, Hubl D, Wahlund LO, John ER, Jelic V (2005) Decreased EEG synchronization in Alzheimer’s disease and mild cognitive impairment. Neurobiol Aging 26(2):165–171. https://doi.org/10.1016/J.NEUROBIOLAGING.2004.03.008
Lahijanian M, Aghajan H, Vahabi Z, Afzal A(2021) Gamma Entrainment Improves Synchronization Deficits in Dementia Patients. BioRxiv, 2021.09.30.462389. https://doi.org/10.1101/2021.09.30.462389
Lee K, Park Y, Suh SW, Kim SS, Kim DW, Lee J, Park J, Yoo S, Kim KW (2021) Optimal flickering light stimulation for entraining gamma waves in the human brain. Sci Rep 2021 11(1):1. https://doi.org/10.1038/s41598-021-95550-1
Lisman JE, Idiart MAP (1995) Storage of 7 ± 2 Short-Term Memories in Oscillatory Subcycles. Science 267(5203):1512–1515. https://doi.org/10.1126/SCIENCE.7878473
Lizio, R., Vecchio, F., Frisoni, G. B., Ferri, R., Rodriguez, G., & Babiloni,C. (2011). Electroencephalographic Rhythms in Alzheimer’s Disease. International Journal of Alzheimer’s Disease, 2011, 1–11. https://doi.org/10.4061/2011/927573
Mably AJ, Colgin LL (2018) Gamma oscillations in cognitive disorders. Curr Opin Neurobiol 52:182–187. https://doi.org/10.1016/J.CONB.2018.07.009
Martinez-Losa M, Tracy TE, Ma K, Verret L, Clemente-Perez A, Khan AS, Cobos I, Ho K, Gan L, Mucke L, Alvarez-Dolado M, Palop JJ (2018) Nav1.1-Overexpressing Interneuron Transplants Restore Brain Rhythms and Cognition in a Mouse Model of Alzheimer’s Disease. Neuron 98(1):75–89e5. https://doi.org/10.1016/J.NEURON.2018.02.029
Martorell AJ, Paulson AL, Suk HJ, Abdurrob F, Drummond GT, Guan W, Young JZ, Kim DNW, Kritskiy O, Barker SJ, Mangena V, Prince SM, Brown EN, Chung K, Boyden ES, Singer AC, Tsai LH (2019) Multi-sensory Gamma Stimulation Ameliorates Alzheimer’s-Associated Pathology and Improves Cognition. Cell 177(2):256–271e22. https://doi.org/10.1016/J.CELL.2019.02.014
McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical diagnosis of Alzheimer’s disease. Neurology 34(7):939–939. https://doi.org/10.1212/WNL.34.7.939
McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR, Kawas CH, Klunk WE, Koroshetz WJ, Manly JJ, Mayeux R, Mohs RC, Morris JC, Rossor MN, Scheltens P, Carrillo MC, Thies B, Weintraub S, Phelps CH (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. Alzheimer’s & Dementia 7(3):263–269. https://doi.org/10.1016/J.JALZ.2011.03.005
Murty DVPS, Manikandan K, Kumar WS, Ramesh RG, Purokayastha S, Javali M, Rao NP, Ray S Gamma oscillations weaken with age in healthy elderly in human EEG. NeuroImage(2020) 215,116826. https://doi.org/10.1016/J.NEUROIMAGE.2020.116826
Osipova D, Pekkonen E, Ahveninen J (2006) Enhanced magnetic auditory steady-state response in early Alzheimer’s disease. Clin Neurophysiol 117(9):1990–1995. https://doi.org/10.1016/J.CLINPH.2006.05.034
Palop JJ, Chin J, Mucke L (2006) A network dysfunction perspective on neurodegenerative diseases. Nat 2006 443(7113):768–773. https://doi.org/10.1038/nature05289
Palop JJ, Chin J, Roberson ED, Wang J, Thwin MT, Bien-Ly N, Yoo J, Ho KO, Yu GQ, Kreitzer A, Finkbeiner S, Noebels JL, Mucke L (2007) Aberrant Excitatory Neuronal Activity and Compensatory Remodeling of Inhibitory Hippocampal Circuits in Mouse Models of Alzheimer’s Disease. Neuron 55(5):697–711. https://doi.org/10.1016/J.NEURON.2007.07.025
Palop JJ, Mucke L (2009) Epilepsy and Cognitive Impairments in Alzheimer Disease. Arch Neurol 66(4):435–440. https://doi.org/10.1001/ARCHNEUROL.2009.15
Palop JJ, Mucke L (2010a) Amyloid-β–induced neuronal dysfunction in Alzheimer’s disease: from synapses toward neural networks. Nat Neurosci 2010 13:7(7):812–818. https://doi.org/10.1038/nn.2583
Palop JJ, Mucke L (2010b) Synaptic depression and aberrant excitatory network activity in Alzheimer’s disease: Two faces of the same coin? NeuroMolecular. Medicine 12(1):48–55. https://doi.org/10.1007/S12017-009-8097-7/FIGURES/4
Palop JJ, Mucke L (2016) Network abnormalities and interneuron dysfunction in Alzheimer disease. Nat Reviews Neurosci 2016 17(12):12. https://doi.org/10.1038/nrn.2016.141
