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当代阿耳茨海默病研究

Editor-in-Chief

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

Research Article

不同阿尔茨海默病小鼠海马CA1区的神经振荡紊乱

卷 20, 期 5, 2023

发表于: 06 September, 2023

页: [350 - 359] 页: 10

弟呕挨: 10.2174/1567205020666230808122643

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摘要

背景:阿尔茨海默病(AD)是一种众所周知的神经退行性疾病,可逐渐引起神经网络功能障碍和进行性记忆缺陷。神经网络活动由影响局部场电位(LFPs)的节律性振荡表示。然而,阿尔茨海默病早期海马神经节律振荡的变化在很大程度上仍未被研究。 目的:本研究研究了3月龄APP/PS1和5x- FAD小鼠的神经节律振荡,以评估AD的早期神经连通性。 方法:在小鼠处于清醒静息期时,植入微电极阵列记录海马CA1区LFP。采用Welch快速傅立叶变换、连续小波变换和相幅耦合分析计算了LFPs中不同频段的功率密度和相幅调制指标。 结果:我们的研究结果显示APP/PS1和5xFAD小鼠在清醒休息阶段的θ、低伽马和高伽马频段功率受损。AD小鼠也表现出δ、α和β频段功率的下降。在5xFAD小鼠中观察到θ -低γ和θ -高γ相幅耦合受损。 结论:本研究揭示了AD早期神经网络活动在振荡功率和交叉频率耦合方面的差异,为开发AD早期诊断的生物标志物提供了新的视角。

关键词: 阿尔茨海默病,海马体,神经节律振荡,局部场电位,θ - γ相位振幅耦合,神经退行性疾病。

[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]

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