Login Register Cart 0
Generic placeholder image

Current Alzheimer Research

Editor-in-Chief

ISSN (Print): 1567-2050
ISSN (Online): 1875-5828

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Neural Oscillation Disorder in the Hippocampal CA1 Region of Different Alzheimer's Disease Mice

Author(s): Weiming Yuan, Weijia Zhi, Lizhen Ma, Xiangjun Hu, Qian Wang, Yong Zou* and Lifeng Wang*

Volume 20, Issue 5, 2023

Published on: 06 September, 2023

Page: [350 - 359] Pages: 10

DOI: 10.2174/1567205020666230808122643

Price: $65

Abstract

Background: Alzheimer's disease (AD) is a well-known neurodegenerative disease that gradually induces neural network dysfunction and progressive memory deficits. Neural network activity is represented by rhythmic oscillations that influence local field potentials (LFPs). However, changes in hippocampal neural rhythmic oscillations in the early stage of AD remain largely unexplored.

Objective: This study investigated neural rhythmic oscillations in 3-month-old APP/PS1 and 5x- FAD mice to assess early neural connectivity in AD.

Methods: LFPs were recorded from the hippocampal CA1 region with implanted microelectrode arrays while the mice were in the awake resting stage. Welch fast Fourier transforms, continuous wavelet transforms, and phase-amplitude coupling analyses were used to compute the power density of different frequency bands and phase-amplitude modulation indices in the LFPs.

Results: Our results showed impaired theta, low gamma, and high gamma frequency band power in APP/PS1 and 5xFAD mice during the awake resting stage. AD mice also showed decreased delta, alpha, and beta frequency band power. Impaired theta-low gamma and theta-high gamma phaseamplitude coupling were observed in 5xFAD mice.

Conclusion: This study revealed neural network activity differences in oscillation power and cross-frequency coupling in the early stage of AD, providing a new perspective for developing biomarkers for early AD diagnosis.