Pelletier A, Periot O, Dilharreguy B, Hiba B, Bordessoules M, Pérès K, Amieva H, Dartigues JF, Allard M, Catheline G (2013) Structural hippocampal network alterations during healthy aging: A multi-modal MRI study. Front Aging Neurosci 5(DEC):84. https://doi.org/10.3389/FNAGI.2013.00084/ABSTRACT
Reid W, Broe G, Creasey H, Grayson D, McCusker E, Bennett H, Longley W, Sulway MR (1996) Age at Onset and Pattern of Neuropsychological Impairment in Mild Early-Stage Alzheimer Disease: A Study of a Community-Based Population. Arch Neurol 53(10):1056–1061. https://doi.org/10.1001/ARCHNEUR.1996.00550100142023
Rey CC, Cattaud V, Rampon C, Verret L (2019) What’s new on Alzheimer’s disease? Insights from AD mouse models. Reference Module in Biomedical Sciences
Sauseng P, Griesmayr B, Freunberger R, Klimesch W (2010) Control mechanisms in working memory: A possible function of EEG theta oscillations. Neurosci Biobehavioral Reviews 34(7):1015–1022. https://doi.org/10.1016/J.NEUBIOREV.2009.12.006
Sauseng P, Peylo C, Biel AL, Friedrich EVC, Romberg-Taylor C (2019) Does cross-frequency phase coupling of oscillatory brain activity contribute to a better understanding of visual working memory? Br J Psychol 110(2):245–255. https://doi.org/10.1111/BJOP.12340
Smit DJA, de Geus EJC, van de Nieuwenhuijzen ME, van Beijsterveldt CEM, van Baal GCM, Mansvelder HD, Boomsma DI, Linkenkaer-Hansen K (2011) Scale-free modulation of resting-state neuronal oscillations reflects prolonged brain maturation in humans. J Neurosci 31(37):13128–13136
Singer W, Gray CM (1995) Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18(1):555–586
Sperling RA, Aisen PS, Beckett LA, Bennett DA, Craft S, Fagan AM, Iwatsubo T, Jack CR, Kaye J, Montine TJ, Park DC, Reiman EM, Rowe CC, Siemers E, Stern Y, Yaffe K, Carrillo MC, Thies B, Morrison-Bogorad M, Phelps CH (2011) Toward defining the preclinical stages of Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s & Dementia 7(3):280–292. https://doi.org/10.1016/J.JALZ.2011.03.003
Stam CJ, Montez T, Jones BF, Rombouts SARB, Van Der Made Y, Pijnenburg YAL, Scheltens P (2005) Disturbed fluctuations of resting state EEG synchronization in Alzheimer’s disease. Clin Neurophysiol 116(3):708–715. https://doi.org/10.1016/J.CLINPH.2004.09.022
Stam CJ, van Walsum AMVC, Pijnenburg YA, Berendse HW, de Munck JC, Scheltens P, van Dijk BW (2002) Generalized synchronization of MEG recordings in Alzheimer’s disease: evidence for involvement of the gamma band. J Clin Neurophysiol 19(6):562–574
Stargardt A, Swaab DF, Bossers K (2015) The storm before the quiet: neuronal hyperactivity and Aβ in the presymptomatic stages of Alzheimer’s disease. Neurobiol Aging 36(1):1–11. https://doi.org/10.1016/J.NEUROBIOLAGING.2014.08.014
Svenningsson AL, Stomrud E, Insel PS, Mattsson N, Palmqvist S, Hansson O (2019) β-amyloid pathology and hippocampal atrophy are independently associated with memory function in cognitively healthy elderly. Sci Rep 2019 9(1):1–9. https://doi.org/10.1038/s41598-019-47638-y
The jamovi project. jamovi (Version 1.6) [Computer Software] (2021) Retrieved from https://www.jamovi.org
van der Hiele K, Vein AA, Reijntjes RHAM, Westendorp RGJ, Bollen ELEM, van Buchem MA, van Dijk JG, Middelkoop HAM (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
Van Deursen JA, Vuurman EFPM, van Kranen-Mastenbroek VHJM, Verhey FRJ, Riedel WJ (2011) 40-Hz steady state response in Alzheimer’s disease and mild cognitive impairment. Neurobiol Aging 32(1):24–30. https://doi.org/10.1016/J.NEUROBIOLAGING.2009.01.002
Van Deursen JA, Vuurman EFPM, Verhey FRJ, Van Kranen-Mastenbroek VHJM, Riedel WJ (2008) Increased EEG gamma band activity in Alzheimer’s disease and mild cognitive impairment. J Neural Transm 115(9):1301–1311. https://doi.org/10.1007/S00702-008-0083-Y/TABLES/3
Verret L, Mann EO, Hang GB, Barth AMI, Cobos I, Ho K, Devidze N, Masliah E, Kreitzer AC, Mody I, Mucke L, Palop JJ (2012) Inhibitory Interneuron Deficit Links Altered Network Activity and Cognitive Dysfunction in Alzheimer Model. Cell 149(3):708–721. https://doi.org/10.1016/J.CELL.2012.02.046
Vossel KA, Beagle AJ, Rabinovici GD, Shu H, Lee SE, Naasan G, Hegde M, Cornes SB, Henry ML, Nelson AB, Seeley WW, Geschwind MD, Gorno-Tempini ML, Shih T, Kirsch HE, Garcia PA, Miller BL, Mucke L (2013) Seizures and Epileptiform Activity in the Early Stages of Alzheimer Disease. JAMA Neurol 70(9):1158–1166. https://doi.org/10.1001/JAMANEUROL.2013.136
Vossel KA, Ranasinghe KG, Beagle AJ, Mizuiri D, Honma SM, Dowling AF, Darwish SM, Van Berlo V, Barnes DE, Mantle M, Karydas AM, Coppola G, Roberson ED, Miller BL, Garcia PA, Kirsch HE, Mucke L, Nagarajan SS (2016) Incidence and impact of subclinical epileptiform activity in Alzheimer’s disease. Ann Neurol 80(6):858–870. https://doi.org/10.1002/ANA.24794
Vreugdenhil M, Toescu EC (2005) Age-dependent reduction of γ oscillations in the mouse hippocampus in vitro. Neuroscience 132(4):1151–1157. https://doi.org/10.1016/J.NEUROSCIENCE.2005.01.025
Wang J, Fang Y, Wang X, Yang H, Yu X, Wang H (2017) Enhanced gamma activity and cross-frequency interaction of resting-state electroencephalographic oscillations in patients with Alzheimer’s disease. Front Aging Neurosci 9(JUL):243. https://doi.org/10.3389/FNAGI.2017.00243/BIBTEX
Weintraub S, Wicklund AH, Salmon DP (2012) The Neuropsychological Profile of Alzheimer Disease. Cold Spring Harbor Perspectives in Medicine 2(4):a006171. https://doi.org/10.1101/CSHPERSPECT.A006171
Wolinski N, Cooper NR, Sauseng P, Romei V (2018) The speed of parietal theta frequency drives visuospatial working memory capacity. PLoS Biol 16(3):e2005348. https://doi.org/10.1371/JOURNAL.PBIO.2005348
Wulff P, Ponomarenko AA, Bartos M, Korotkova TM, Fuchs EC, Bähner F, Both M, Tort ABL, Kopell NJ, Wisden W, Monyer H (2009) Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons. Proc Natl Acad Sci USA 106(9):3561–3566. https://doi.org/10.1073/PNAS.0813176106
Xu Y, Zhao M, Han Y, Zhang H (2020) GABAergic Inhibitory Interneuron Deficits in Alzheimer’s Disease: Implications for Treatment. Front NeuroSci 14:660. https://doi.org/10.3389/FNINS.2020.00660/BIBTEX
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
Acknowledgements
Conceptualization: Bahar Güntekin, Görsev Yener, Lütfü Hanoğlu; Methodology: Bahar Güntekin, Görsev Yener, Lütfü Hanoğlu; Investigation: Bahar Güntekin, Furkan Erdal, Burcu Bölükbaş, Görsev Yener, Lütfü Hanoğlu, Rümeysa Duygun; Supervision: Bahar Güntekin, Görsev Yener, Lütfü Hanoğlu; Writing - original draft preparation: Bahar Güntekin, Furkan Erdal, Burcu Bölükbaş, Görsev Yener, Lütfü Hanoğlu, Rümeysa Duygun; Writing - review & editing: Bahar Güntekin, Furkan Erdal, Görsev Yener, Lütfü Hanoğlu, Rümeysa Duygun; Planning: Bahar Güntekin, Görsev Yener, Lütfü Hanoğlu; Data collection - EEG recording: Bahar Güntekin, Görsev Yener, Lütfü Hanoğlu; Project administration: Bahar Güntekin, Görsev Yener, Lütfü Hanoğlu; Data curation: Burcu Bölükbaş, Rümeysa Duygun; Formal Analysis - Software: Burcu Bölükbaş, Rümeysa Duygun; Visualization: Furkan Erdal, Burcu Bölükbaş.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Furkan Erdal was supported by TÜBİTAK (Scientific and Technological Research Council of Turkey)-2210 National Scholarship Program for MSc Students grant.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval and consent to participate
For all participants included in this retrospective analysis, an informed consent form was obtained at the time of data collection. Ethical approval for this study was obtained from the ethics committee of Istanbul Medipol University (no: E-10840098-772.02-5002).
Conflict of interest
Authors declare having no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Güntekin, B., Erdal, F., Bölükbaş, B. et al. Alterations of resting-state Gamma frequency characteristics in aging and Alzheimer’s disease. Cogn Neurodyn 17, 829–844 (2023). https://doi.org/10.1007/s11571-022-09873-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11571-022-09873-4