« Previous Next »
[1]
Alzheimer’s Association. 2021 Alzheimer’s disease facts and figures. Alzheimers Dement., 2021, 17(3), 327-406.
[http://dx.doi.org/10.1002/alz.12328] [PMID: 33756057]
[2]
DeTure, M.A.; Dickson, D.W. The neuropathological diagnosis of Alzheimer’s disease. Mol. Neurodegener., 2019, 14(1), 32.
[http://dx.doi.org/10.1186/s13024-019-0333-5] [PMID: 31375134]
[3]
Pereira, J.B.; Janelidze, S.; Ossenkoppele, R.; Kvartsberg, H.; Brinkmalm, A.; Mattsson-Carlgren, N.; Stomrud, E.; Smith, R.; Zetterberg, H.; Blennow, K.; Hansson, O. Untangling the association of amyloid-β and tau with synaptic and axonal loss in Alzheimer’s disease. Brain, 2021, 144(1), 310-324.
[http://dx.doi.org/10.1093/brain/awaa395] [PMID: 33279949]
[4]
Buzsáki, G.; Anastassiou, C.A.; Koch, C. The origin of extracellular fields and currents-EEG, ECoG, LFP and spikes. Nat. Rev. Neurosci., 2012, 13(6), 407-420.
[http://dx.doi.org/10.1038/nrn3241] [PMID: 22595786]
[5]
David, O.; Kilner, J.M.; Friston, K.J. Mechanisms of evoked and induced responses in MEG/EEG. Neuroimage, 2006, 31(4), 1580-1591.
[http://dx.doi.org/10.1016/j.neuroimage.2006.02.034] [PMID: 16632378]
[6]
Wang, H.; Xie, K.; Xie, L.; Li, X.; Li, M.; Lyu, C.; Chen, H.; Chen, Y.; Liu, X.; Tsien, J.; Liu, T. Functional brain connectivity revealed by sparse coding of large-scale local field potential dynamics. Brain Topogr., 2019, 32(2), 255-270.
[http://dx.doi.org/10.1007/s10548-018-0682-3] [PMID: 30341589]
[7]
Pesaran, B.; Musallam, S.; Andersen, R.A. Cognitive neural prosthetics. Curr. Biol., 2006, 16(3), R77-R80.
[http://dx.doi.org/10.1016/j.cub.2006.01.043] [PMID: 16461265]
[8]
Jafari, Z.; Kolb, B.E.; Mohajerani, M.H. Neural oscillations and brain stimulation in Alzheimer’s disease. Prog. Neurobiol., 2020, 194, 101878.
[http://dx.doi.org/10.1016/j.pneurobio.2020.101878] [PMID: 32615147]
[9]
Başar, E.; Başar-Eroğlu, C.; Güntekin, B.; Yener, G.G. Brain’s alpha, beta, gamma, delta, and theta oscillations in neuropsychiatric diseases. Suppl. Clin. Neurophysiol., 2013, 62, 19-54.
[http://dx.doi.org/10.1016/B978-0-7020-5307-8.00002-8] [PMID: 24053030]
[10]
Yener, G.G.; Başar, E. Brain oscillations as biomarkers in neuropsychiatric disorders. Suppl. Clin. Neurophysiol., 2013, 62, 343-363.
[http://dx.doi.org/10.1016/B978-0-7020-5307-8.00016-8] [PMID: 24053048]
[11]
Yener, G.G.; Başar, E. Biomarkers in Alzheimer’s disease with a special emphasis on event-related oscillatory responses. Suppl. Clin. Neurophysiol., 2013, 62, 237-273.
[http://dx.doi.org/10.1016/B978-0-7020-5307-8.00020-X] [PMID: 24053044]
[12]
Salimpour, Y.; Anderson, W.S. Cross-frequency coupling based neuromodulation for treating neurological disorders. Front. Neurosci., 2019, 13, 125.
[http://dx.doi.org/10.3389/fnins.2019.00125] [PMID: 30846925]
[13]
Goutagny, R.; Gu, N.; Cavanagh, C.; Jackson, J.; Chabot, J.G.; Quirion, R.; Krantic, S.; Williams, S. Alterations in hippocampal network oscillations and theta-gamma coupling arise before Aβ overproduction in a mouse model of Alzheimer’s disease. Eur. J. Neurosci., 2013, 37(12), 1896-1902.
[http://dx.doi.org/10.1111/ejn.12233] [PMID: 23773058]
[14]
Bazzigaluppi, P.; Beckett, T.L.; Koletar, M.M.; Lai, A.Y.; Joo, I.L.; Brown, M.E.; Carlen, P.L.; McLaurin, J.; Stefanovic, B. Early-stage attenuation of phase-amplitude coupling in the hippocampus and medial prefrontal cortex in a transgenic rat model of Alzheimer’s disease. J. Neurochem., 2018, 144(5), 669-679.
[http://dx.doi.org/10.1111/jnc.14136] [PMID: 28777881]
[15]
Tort, A.B.L.; Komorowski, R.W.; Manns, J.R.; Kopell, N.J.; Eichenbaum, H. Theta–gamma coupling increases during the learning of item–context associations. Proc. Natl. Acad. Sci. USA, 2009, 106(49), 20942-20947.
[http://dx.doi.org/10.1073/pnas.0911331106] [PMID: 19934062]
[16]
Santner, T.D. D. The Statistical Analysis of Discrete Data; Springer: New York, 1989.
[http://dx.doi.org/10.1007/978-1-4612-1017-7]
[17]
Bhattacharya, S.; Haertel, C.; Maelicke, A.; Montag, D. Galantamine slows down plaque formation and behavioral decline in the 5XFAD mouse model of Alzheimer’s disease. PLoS One, 2014, 9(2), e89454.
[http://dx.doi.org/10.1371/journal.pone.0089454] [PMID: 24586789]
[18]
Oakley, H.; Cole, S.L.; Logan, S.; Maus, E.; Shao, P.; Craft, J.; Guillozet-Bongaarts, A.; Ohno, M.; Disterhoft, J.; Van Eldik, L.; Berry, R.; Vassar, R. Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer’s disease mutations: Potential factors in amyloid plaque formation. J. Neurosci., 2006, 26(40), 10129-10140.
[http://dx.doi.org/10.1523/JNEUROSCI.1202-06.2006] [PMID: 17021169]
[19]
Sun, H.; Liu, M.; Sun, T.; Chen, Y.; Lan, Z.; Lian, B.; Zhao, C.; Liu, Z.; Zhang, J.; Liu, Y. Age-related changes in hippocampal AD pathology, actin remodeling proteins and spatial memory behavior of male APP/PS1 mice. Behav. Brain Res., 2019, 376, 112182.
[http://dx.doi.org/10.1016/j.bbr.2019.112182] [PMID: 31472195]
[20]
Zhang, X.; Zhong, W.; Brankačk, J.; Weyer, S.W.; Müller, U.C.; Tort, A.B.L.; Draguhn, A. Impaired theta-gamma coupling in APP-deficient mice. Sci. Rep., 2016, 6(1), 21948.
[http://dx.doi.org/10.1038/srep21948] [PMID: 26905287]
[21]
Kurudenkandy, F.R.; Zilberter, M.; Biverstål, H.; Presto, J.; Honcharenko, D.; Strömberg, R.; Johansson, J.; Winblad, B.; Fisahn, A. Amyloid-β-induced action potential desynchronization and degradation of hippocampal gamma oscillations is prevented by interference with peptide conformation change and aggregation. J. Neurosci., 2014, 34(34), 11416-11425.
[http://dx.doi.org/10.1523/JNEUROSCI.1195-14.2014] [PMID: 25143621]
[22]
Pastoll, H.; Solanka, L.; van Rossum, M.C.W.; Nolan, M.F. Feedback inhibition enables θ-nested γ oscillations and grid firing fields. Neuron, 2013, 77(1), 141-154.
[http://dx.doi.org/10.1016/j.neuron.2012.11.032] [PMID: 23312522]
[23]
Whittington, M.A.; Traub, R.D. Interneuron Diversity series: Inhibitory interneurons and network oscillations in vitro. Trends Neurosci., 2003, 26(12), 676-682.
[http://dx.doi.org/10.1016/j.tins.2003.09.016] [PMID: 14624852]
[24]
McNaughton, N.; Ruan, M.; Woodnorth, M.A. Restoring theta-like rhythmicity in rats restores initial learning in the Morris water maze. Hippocampus, 2006, 16(12), 1102-1110.
[http://dx.doi.org/10.1002/hipo.20235] [PMID: 17068783]
[25]
Honkanen, R.; Rouhinen, S.; Wang, S.H.; Palva, J.M.; Palva, S. Gamma Oscillations underlie the maintenance of feature-specific information and the contents of visual working memory. Cereb Cortex, 2015, 25(10), 3788-801.
[http://dx.doi.org/10.1093/cercor/bhu263]
[26]
Jensen, O.; Kaiser, J.; Lachaux, J.P. Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci., 2007, 30(7), 317-324.
[http://dx.doi.org/10.1016/j.tins.2007.05.001] [PMID: 17499860]
[27]
Papazoglou, A.; Soos, J.; Lundt, A.; Wormuth, C.; Ginde, V.R.; Müller, R.; Henseler, C.; Broich, K.; Xie, K.; Ehninger, D.; Haenisch, B.; Weiergräber, M. Gender-specific hippocampal dysrhythmia and aberrant hippocampal and cortical excitability in the APPswePS1dE9 model of Alzheimer’s disease. Neural Plast., 2016, 2016, 1-16.
[http://dx.doi.org/10.1155/2016/7167358] [PMID: 27840743]
[28]
Zhen, J; Qian, Y; Weng, X; Su, W; Zhang, J; Cai, L Gamma rhythm low field magnetic stimulation alleviates neuropathologic changes and rescues memory and cognitive impairments in a mouse model of Alzheimer's disease. Alzheimers Dement., 2017, 3(4), 487-497.
[http://dx.doi.org/10.1016/j.trci.2017.07.002]
[29]
Iaccarino, H.F.; Singer, A.C.; Martorell, A.J.; Rudenko, A.; Gao, F.; Gillingham, T.Z.; Mathys, H.; Seo, J.; Kritskiy, O.; Abdurrob, F.; Adaikkan, C.; Canter, R.G.; Rueda, R.; Brown, E.N.; Boyden, E.S.; Tsai, L.H. Gamma frequency entrainment attenuates amyloid load and modifies microglia. Nature, 2016, 540(7632), 230-235.
[http://dx.doi.org/10.1038/nature20587] [PMID: 27929004]
[30]
Martorell, A.J.; Paulson, A.L.; Suk, H.J.; Abdurrob, F.; Drummond, G.T.; Guan, W.; Young, J.Z.; Kim, D.N.W.; Kritskiy, O.; Barker, S.J.; Mangena, V.; Prince, S.M.; Brown, E.N.; Chung, K.; Boyden, E.S.; Singer, A.C.; Tsai, L.H. Multi-sensory Gamma Stimulation Ameliorates Alzheimer’s-Associated Pathology and Improves Cognition. Cell, 2019, 177(2), 256-271.e22.
[http://dx.doi.org/10.1016/j.cell.2019.02.014] [PMID: 30879788]
[31]
Girardeau, G.; Lopes-dos-Santos, V. Brain neural patterns and the memory function of sleep. Science, 2021, 374(6567), 560-564.
[http://dx.doi.org/10.1126/science.abi8370] [PMID: 34709916]
[32]
Herrmann, C.S.; Strüber, D.; Helfrich, R.F.; Engel, A.K. EEG oscillations: From correlation to causality. Int. J. Psychophysiol., 2016, 103(6567), 12-21.
[33]
Iwasaki, S.; Sasaki, T.; Ikegaya, Y. Hippocampal beta oscillations predict mouse object-location associative memory performance. Hippocampus, 2021, 31(5), 503-511.
[http://dx.doi.org/10.1002/hipo.23311] [PMID: 33556218]
[34]
Wianda, E.; Ross, B. The roles of alpha oscillation in working memory retention. Brain Behav., 2019, 9(4), e01263.
[http://dx.doi.org/10.1002/brb3.1263] [PMID: 30887701]
[35]
Abubaker, M.; Al Qasem, W.; Kvašňák, E. Working memory and cross-frequency coupling of Neuronal Oscillations. Front. Psychol., 2021, 12, 756661.
[http://dx.doi.org/10.3389/fpsyg.2021.756661] [PMID: 34744934]
[36]
Goodman, M.S.; Kumar, S.; Zomorrodi, R.; Ghazala, Z.; Cheam, A.S.M.; Barr, M.S.; Daskalakis, Z.J.; Blumberger, D.M.; Fischer, C.; Flint, A.; Mah, L.; Herrmann, N.; Bowie, C.R.; Mulsant, B.H.; Rajji, T.K. Theta-gamma coupling and working memory in Alzheimer’s dementia and mild cognitive impairment. Front. Aging Neurosci., 2018, 10, 101.
[http://dx.doi.org/10.3389/fnagi.2018.00101] [PMID: 29713274]
[37]
Ittner, A.A.; Gladbach, A.; Bertz, J.; Suh, L.S.; Ittner, L.M. p38 MAP kinase-mediated NMDA receptor-dependent suppression of hippocampal hypersynchronicity in a mouse model of Alzheimer’s disease. Acta Neuropathol. Commun., 2014, 2(1), 149.
[http://dx.doi.org/10.1186/s40478-014-0149-z] [PMID: 25331068]
[38]
Taxidis, J.; Coomber, B.; Mason, R.; Owen, M. Assessing cortico-hippocampal functional connectivity under anesthesia and kainic acid using generalized partial directed coherence. Biol. Cybern., 2010, 102(4), 327-340.
[http://dx.doi.org/10.1007/s00422-010-0370-1] [PMID: 20204395]
[39]
Buzsáki, G.; Wang, X.J. Mechanisms of gamma oscillations. Annu. Rev. Neurosci., 2012, 35(1), 203-225.
[http://dx.doi.org/10.1146/annurev-neuro-062111-150444] [PMID: 22443509]
[40]
Cerpa, W.; Dinamarca, M.; Inestrosa, N. Structure-function implications in Alzheimer’s disease: Effect of Abeta oligomers at central synapses. Curr. Alzheimer Res., 2008, 5(3), 233-243.
[http://dx.doi.org/10.2174/156720508784533321] [PMID: 18537540]
[41]
Mucke, L.; Selkoe, D.J. Neurotoxicity of amyloid β-protein: Synaptic and network dysfunction. Cold Spring Harb. Perspect. Med., 2012, 2(7), a006338.
[http://dx.doi.org/10.1101/cshperspect.a006338] [PMID: 22762015]
[42]
Pinheiro, L.; Faustino, C. Therapeutic strategies targeting amyloid-β in Alzheimer’s disease. Curr. Alzheimer Res., 2019, 16(5), 418-452.
[http://dx.doi.org/10.2174/1567205016666190321163438] [PMID: 30907320]
[43]
Pereira, C.; Agostinho, P.; Moreira, P.; Cardoso, S.; Oliveira, C. Alzheimer’s disease-associated neurotoxic mechanisms and neuroprotective strategies. Curr. Drug Targets CNS Neurol. Disord., 2005, 4(4), 383-403.
[http://dx.doi.org/10.2174/1568007054546117] [PMID: 16101556]
[44]
Cantero, J.L.; Moreno-Lopez, B.; Portillo, F.; Rubio, A.; Hita-Yañez, E.; Avila, J. Role of tau protein on neocortical and hippocampal oscillatory patterns. Hippocampus, 2011, 21(8), 827-834.
[PMID: 20607795]
[45]
Mondragón-Rodríguez, S.; Salas-Gallardo, A.; González-Pereyra, P.; Macías, M.; Ordaz, B.; Peña-Ortega, F.; Aguilar-Vázquez, A.; Orta-Salazar, E.; Díaz-Cintra, S.; Perry, G.; Williams, S. Phosphorylation of Tau protein correlates with changes in hippocampal theta oscillations and reduces hippocampal excitability in Alzheimer’s model. J. Biol. Chem., 2018, 293(22), 8462-8472.
[http://dx.doi.org/10.1074/jbc.RA117.001187] [PMID: 29632073]
[46]
Karlsson, A.E.; Lindenberger, U.; Sander, M.C. Out of rhythm: Compromised precision of theta-gamma coupling impairs associative memory in old age. J. Neurosci., 2022, 42(9), 1752-1764.
[http://dx.doi.org/10.1523/JNEUROSCI.1678-21.2021] [PMID: 34996815]
[47]
Counts, S.E.; Ikonomovic, M.D.; Mercado, N.; Vega, I.E.; Mufson, E.J. Biomarkers for the Early Detection and Progression of Alzheimer’s Disease. Neurotherapeutics, 2017, 14(1), 35-53.
[http://dx.doi.org/10.1007/s13311-016-0481-z] [PMID: 27738903]
[48]
Long, J.M.; Holtzman, D.M. Alzheimer disease: An update on pathobiology and treatment strategies. Cell, 2019, 179(2), 312-339.
[http://dx.doi.org/10.1016/j.cell.2019.09.001] [PMID: 31564456]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy