I.P. Pavlov Journal of Higher Nervous ActivityI.P. Pavlov Journal of Higher Nervous ActivityЖурнал высшей нервной деятельности им. И.П. Павлова0044-46773034-5316The Russian Academy of Sciences65207010.31857/S0044467724050026ОБЗОРЫ И ТЕОРЕТИЧЕСКИЕ СТАТЬИReview ArticleThe role of the basal forebrain in the pathogenesis of Alzheimer’s diseaseО механизмах патогенеза болезни Альцгеймера: особая роль переднебазального мозгаKitchiginaV. F.КичигинаВ. Ф.
Russian Federation
vkitchigina@gmail.comPopovaI. Yu.ПоповаИ. Ю.
Russian Federation
vkitchigina@gmail.comShubinaL. V.ШубинаЛ. В.
Russian Federation
vkitchigina@gmail.comInstitute of Theoretical and Experimental Biophysics Russian Academy of SciencesФГБУН Институт теоретической и экспериментальной биофизики РАНEngelhardt Institute of Molecular Biology, Russian Academy of SciencesИнститут молекулярной биологии им. В.А. Энгельгардта РАН2611202474553856402022025Copyright ©; 2024, Russian Academy of SciencesCopyright ©; 2024, Российская академия наук2024Russian Academy of SciencesРоссийская академия наукhttps://innoscience.ru/0044-4677/article/view/652070

Alzheimer’s disease (AD) is a progressive neurodegenerative disease characterized by impaired cognitive functions, from minor deviations to dementia, as well as altered behavior. Typical features of this disease include the presence of senile plaques, neurofibrillary tangles, synaptic damage, and neuronal loss. Many factors contribute to cognitive decline in patients with AD. According to the cholinergic hypothesis, which prevailed at the end of the last century and remains relevant today, a key event in the pathogenesis of AD is the loss of cholinergic neurons in the basal forebrain (BFB), found in this region in AD patients. However, the death of neurons deprives the brain of a range of other neurochemical agents. In addition, the occurrence of AD may also be caused also caused by other morphofunctional abnormalities in this area of the brain. In modern literature there is no summary information about the role of BFB in the pathogenesis of AD. The functions of the BFB and the mechanisms of regulation of the neural network of this part of the brain in normal conditions and in neuropathologies remain unclear. This review comprehensively examines the involvement of the BFB and its connections with other brain regions in the development of AD. The article includes data from clinical observations and experiments conducted both on healthy animals and on those with models of this disease. The analysis of the available literature data will improve the understanding of the functioning of the BFB normally and its disturbances during the development of AD, which can advance the development of therapeutic approaches for the treatment of this disease.

Болезнь Альцгеймера (БА) – прогрессирующее нейродегенеративное заболевание, характеризующееся измененным поведением и нарушением когнитивных функций, от незначительных их отклонений до деменции. Типичным для этой болезни является наличие в мозге сенильных бляшек, нейрофибриллярных клубков, повреждение синапсов и потеря нейронов. Многие факторы способствуют ослаблению когнитивных способностей у пациентов с БА. По холинергической гипотезе, преобладающей в конце прошлого века и сохраняющей свою актуальность в настоящее время, ключевым событием в патогенезе БА является потеря холинергических нейронов в переднебазальном мозге (ПБМ), обнаруженная в этой области у пациентов с БА. Однако гибель нейронов ПБМ лишает мозг целого набора других нейрохимических агентов. Кроме того, возникновение БА, очевидно, обусловлено также иными морфофункциональными отклонениями в этой области мозга. В современной литературе отсутствуют суммарные сведения о роли ПБМ в патогенезе БА. Функции ПБМ и механизмы регуляции нейронной сети этого отдела мозга в норме и при нейропатологиях остаются неясными. В настоящем обзоре всесторонне рассматривается участие ПБМ и его связей с другими областями мозга в развитии БА. В статью включены данные клинических наблюдений и экспериментов, проведенных как на здоровых животных, так и на животных с моделями этого заболевания. Проведенный анализ имеющихся литературных данных улучшит понимание функционирования ПБМ в норме и его нарушений при развитии БА, что может продвинуть разработку терапевтических подходов для лечения этой болезни.

basal forebrainacetylcholinemedial septal areabasal nucleus of Meynerthippocampussepto-hippocampal system, neocortexgamma-aminobutyric acidtheta rhythmtheta-gamma cross-frequency interactionsпереднебазальный мозгацетилхолинмедиальная септальная областьбазальное ядро Мейнертагиппокампсепто-гиппокампальная системанеокортексгамма-аминомасляная кислотатета-ритмтета-гамма кросс-частотные взаимодействияПравительство РФGovernment of the Russian Federation075-00224-24-03Российский научный фондRussian Science Foundation19-74-30007Бражник Е.С. Сравнительные характеристики залповых нейронов септум при устранении восходящих влияний ретикулярной формации у кроликов (хирургическими и фармакологическими воздействиями). Журн. высш. нервн. деят. им. И.П. Павлова. 1986. 36: 721–729.Бражник Е.С., Виноградова О.С. Влияние полной подрезки септум на активность ее нейронов. Журн. высш. нерв. деят. И.П. Павлова. 1980. 30: 141–152.Кичигина В.Ф. Нарушения тета- и гамма-осцилляций в мозге с патологиями, характерными для болезни Альцгеймера и височной эпилепсии. Журн. высш. нервн. деят. И.П. Павлова. 2019. 69 (4): 395–412.Abe H., Iwasaki T. NMDA and muscarinic blockade in the perirhinal cortex impairs object discrimination in rats. Neuroreport 2001. 12: 3375–3379.Abramov U., Kurrikoff K., Matsui T., Vasar E. Environmental enrichment reduces mechanical hypersensitivity in neuropathic mice, but fails to abolish the phenotype of CCK2 receptor deficient mice. Neurosci. Lett. 2009. 467(3): 230–233.Acsády L., Arabadzisz D., Katona I., Freund T.F. Topographic distribution of dorsal and median raphe neurons with hippocampal, septal and dual projection. Acta Biol. Hung. 1996. 47 (1–4): 9–19.Adler G., Brassen S., Jajcevic A. EEG coherence in Alzheimer’s dementia. J. Neural Transm. 2003. 110: 1051–1058.Ahmadian S.S., Rezvanian A., Peterson M., Weintraub S., Bigio E.H., Mesulam M.M., Geula C. Loss of calbindin-D28K is associated with the full range of tangle pathology within basal forebrain cholinergic neurons in Alzheimer’s disease. Neurobiol.Aging 2015. 36: 3163–3170.Ahnaou A., Drinkenburg W.H.I.M. Sleep, neuronal hyperexcitability, inflammation and neurodegeneration: Does early chronic short sleep trigger and is it the key to overcoming Alzheimer’s disease? Neurosci. Biobehav. Rev. 2021. 129: 157–179.Allaway K.C., Machold R. Developmental specification of forebrain cholinergic neurons. Dev. Biol. 2017. 421 (1): 1–7.Ally B.A. Using pictures and words to understand recognition memory deterioration in amnestic mild cognitive impairment and Alzheimer’s disease: a review. Curr. Neurol. Neurosci. Rep. 2012 Dec; 12(6): 687–94.Alves F., Kalinowski P., Ayton S. Accelerated Brain Volume Loss Caused by Anti-β-Amyloid Drugs: A Systematic Review and Meta-analysis. Neurology 2023. 100(20): e2114–e2124Amaral D.G., Scharfman H.E., Lavenex P. The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog. Brain Res. 2007. 163: 3–22.Amatniek J.C., Hauser W.A., DelCastillo-Castaneda C., Jacobs D.M., Marder K., Bell K., Albert M., Brandt J., Stern Y. Incidence and predictors of seizures in patients with Alzheimer’s disease. Epilepsia 2006. 47 (5): 867–872.Ananth M.R., Rajebhosale P., Kim R., Talmage D.A., Role L.W. Basal forebrain cholinergic signalling: development, connectivity and roles in cognition. Nat. Rev. Neurosci. 2023. 24(4): 233–251.Andy O. J., Stephan H. (1968) The septum in the human brain. J. Comp. Neurol. 133, 383–410.Arendt T., Bigl V., Tennstedt A., Arendt A. Neuronal loss in different parts of the nucleus basalis is related to neuritic plaque formation in cortical target areas in Alzheimer’s disease. Neuroscience 1985. 14(1): 1–14.Ashton N.J., Brum W.S., Di Molfetta G., Benedet A.L., Arslan B., Jonaitis E., Langhough R.E., Cody K., Wilson R., Carlsson C.M., Vanmechelen E., Montoliu-Gaya L., Lantero-Rodriguez J., Rahmouni N., Tissot C., Stevenson J., Servaes S., Therriault J., Pascoal T., Lleó A., Alcolea D., Fortea .J, Rosa-Neto P., Johnson S., Jeromin A., Blennow K., Zetterberg H. Diagnostic Accuracy of a Plasma Phosphorylated Tau 217 Immunoassay for Alzheimer Disease Pathology. JAMA Neurol. 2024. 81(3): 255–263.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. What electrophysiology tells us about Alzheimer’s disease: a window into the synchronization and connectivity of brain neurons. Neurobiol. Aging 2020. 85: 58–73.Baglietto-Vargas D., Moreno-Gonzalez I., Sanchez-Varo R., Jimenez S., Trujillo-Estrada L., Sanchez-Mejias E., Torres M., Romero-Acebal M., Ruano D., Vizuete M., Vitorica J., Gutierrez A. Calretinin interneurons are early targets of extracellular amyloid-beta pathology in PS1/AbetaPP Alzheimer mice hippocampus. J. Alzheimers Dis. 2010; 21(1): 119–32.Ballard C., Gauthier S., Corbett A., Brayne C., Aarsland D., Jones E. Alzheimer’s disease. Lancet 2011. 377 (9770): 1019–31.Bezzina C., Verret L., Juan C., Remaud J., Halley H., Rampon C, Dahan L. Early onset of hypersynchronous network activity and expression of a marker of chronic seizures in the Tg2576 mouse model of Alzheimer’s disease. PLoS One 2015. 10 (3): e0119910.Balázs N., Bereczki D, Kovács T. Cholinesterase inhibitors and memantine for the treatment of Alzheimer and non-Alzheimer dementias. Ideggyogy Sz. 2021. 74(11–12): 379–387.Bartus R.T., Dean R.L., 3rd, Beer B., Lippa A.S. The cholinergic hypothesis of geriatric memory dysfunction. Science 1982. 217 (4558): 408–14.Bateman R.J., Xiong C., Benzinger T.L., Fagan A.M., Goate A., Fox N.C., Marcus D.S.,Cairns N.J., Xie X., Blazey T.M., et al. Clinical and biomarker changes in dominantly inherited Аlzheimer’s disease. N. Engl. J. Med. 2012, 367, 795–804.Benchenane K., Peyrache A., Khamassi M., Tierney P.L., Gioanni Y., Battaglia F.P., Wiener S.I. Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron 2010, 66, 921–936.Bhattacharya B., Coyle D, Maguire LP. Alpha and Theta Rhythm Abnormality in Alzheimer’s Disease: A Study Using a Computational Model. Adv. Exp. Med. Biol. 2011. 718: 57–73.Bigl V., Woolf N.J., Butcher L.L. Cholinergic projectionsfrom the basal forebrain to frontal, parietal, temporal, occipital, and cingulate cortices: a combined fluorescent tracer and acetylcholinesterase analysis. Brain Res. Bull. 1982. 8(6): 727–749.Birks J.S., Harvey R.J. Donepezil for dementia due to Alzheimer’s disease. Cochrane Database Syst. Rev. 2018. 6 (6): CD001190.Boada-Rovira M., Brodaty H., Cras P., Baloyannis S., Emre M., Zhang R., Bahra R. Efficacy and safety of donepezil in patients with Alzheimer’s disease: results of a global, multinational, clinical experience study. Drugs Aging. 2004. 21 (1): 43–53.Bortolami M., Pandolfi F., De Vita D., Carafa C., Messore A., Di Santo R., Feroci M., Costi R., Chiarotto I., Bagetta D. New deferiprone derivatives as multi-functional cholinesterase inhibitors: design, synthesis and in vitro evaluation. Eur. J. Med. Chem. 2020. 198: 112350.Bowen D.M., Smith C.B., White P., Davison A.N. Neurotransmitter-related enzymes and indices of hypoxia in senile dementia and other abiotrophies. Brain 1976. 99: 459–496.Bowen D.M., Allen S.J., Benton J.S., Goodhardt M.J., Haan E.A., Palmer A.M., Sims N.R., Smith C.C., Spillane J.A., Esiri M.M., Neary D., Snowdon J.S., Wilcock G.K., Davison A.N. Biochemical assessment of serotonergic and cholinergic dysfunction and cerebral atrophy in Alzheimer’s disease. J. Neurochem. 1983. 41: 266–272.Braak H., Braak E. Temporal sequence of Alzheimer’s disease-related pathology. in: Cerebral Cortex, Vol. 14. Neurodegenerative and Age-related Changes in Structure and Function of Cerebral Cortex. Eds. Peters A., Morrison J.H. New York: Kluwer Academic/Plenum Publishers, 1999. 475–512.Brazhnik E.S., Fox S.E. Action potentials and relations to the theta rhythm of medial septal neurons in vivo. Exp. Brain Res. 1999. 127 (3): 244–58.Brazhnik E.S., Fox S.E. Intracellular recordings from medial septal neurons during hippocampal theta rhythm. Exp. Brain Res. 1997. 114 (3): 442–53.Butterfield D.A., Halliwell B. Oxidative stress, dysfunctional glucose metabolism and Alzheimer disease. Nat. Rev. Neurosci. 2019. 20: 148e160.Brown M. W., Aggleton J. P. Recognition memory: What are the roles of the perirhinal cortex and hippocampus? Nat. Rev. Neurosci. 2001. 2: 51–61.Brown M.W., Barker G.R.I., Aggleton J.P., Warburton E.C. What pharmacological interventions indicate concerning the role of the perirhinal cortex in recognition memory. Neuropsychologia 2012. 50 (13): 3122–3140.Brown J.T., Chin J., Leiser S.C., Pangalos M.N., Randall A.D. Altered intrinsic neuronal excitability and reduced Na+currents in a mouse model of Alzheimer’s disease. Neurobiol. Aging 2011. 32 (11): 2109.e1–14.Busche M.A., Konnerth A. Impairments of neural circuit function in alzheimer’s disease. Philos. Trans. R. Soc. B. Biol. Sci. 2016. 371: 20150429.Buzsáki G. Theta oscillations in the hippocampus. Neuron 2002. 33: 325–340.Buzsáki G. Rhythms of the Brain. Oxford University Press, New York, NY. (2006).Buzsáki G., Wang X. J. Mechanisms of γ oscillations. Annu. Rev. Neurosci. 2010. 35: 203–225.Calvo-Rodriguez M., Bacskai B.J. Mitochondria and Calcium in Alzheimer’s Disease: From Cell Signaling to Neuronal Cell Death. Trends Neurosci. 2021. 44(2): 136–151.Canolty R. T., Knight R. T. The functional role of cross-frequency coupling. Trends Cogn. Sci. 2010. 14, 506–515.Canter R.G., Penney J., Tsai L.H. The road to restoring neural circuits for the treatment of alzheimer’s disease. Nature 2016. 539: 187–196.Camandola S., Mattson M.P. Aberrant subcellular neuronal calcium regulation in aging and Alzheimer’s disease. Biochim. Biophys. Acta. 2011. 1813: 965–973.Canter R.G., Penney J., Tsai L.H. The road to restoring neural circuits for the treatment of alzheimer’s disease. Nature 2016, 539, 187–196.Cantero J.L., Atienza M., Lage C., Zaborszky L., Vilaplana E., Lopez-Garcia S., Pozueta A., Rodriguez-Rodriguez E., Blesa R., Alcolea D., Lleo A., Sanchez-Juan P., Fortea J. Atrophy of basal forebrain initiates with tau pathology in individuals at risk for Alzheimer’s disease. Cereb Cortex 2020. 30: 2083–2098.Caravaglios G., Castro G., Costanzo E., Di Maria G., Mancuso D., Muscoso E. G. Theta power responses in mild Alzheimer’s disease during an auditory oddball paradigm: lack of theta enhancement during stimulus processing. J. Neural Transm. 2010. 117: 1195–1208.Case D.T., Burton S.D., Gedeon J.Y., Williams S.G., Urban N.N., Seal R.P. Layer- and cell type-selective co-transmission by a basal forebrain cholinergic projection to the olfactory bulb. Nat. Commun. 2017. 8: 652.Cavedo E., Grothe M. J., Colliot O., Lista S., Chupin M., Dormont D., Houot M., Lehéricy S., Teipel S., Dubois B., Hampel H. Reduced basal forebrain atrophy progression in a randomized Donepezil trial in prodromal Alzheimer’s disease. Sci. Rep. 2017. 7: 11706.Chen D., Zhang Y., Qiao R., Kong X., Zhong H., Wang X., Zhu J., Li B. Integrated bioinformatics-based identification of diagnostic markers in Alzheimer disease. Front. Aging Neurosci. 2022. 14: 988143.Chang Z., Luo Y., Zhang Y., Wei G. Interactions of A_25-35-barrel-like oligomers with anionic lipid bilayer and resulting membrane leakage: an all-atom molecular dynamics study. J. Phys. Chem. B. 2011. 115: 1165–1174.Colgin L.L. Theta-g coupling in the entorhinal-hippocampal system. Curr. Opin. Neurobiol. 2015. 31: 45–50.Colgin L.L. Rhythms of the hippocampal network. Nat. Rev. Neurosci. 2016. 17: 239–249.Colgin L.L., Denninger T., Fyhn M., Hafting T., Bonnevie T., Jensen O., Moser M.B., Moser E.I. Frequency of g oscillations routes flow of information in the hippocampus. Nature 2009. 462 (7271): 353–357.Colom L.V. Septal networks: relevance to theta rhythm, epilepsy and Alzheimer’s disease. J. Neurochem. 2006. 96 (3): 609–23.Colom L.V., Castaneda M.T., Reyna T., Hernandez S., Garrido-Sanabria E. Characterization of medial septal glutamatergic neurons and their projection to the hippocampus. Synapse 2005. 58: 151–64.Coyle J.T., Price D.L., DeLong M.R. Alzheimer’s disease: A disorder of cortical cholinergic innervation. Science 1983. 219: 1184–1190.Crimins J.L., Pooler A., Polydoro M., Luebke J.I., Spires-Jones T.L. The intersection of amyloid b and tau in glutamatergic synaptic dysfunction and collapse in Alzheimer’s disease. Ageing Res. Rev. 2013. 12: 757–763.Cutuli D., De Bartolo P., Caporali P., Tartaglione A. M., Oddi D., D’Amato F. R., Nobili A., D’Amelio M., Petrosini L. Neuroprotective effects of donepezil against cholinergic depletion. Alzheimers Res. Ther. 2013. 5: 50.Czigler B., Csikos D., Hidasi Z., Anna Gaál Z., Csibri E., Kiss E., Salacz P., Molnár M. Quantitative EEG in early Alzheimer’s disease patients–power spectrum and complexity features. Int. J. Psychophysiol. 2008. 68 (1): 75–80.Dannenberg H., Pabst M., Braganza O., Schoch S., Niediek J., Bayraktar M., Mormann F. Beck H. Synergy of direct and indirect cholinergic septo-hippocampal pathways coordinates firing in hippocampal networks. J. Neurosci. 2015, 35, 8394–8410.Davies P., Maloney A.J.F. Selective loss of central cholinergic neurons in Alzheimer’s disease. Lancet 1976. 2: 1403.Davis K.L., Mohs R.C., Marin D., Purohit D.P., Perl D.P., Lantz M., Austin G., Haroutunian V. Cholinergic markers in elderly patients with early signs of Alzheimer disease. JAMA 1999. 281 (15): 1401–1406.DeKosky S.T., Sche S.W. Synapse loss in frontal cortex biopsies in alzheimer’s disease: Correlation with cognitive severity. Ann. Neurol. 1990. 27: 457–464.DeKosky S.T., Ikonomovic M.D., Styren S.D., Beckett L., Wisniewski S., Bennett D.A., Cochran E.J., Kordower J.H., Mufson E.J. Upregulation of choline acetyltransferase activity in hippocampus and frontal cortex of elderly subjects with mild cognitive impairment Ann. Neurol. 2002. 51 (2): 145–55.Desikan R.S., Cabral H.J., Fischl B., Guttmann C.R.G., Blacker D., Hyman B.T., Albert M.S., Killiany R.J. Temporoparietal MR Imaging Measures of Atrophy in Subjects with Mild Cognitive Impairment That Predict Subsequent Diagnosis of Alzheimer Disease. AJNR Am. J. Neuroradiol. 2009. 30 (3): 532–538.Devi L., Ohno M. Phospho-eif2alpha level is important for determining abilities of bace1 reduction to rescue cholinergic neurodegeneration and memory defects in 5xfad mice. PLoS ONE 2010. 5: e12974.Divac I. Magnocellular nuclei of the basal forebrain project to neocortex, brain stem, and olfactory bulb. Review of some functional correlates. Brain Res. 1975. 93 (3): 385–98.Dmitrieva E., Malkov A. Optogenetic stimulation of medial septal glutamatergic neurons modulates theta-gamma coupling in the hippocampus. bioRxiv preprint doi: https: //doi.org/10.1101/2022.03.15.484394.Dranovsky A., Kirshenbaum G., Chang C.Y., Bompolaki M., Bradford V., Bell J., Kosmidis S., Shansky R., Orlandi J., Savage L., Leonardo E., Harris A. Adult-born neurons maintain hippocampal cholinergic inputs and support working memory during aging. Res Sq. 2023. Jan 31:rs.3.rs-1851645.doi: 10.21203/rs.3.rs-1851645/v1. Preprint.Dragoi G., Carpi D., Recce M., Csicsvari J., Buzsaki G. Interactions between hippocampus and medial septum during sharp waves and theta oscillation in the behaving rat. J. Neurosci. 1999. 19: 6191–6199.Drew M.R., Denny C.A., Hen R. Arrest of adult hippocampal neurogenesis in mice impairs single- but not multiple-trial contextual fear conditioning. Behav. Neurosci. 2010. 124: 446–54.Dunnett S.B., Wareham A.T., Torres E.M. Cholinergic blockade in prefrontal cortex and hippocampus disrupts shortterm memory in rats. Neuroreport 1990. 1: 61–64.Dubois B., Feldman H. H., Jacova C., DeKosky S. T., Barberger-Gateau P., Cummings J., Delacourte A., Galasko D., Gauthier S., Jicha G., Meguro K., O’brien J., Pasquier F., Robert P., Rossor M., Salloway S., Stern Y., Visser P.J., Scheltens P. Research criteria for the diagnosis of Alzheimer’s disease: revising the NINCDS-ADRDA criteria. Lancet Neurol. 2007. 6 (8): 734–746.Dutar P., Bassant M.H., Senut M.C., Lamour Y. The septohippocampal pathway: structure and function of a central cholinergic system. Physiol. Rev. 1995. 75: 393–427.Eriksdotter M., Mitra S. Gene and cell therapy for the nucleus basalis of Meynert with NGF in Alzheimer’s disease. Handb. Clin. Neurol. 2021. 179: 219–229.Ezrin-Waters C., Resch L. The Nucleus Basalis of Meynert. Can. J. Neurol. Sci. 1986. 13: 8–1.Etter G., van der Veldt S., Manseau F., Zarrinkoub I., Trillaud-Doppia E., Williams S. Optogenetic gamma stimulation rescues memory impairments in an Alzheimer’s disease mouse model. Nat. Commun. 2019. 10 (1): 5322.Falangola M.F., Nie X., Ward R., Dhiman S., Voltin J., Nietert P.J., Jensen J.H. Diffusion MRI detects basal forebrain cholinergic abnormalities in the 3xTg-AD mouse model of Alzheimer’s disease. Magn. Reson. Imaging 2021. 83: 1–13.Faucher P., Mons N., Micheau J., Louis C., Beracochea D.J. Hippocampal Injections of Oligomeric Amyloid β-peptide (1-42) Induce Selective Working Memory Deficits and Long-lasting Alterations of ERK Signaling Pathway. Front. Aging Neurosci. 2016. 7: 245.Feng Y., Wang X. Antioxidant therapies for Alzheimer’s disease. Oxid. Med. Cell. Longevity. 2012. 2012: 472932.Ferreira S.T., Klein W.L. The Aβ oligomer hypothesis for synapse failure and memory loss in Alzheimer’s disease. Neurobiol. Learn. Mem. 2011. 96(4): 529–543.Ferrer I. Defining Alzheimer as a common age-related neurodegenerative process not inevitably leading to dementia. Prog. Neurobiol. 2012. 97 (1): 38–51.Freund T.F., Antal M. Gaba-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 1988. 336: 170–173.Freund T.F., Buzsaki G. Interneurons of the hippocampus. Hippocampus 1996. 4: 347–470.Fries P. Neuronal g-band synchronization as a fundamental process in cortical computation. Annu. Rev. Neurosci. 2009. 32: 209–224.Frisoni G.B., Altomare D., Thal D.R., Ribaldi F., van der Kant R., Ossenkoppele R., Blennow K., Cummings J., van Duijn C., Nilsson P.M., Dietrich P.-Y., Scheltens P., Dubois B. The probabilistic model of Alzheimer disease: the amyloid hypothesis revised. Nat. Rev. Neurosci. 2022. 23: 53–66.Frotscher M., Leranth C. Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J. Comp. Neurol. 1985. 239: 237–246.Fuhrmann F., Justus D., Sosulina L., Kaneko H., Beutel T., Friedrichs D., Schoch S., Schwarz M.K., Fuhrmann M., Remy S. Locomotion, Theta Oscillations, and the Speed-Correlated Firing of Hippocampal Neurons Are Controlled by a Medial Septal Glutamatergic Circuit. Neuron 2015. 86(5): 1253–64.Gaykema R.P., Luiten P.G., Nyakas C., Traber J. Cortical projection patterns of the medial septum-diagonal band complex. J. Comp. Neurol. 1990. 293: 103–124.George A.A., Vieira J.M., Xavier-Jackson C., Gee M.T., Cirrito J.R., Bimonte-Nelson H.A., Picciotto M.R., Lukas R.J., Whiteaker P. Implications of Oligomeric Amyloid-Beta (oAb42) Signaling through a7b2-Nicotinic Acetylcholine Receptors (nAChRs) on Basal Forebrain Cholinergic Neuronal Intrinsic Excitability and Cognitive Decline. J. Neurosci. 2021. 41(3): 555–575.Geula C., Dunlop S.R., Ayala I., Kawles A.S., Flanagan M.E., Gefen T., Mesulam M.M. Basal forebrain cholinergic system in the dementias: Vulnerability, resilience, and resistance. J. Neurochem. 2021. 158 (6): 1394–1411.Giacobini E., Cuello A.C., Fisher A. Reimagining cholinergic therapy for Alzheimer’s disease. Brain 2022. 145 (7): 2250–2275.Goldstein F.C., Loring D.W., Thomas T., Saleh S., Hajjar I. Recognition memory performance as a cognitive marker of prodromal Alzheimer’sdisease. J. Alzheimers Dis. 2019. 72: 507–514.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. 16:1 0:101.Gorry J.D. Studies on the comparative anatomy of the ganglion basale of Meynert. Acta Anat. (Basel). 1963. 55: 51–104.Goutagny R., Krantic S. Hippocampal oscillatory activity in Alzheimer’s disease: toward the identification of early biomarkers? Aging Dis. 2013. 4: 134–140.Green J.D., Arduini A.A. Hippocampal electrical activity in arousal. J. Neurophysiol. 1954. 17: 533–557.Green K.N., LaFerla F.M. Linking calcium to Abeta and Alzheimer’s disease. Neuron 2008. 59: 190–194.Gritti I., Henny P., Galloni F., Mainville L., Mariotti M., Jones B. E. Stereological estimates of the basal forebrain cell population in the rat, including neurons containing choline acetyltransferase, glutamic acid decarboxylase or phosphate-activated glutaminase and colocalizing vesicular glutamate transporters. Neuroscience 2006. 143 (4): 1051–64.Gulyás A.I., Acsády L., Freund T.F. Structural basis of the cholinergic and serotonergic modulation of GABAergic neurons in the hippocampus. Neurochem. Int. 1999. 34: 359–372.Hamm V., Héraud C., Cassel J.-C., Chantal Mathis C.l., Goutagny R. Precocious Alterations of Brain Oscillatory Activity in Alzheimer’s Disease: A Window of Opportunity for Early Diagnosis and Treatment. Front. Cell. Neurosci. 2015. 9: 491.Hampel H., Mesulam M.M., Cuello A.C., Farlow M.R., Giacobini E., Grossberg G.T., Khachaturian A.S., Vergallo A., Cavedo E., Snyder P.J., Khachaturian Z.S. The cholinergic system in the pathophysiology and treatment of Alzheimer’s disease. Brain. 2018. 141 (7): 1917–33.Hardy J.A., Higgins G.A. Alzheimer’s disease: the amyloid cascade hypothesis. Science 1992. 256: 184–185.Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics. Science 2002. 297: 353–356.Harris M.E., Hensley K., Butterfield D.A., Leedle R.A., Carney J.M. Direct evidence of oxidative injury produced by the Alzheimer’s beta-amyloid peptide (1-40) in cultured hippocampal neurons. Exp. Neurol. 1995. 131(2): 193–202.Haroutunian V., Santucci A.C., Davis K.L. Implications of multiple transmitter system lesions for cholinomimetic therapy in Alzheimer’s disease. Prog. Brain Res. 1990. 84: 333–346.Hasselmo M.E. What is the function of hippocampal theta rhythm? – Linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus 2005. 15: 936–949.Hasselmo M.E. The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol. 2006. 16: 710–715.Hasselmo M.E., Barkai E. Cholinergic modulation of activity-dependent synaptic plasticity in the piriform cortex and associative memory function in a network biophysical simulation. J. Neurosci. 1995. 15: 6592–6604.He G., Li Y., Deng H., Zuo H. Advances in the study of cholinergic circuits in the central nervous system. Ann. Clin. Transl. Neurol. 2023. 10 (12): 2179–2191.Hedden T., Van Dijk K.R., Becker J.A., Mehta A., Sperling R.A., Johnson K.A., Buckner R.L. Disruption of functional connectivity in clinically normal older adults harboring amyloid burden. J. Neurosci. 2009. 29: 12686–12694.Henderson Z., Lu C.B., Janzsó G., Matto N., McKinley C.E., Yanagawa Y., Halasy K. Distribution and role of Kv3.1b in neurons in the medial septum diagonal band complex. Neuroscience 2010. 166: 952–69.Henke H., Lang W. Cholinergic enzymes in neocortex, hippocampus and basal forebrain of non-neurological and senile dementia of Alzheimer-type patients. Brain Res. 1983. 267: 281–291.Herrmann C.S., Demiralp T. Human EEG g oscillations in neuropsychiatric disorders. Clin. Neurophysiol. 2005. 116: 2719–2733.Hey J.A., Yu J.Y., Versavel M., Abushakra S., Kocis P., Power A., Kaplan P.L., Amedio J., Tolar M. Clinical pharmacokinetics and safety of ALZ-801, a novel prodrug of tramiprosate in development for the treatment of Alzheimer’s disease. Clin. Pharmacokinet. 2018. 57: 315–333.Hijazi S., Smit A.B., van Kesteren R.E. Fast-spiking parvalbumin-positive interneurons in brain physiology and Alzheimer’s disease. Mol. Psychiatry. 2023. 28: 4954–4967.Hyman B.T., Kromer L.J., Van Hoesen G.W. Reinnervation of the hippocampal perforant pathway zone in Alzheimer’s disease. Ann. Neurol. 1987. 21 (3): 259–267.Jack C.R., Bennett D.A., Blennow K., Carrillo M.C., Dunn B., Haeberlein S.B., Holtzman D.M., Jagust W., Jessen F., Karlawish J., Liu E., Molinuevo J.L., Montine T., Phelps C., Rankin K.P., Rowe C.C., Scheltens P., Siemers E., Jagust W. Imaging the evolution and pathophysiology of Alzheimer disease. Nat. Rev. Neurosci. 2018. 19 (11): 687–700.Jang H., Arce F.T., Ramachandran S., Capone R., Azimova R., Kagan B.L., Nussinov R., Lal R. Truncated beta-amyloid peptide channels provide an alternative mechanism for Alzheimer’s Disease and Down syndrome. Proc. Natl. Acad. Sci. U.S.A. 2010. 107: 6538–6543.Jeon S.G., Kim Y.J., Kim K.A., Mook-Jung I., Moon M. Visualization of altered hippocampal connectivity in an animal model of alzheimer’s disease. Mol. Neurobiol. 2018. 55: 7886–7899.Jeremic D., Jiménez-Díaz L., Navarro-López J.D. Past, present and future of therapeutic strategies against amyloid-β peptides in Alzheimer’s disease: a systematic review. Ageing Res. Rev. 2021. 72: 101496.Jiang Y., Yuan T.S., Chen Y.C., Guo P., Lian T.H., Liu Y.Y., Liu W., Bai Y.T., Zhang Q., Zhang W., Zhang J.G. Deep brain stimulation of the nucleus basalis of Meynert modulates hippocampal-frontoparietal networks in patients with advanced Alzheimer’s disease. Transl. Neurodegener. 2022. 11 (1): 51.Jimenez S., Baglietto-Vargas D., Caballero C., Moreno-Gonzalez I., Torres M., Sanchez-Varo R., Ruano D., Vizuete M., Gutierrez A., Vitorica J. Inflammatory response in the hippocampus of PS1M146L/APP751SL mouse model of Alzheimer’s disease: age-dependent switch in the microglial phenotype from alternative to classic. J. Neurosci. 2008. 28: 11650–11661.Jongbloed W., Bruggink K.A., Kester M.I., Visser P.J., Scheltens P., Blankenstein M.A., Verbeek M.M., Teunissen C.E., Veerhuis R. Amyloid-beta oligomers relate to cognitive decline in Alzheimer’s disease. J. Alzheimers Dis. 2015. 45: 35–43.Johnson D.A., Zambon N.J., Gobbs R.B. Selective lesion of cholinergic neurons in the medial septum by 192 IgG-saporin impairs learning in a delayed matching to position T-maze paradigm. Brain Res. 2002. 943: 132–141.Johnson E.C.B., Ho K., Yu G.Q., Das M., Sanchez P.E., Djukic B., Lopez I., Yu X., Gill M., Zhang W., Paz J.T., Palop J.J., Mucke L. Behavioral and neural network abnormalities in human APP transgenic mice resemble those of App knock-in mice and are modulated by familial Alzheimer’s disease mutations but not by inhibition of BACE1. Mol. Neurodegener. 2020. 15 (1): 53.Joshi A., Salib M., Viney T.J., Dupret D., Somogyi P. Behavior dependent activity and synaptic organization of septo-hippocampal gabaergic neurons selectively targeting the hippocampal ca3 area. Neuron 2017. 96: 1342–1357.Jutras M.J., Fries P., Buffalo E.A. g-band synchronization in the macaque hippocampus and memory formation. J. Neurosci. 2009. 29: 12521–12531.García-González L., Paumier J.M., Louis L., Pilat D., Bernard A., Stephan D., Jullien N., Checler F., Nivet E., Khrestchatisky M., Baranger K., Rivera S. MT5-MMP controls APP and β-CTF/C99 metabolism through proteolytic-dependent and -independent mechanisms relevant for Alzheimer’s disease. FASEB J. 2021. 35 (7): e21727.Gauthier-Umaña C., Muñoz-Cabrera J., Valderrama M., Múnera A., Nava-Mesa M.O. Acute Effects of Two Different Species of Amyloid-β on Oscillatory Activity and Synaptic Plasticity in the Commissural CA3-CA1 Circuit of the Hippocampus. Neural Plast. 2020. 8869526.George A.A., Vieira J.M., Xavier-Jackson C., Gee M.T., Cirrito J.R., Bimonte-Nelson H.A., Picciotto M.R., Lukas R.J., Whiteaker P. Implications of Oligomeric Amyloid-Beta (oAb42) Signaling through a7b2-Nicotinic Acetylcholine Receptors (nAChRs) on Basal Forebrain Cholinergic Neuronal Intrinsic Excitability and Cognitive Decline Neurobiology of Disease. J. Neurosci. 2021. 41(3): 555–575.Geula C., Dunlop S.R., Ayala I., Kawles A.S., Flanagan M.E., Gefen T., Mesulam M.M. Basal forebrain cholinergic system in the dementias: Vulnerability, resilience, and resistance. J. Neurochem. 2021. 158 (6): 1394–1411.Giovannini M.G., Rakovska A., Benton R.S., Pazzagli M., Bianchi L., Pepeu G. Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats. Neuroscience 2001. 106 (1): 43–53.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.Конец формыGoutagny R., Krantic S. Hippocampal oscillatory activity in Alzheimer’s disease: toward the identification of early biomarkers? Aging Dis. 2013. 4: 134–140.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.Gritti I., Henny P., Galloni F., Mainville L., Mariotti M., Jones B. E. Stereological estimates of the basal forebrain cell population in the rat, including neurons containing choline acetyltransferase, glutamic acid decarboxylase or phosphate-activated glutaminase and colocalizing vesicular glutamate transporters. Neuroscience 2006. 143: 1051–1064.Grueninger F., Bohrmann B., Czech C., Ballard T.M., Frey J.R., Weidensteiner C., von Kienlin M., Ozmen L. Phosphorylation of Tau at S422 is enhanced by Abeta in TauPS2APP triple transgenic mice. Neurobiol. Dis. 2010. 37 (2): 294–306.Kabogo D., Rauw G., Amritraj A., Baker G., Kar S. ß-amyloid-related peptides potentiate K+-evoked glutamate release from adult rat hippocampal slices Neurobiol. Aging 2010. 31(7):1164–1172.Kazim S.F., Seo J.H., Bianchi R., Larson C.S., Sharma A., Wong R.K.S., Gorbachev K.Y., Pereira A.C. Neuronal Network Excitability in Alzheimer’s Disease: The Puzzle of Similar versus Divergent Roles of Amyloid β and Tau. eNeuro 2021. 8 (2): ENEURO.0418-20.2020.Kesler S.R., Acton P., Rao V., Ray W.J. Functional and structural connectome properties in the 5xfad transgenic mouse model of alzheimer’s disease. Netw. Neurosci. 2018. 2: 241–258.Khakpai F., Zarrindast M.R., Nasehi M., Haeri-Rohani A., Eidi A. The role of glutamatergic pathway between septum and hippocampus in the memory formation. EXCLI J. 2013a. 12: 41–51.Khakpai F., Nasehi M., Haeri-Rohani A., Eidi A., Zarrindast M.R. Septo-hippocampo-septal loop and memory formation. Basic Clin. Neurosci. 2013b. 4: 5–23.Kim S., Nam Y., Jeong Y.O., Park H.H., Lee S.K., Shin S.J., Jung H., Kim B.H., Hong S.B., Park Y.H., Kim J., Yu J., Yoo D.H., Park S.H., Jeon S.G., Moon M. Topographical Visualization of the Reciprocal Projection between the Medial Septum and the Hippocampus in the 5XFAD Mouse Model of Alzheimer’s Disease. Int. J. Mol. Sci. 2019. 20: 3992.Kirshenbaum G.S., Chang C.Y., Bompolaki M., Bradford V.R., Bell J., Kosmidis S., Shansky R.M., Orlandi J., Savage L.M., Harris A.Z., David Leonardo E., Dranovsky A. Adult-born neurons maintain hippocampal cholinergic inputs and support working memory during aging. Mol Psychiatry. 2023.doi: 10.1038/s41380-023-02167-z. Epub ahead of print.Kim T., Thankachan S., McKenna J.T., McNally J.M., Yang C., Choi J.H., Chen L., Kocsis B., Deisseroth K., Strecker R.E., Basheer R., Brown R.E., McCarley R.W. Cortically projecting basal forebrain parvalbumin neurons regulate cortical gamma band oscillations. Proc. Natl. Acad. Sci. U.S.A. 2015. 112: 3535–3540.Kitchigina V.F., Vinogradova O.S., Bragin A.G. Neuronal Activity of the Septum Transplanted into the Neocortical Barrel Field of the Rat. Restorative Neurology & Neurosci. 1991. 2: 109–122.Klinkenberg I., Blokland A. The validity of scopolamine as a pharmacological model for cognitive impairment: A review of animal behavioral studies. Neurosci. Biobehav. Rev. 2010. 34: 1307–1350.Klinkenberg I., Sambeth A., Blokland A. Acetylcholine and attention. Behav. Brain Res. 2011. 221: 430–442.Koliatsos V.E., Martin L.J., Walker L.C., Richardson R.T., Delong M.R., Price D.L. Topographic, non-collateralized basal forebrain projections to amygdala, hippocampus and anterior cingulate cortex in the rhesus monkey. Brain Research 1988. 463: 133–139.Koulousakis P., Andrade P., Visser-Vandewalle V., Sesia T. The Nucleus Basalis of Meynert and Its Role in Deep Brain Stimulation for Cognitive Disorders: A Historical Perspective. J Alzheimers Dis. 2019. 69 (4): 905–919.Kondo H., Zaborszky L. Topographic organization of the basal forebrain projections to the perirhinal, postrhinal, and entorhinal cortex in rats. J. Comp. Neurol. 2016. 524: 2503–2515.Koulousakis P., van den Hove D., Visser-Vandewalle V., Sesia T. Cognitive improvements after intermittent deep brain stimulation of the nucleus basalis of Meynert in a transgenic rat model for Alzheimer’s disease: a preliminary approach. J. Alzheimers Dis. 2020. 73: 461–6.Kuhn J., Hardenacke K., Shubina E., Lenartz D., Visser-Vandewalle V., Zilles K., Sturm V., Freund H.J. Deep brain stimulation of the nucleus basalis of Meynert in early stage of Alzheimer’s dementia. Brain Stimul. 2015. 8: 838–9.Kuhn J., Hardenacke K., Lenartz D., Gruendler T., Ullsperger M., Bartsch C., Mai J.K., Zilles K., Bauer A., Matusch A., Schulz R.J., Noreik M., Bührle C.P., Maintz D., Woopen C., Häussermann P., Hellmich M., Klosterkötter J., Wiltfang J., Maarouf M., Freund H.J., Sturm V. Deep brain stimulation of the nucleus basalis of Meynert in Alzheimer’s dementia. Mol Psychiatry. 2015. 20: 353–60.Kumar S., Morton H., Sawant N., Orlov E., Bunquin L.E., Pradeepkiran J.A., Alvir R., Reddy P.H. MicroRNA-455-3p improves synaptic, cognitive functions and extends lifespan: Relevance to Alzheimer’s disease. Redox Biol. 2021. 48: 102182.Kwart D., Gregg A., Scheckel C., Murphy E.A., Paquet D., Duffield M., Fak J., Olsen O., Darnell R.B., Tessier-Lavigne M. A Large Panel of Isogenic APP and PSEN1 Mutant Human iPSC Neurons Reveals Shared Endosomal Abnormalities Mediated by APP β-CTFs, Not Aβ. Neuron. 2019. 104 (2): 256–270.Kwakowsky A., Potapov K., Kim S., Peppercorn K., Tate W.P., Ábrahám I.M. Treatment of beta amyloid 1-42 (Aβ(1-42))-induced basal forebrain cholinergic damage by a non-classical estrogen signaling activator in vivo. Sci. Rep. 2016. 6: 21101.Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., Morgan T.E., Rozovsky I., Trommer B., Viola K.L., Wals P., Zhang C., Finch C.E., Krafft G.A., Klein W.L. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U. S. A. 1998. 95: 6448–6453.Lane C.A., Hardy J., Schott J.M. Alzheimer’s disease. Eur. J. Neurol. 2018. 25: 59–70.Lazzari C., Kipanyula M.J., Agostini M., Pozzan T., Fasolato C.Aβ42 oligomers selectively disrupt neuronal calcium release. Neurobiol. Aging. 2015. 36 (2): 877–885.Leandrou S., Petroudi S., Kyriacou P. A., Reyes-Aldasoro C. C., Pattichis C. S. Quantitative MRI brain studies in mild cognitive impairment and Alzheimer’s disease: a methodological review. IEEE Rev. Biomed. Eng. 2018. 11: 97–111.Leão R.N., Colom L.V., Borgius L., Kiehn O., Fisahn A. Medial septal dysfunction by Aβ-induced KCNQ channel-block in glutamatergic neurons. Neurobiol Aging. 2012. 33(9): 2046–2061.Lehmann J., Nagy J.I., Atmadia S., Fibiger H.C. The nucleus basalis magnocellularis: the origin of a cholinergic projection to the neocortex of the rat. Neuroscience. 1980. 5 (7): 1161–1174.Lehmann O., Grottick A. J., Cassel J.-C., Higgins G. A. A double dissociation between serial reaction time and radial maze performance in rats subjected to 192 IgG-saporin lesions of the nucleus basalis and/or the septal region. Eur. J. Neurosci. 2003. 18: 651–666.Lepeta K., Lourenco M.V., Schweitzer B.C., Martino Adami P.V., Banerjee P., Catuara-Solarz S., de La Fuente Revenga M., Guillem A.M., Haidar M., Ijomone O.M., Nadorp B., Qi L., Perera N.D., Refsgaard L.K., Reid K.M., Sabbar M., Sahoo A., Schaefer N., Sheean R.K., Suska A., Verma R., Vicidomini C., Wright D., Zhang X.D., Seidenbecher C. Synaptopathies: Synaptic dysfunction in neurological disorders–A review from students to students. J. Neurochem. 2016. 138: 785–805.Levy M. L., Cummings J. L., Kahn-Rose R. Neuropsychiatric symptoms and cholinergic therapy for Alzheimer’s disease. Gerontology 1999. 45(Suppl 1): 15–22.Li S., Hong S., Shepardson N.E., Walsh D.M., Shankar G.M., Selkoe D. Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 2009. 62(6): 788–801.Li S., Jin M., Koeglsperger T., Shepardson N.E., Shankar G.M., Selkoe D.J. Soluble Aβ oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. J. Neurosci. 2011. 31(18): 6627–6638.Liebscher S., Meyer-Luehmann M. A Peephole into the Brain: Neuropathological Features of Alzheimer’s Disease Revealed by in vivo Two-Photon Imaging. Front. Psychiatry. 2012. 3: 26.Lin S.C., Brown R.E., Hussain Shuler M.G., Petersen C.C., Kepecs A. Optogenetic Dissection of the Basal Forebrain Neuromodulatory Control of Cortical Activation, Plasticity, and Cognition. J Neurosci. 2015. 35 (41): 13896–903.Lindvall O., Stenevi U. Dopamine and noradrenaline neurons projecting to the septal area in the rat. Cell Tissue Res. 1978. 190 (3): 383–407.Lisgaras C.P., Scharfman H.E. High Frequency Oscillations (>250Hz) Outnumber Interictal Spikes in Preclinical Studies of Alzheimer’s Disease Neurobiol Dis. 2023. 187: 106294.Lisman J. E., Jensen O. The theta-g neural code. Neuron 2013. 77: 1002–1016.Liu R., Crawford J., Callahan P.M., Terry A.V., Constantinidis C., Blake D.T. Intermittent stimulation of the nucleus basalis of Meynert improves working memory in adult monkeys. Curr Biol. 2017. 27: 2640–2646.e4.Liu X., Chen K., Wu T., Weidman D., Lure F., Li J. Use of multimodality imaging and artificial intelligence for diagnosis and prognosis of early stages of Alzheimer’s disease. Transl. Res. 2018. 194: 56–67.Liu A.K., Chang R.C., Pearce R.K., Gentleman S.M. Nucleus basalis of Meynert revisited: anatomy, history and differential involvement in Alzheimer’s and Parkinson’s disease. Acta Neuropathol. 2015. 129 (4): 527–40.Liu X., Hou D., Lin F., Luo J., Xie J., Wang Y., Tian Y. The role of neurovascular unit damage in the occurrence and development of Alzheimer’s disease. Rev. Neurosci. 2019. 30 (5): 477–484.Loreth D., Ozmen L., Revel F.G., Knoflach F., Wetzel P., Frotscher M., Metzger F., Kretz O. Selective degeneration of septal and hippocampal GABAergic neurons in a mouse model of amyloidosis and tauopathy. Neurobiol. Dis. 2012. 47 (1): 1–12.Malkov A., Popova I., Ivanov A., Jang S.-S., Yoon S. Y., Osypov A., Huang Y., Zilberter Y., Zilberter M. Aβ initiates brain hypometabolism, network dysfunction and behavioral abnormalities via NOX2-induced oxidative stress in mice. Communications biology 2021. 4 (1):1054.Malkov A., Shevkova L., Latyshkova A., Kitchigina V. Theta and gamma hippocampal–neocortical oscillations during the episodic-like memory test: impairment in epileptogenic rats. Experimental Neurology 2022. 354: 114110.Mamad O., McNamara H.M., Reilly R.B., Tsanov M. Medial septum regulates the hippocampal spatial representation. Front. Behav. Neurosci. 2015. 9: 166.Mangalmurti A., Lukens J.R. How neurons die in Alzheimer’s disease: Implications for neuroinflammation. Curr Opin Neurobiol. 2022. 75: 102575.Mann D.M., Yates P.O. Neurotransmitter deficits in Alzheimer’s disease and in other dementing disorders. Hum. Neurobiol. 1986. 5: 147–158.Manseau F., Danik M., Williams S. A functional glutamatergic neurone network in the medial septum and diagonal band area. J Physiol. 2005. 566: 865–884.Martinez J.L., Zammit M.D., West N.R., Christian B.T., Bhattacharyya A. Basal Forebrain Cholinergic Neurons: Linking Down Syndrome and Alzheimer’s Disease. Front. Aging Neurosci. 2021. 13: 703876.Martinez-Rubio C., Paulk A.C., McDonald E.J, Widge A.S., Eskandar E.N. Multimodal Encoding of Novelty, Reward, and Learning in the Primate Nucleus Basalis of Meynert. J. Neurosci. 2018. 38(8): 1942–1958.Marsh J., Alifragis P. Synaptic dysfunction in Alzheimer’s disease: the effects of amyloid beta on synaptic vesicle dynamics as a novel target for therapeutic intervention. Neural Regen. Res. 2018. 13(4): 616–623.Martinez-Rubio C., Paulk A.C., McDonald E.J., Widge A.S., Eskandar E.N. Multimodal Encoding of Novelty, Reward, and Learning in the Primate Nucleus Basalis of Meynert. J Neurosci. 2018. 38 (8): 1942–1958.Masliah E., Terry R.D., DeTeresa R.M., Hansen L.A. Immunohistochemical quantification of the synapse-related protein synaptophysin in alzheimer disease. Neurosci. Lett. 1989. 103: 234–239.Mamad O., McNamara H.M., Reilly R.B., Tsanov M. Medial septum regulates the hippocampal spatial representation. Front. Behav. Neurosci. 2015. 9: 166.Martin-Moreno A.M., Brera B., Spuch C., Carro E., Garcia-Garcia L., Delgado M., Pozo M.A., Innamorato N.G., Cuadrado A., de Ceballos M.L. Prolonged oral cannabinoid administration prevents neuroinflammation, lowers β-amyloid levels and improves cognitive performance in Tg APP 2576 mice. J. Neuroinflammation. 2012. 9: 8.Marucci G., Buccioni M., Ben D.D., Lambertucci C., Volpini R., Amenta F. Efficacy of acetylcholinesterase inhibitors in Alzheimer’s disease. Neuropharmacology. 2021. 190: 108352.Meftah S., Gan J. Alzheimer’s disease as a synaptopathy: Evidence for dysfunction of synapses during disease progression. Front Synaptic Neurosci. 2023. 15: 1129036.Melichercik A.M., Elliott K.S., Bianchi C., Ernst S.M., Winters B.D. Nicotinic receptor activation in perirhinal cortex and hippocampus enhances object memory in rats. Neuropharmacology 2012. 62: 2096–2105.Mesulam M.M. Cholinergic circuitry of the human nucleus basalis and its fate in Alzheimer’s disease. J Comp Neurol. 2013. 521 (18): 4124–44.Mesulam M.M., Lalehzari N., Rahmani F., Ohm D., Shahidehpour R., Kim G., Gefen T., Weintraub S., Bigio E., Geula C. Cortical cholinergic denervation in primary progressive aphasia with Alzheimer pathology. Neurology 2019. 92: e1580–e1588.Mesulam M.M., Mufson E.J., Wainer B.H., Levey A.I. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 1983. 10: 1185–1201.Mesulam M.M., Geula C.J. Nucleus basalis (Ch4) and cortical cholinergic innervation in the human brain: observations based on the distribution of acetylcholinesterase and choline acetyltransferase. Comp Neurol. 1988. 275 (2): 216–40.Mesulam M.M., Van Hoesen G.W. Acetylcholinesterase-rich projections from the basal forebrain of the rhesus monkey to neocortex. Brain Research 1976. 109: 152–157.Meynert T.H. The brain of mammals. In: A manual of histology (Stricker S, ed), New York: Wood. 1872. 650–766.Mikulca J.A., NguyenV., Gajdosik D.A., Teklu S.G., Giunta E.A., Lessa E.A., Tran C.H., Terak E.C., Raffa R.B. Potential novel targets for Alzheimer pharmacotherapy: II. Update on secretase inhibitors and related approaches. J. Clin. Pharm. Ther. 2014. 39: 25–37.Milner T.A., Veznedaroglu E.J. Serotonin-containing terminals synapse on septohippocampal neurons in the rat. Neurosci Res. 1993. 36 (3): 260–71.Milner T.A., Hammel J.R., Ghorbani T.T., Wiley R.G., Pierce J.P. Septal cholinergic deafferentation of the dentate gyrus results in a loss of a subset of neuropeptide Y somata and an increase in synaptic area on remaining neuropeptide Y dendrites. Brain Res. 1999. 831 (1–2): 322–36.Mocellin P., Mikulovic S. The role of the medial septum-associated networks in controlling locomotion and motivation to move. Front. Neural Circuits 2021. 15: 699798.Moon M., Cha M.Y., Mook-Jung I. Impaired hippocampal neurogenesis and its enhancement with ghrelin in 5xfad mice. J. Alzheimer’s Dis. 2014. 41: 233–241.Moon M., Hong H.S., Nam D.W., Baik S.H., Song H., Kook S.Y., Kim Y.S., Lee J., Mook-Jung I. Intracellular amyloid-beta accumulation in calcium-binding protein-deficient neurons leads to amyloid-beta plaque formation in animal model of Аlzheimer’s disease. J. Alzheimer’s Dis. 2012. 29: 615–628.Moore R.Y., Halaris A.E., Jones B.E. Serotonin neurons of the midbrain raphe: ascending projections. J. Comp. Neurol. 1978. 180: 417–438.Mucke L., Selkoe D.J. Neurotoxicity of amyloid b-protein: synaptic and network dysfunction. Cold Spring Harb. Perspect. Med. 2012. 2: a006338.Mufson E.J., Counts S.E., Perez S.E., Ginsberg S.D. Cholinergic system during the progression of Alzheimer’s disease: therapeutic implications. Expert Rev Neurother. 2008. 8 (11): 1703–18.Mufson E.J., Mahady L., Waters D., Counts S.E., Perez S. E., DeKosky S., Ginsberg S.D., Ikonomovic M.D., Scheff S., Binder L. Hippocampal Plasticity During the Progression of Alzheimer’s disease. Neuroscience. 2015. 309: 51–67.Muir J.L. Acetylcholine, aging, and Alzheimer’s disease. Pharmacol Biochem Behav. 1997. 56 (4): 687–96.Muller C., Remy S. Septo-hippocampal interaction. Cell Tissue Res. 2018. 373: 565–575.Mysin I.E., Kitchigina V.F., Kazanovich Y.B. Phase relations of theta oscillations in a computer model of the hippocampal CA1 field: Key role of Schaffer collaterals. Neural Netw. 2019. 116: 119–138.Mysin I., Shubina L. From mechanisms to functions: The role of theta and gamma coherence in the intrahippocampal circuits. Hippocampus 2022. 32(5): 342–358.Naser P.V., Kuner R. Molecular, Cellular and Circuit Basis of Cholinergic Modulation of Pain Neuroscience 2018. 387:135–148.Nazmuddin M., Philippens I.H., van Laar T. Electrical stimulation of the nucleus basalis of Meynert: a systematic review of preclinical and clinical data. Sci Rep. 2021. 11: 11751.Negash S., Wilson R.S., Leurgans S.E., Wolk D.A., Schneider J.A., Buchman A.S., Bennett D.A., Arnold S.E. Resilient brain aging: characterization of discordance between Alzheimer’s disease pathology and cognition. Curr. Alzheimer Res. 2013. 10 (8): 844–851.Nemy M., Dyrba M., Brosseron F., Buerger K, Dechent P, Dobisch L, Ewers M, Fliessbach K, Glanz W, Goerss D, Heneka MT, Hetzer S., Incesoy E.I., Janowitz D., Kilimann I., Laske C., Maier F., Munk M.H., Perneczky R., Peters O., Preis L., Priller J., Rauchmann B.S., Röske S., Roy N., Scheffler K., Schneider A., Schott B.H., Spottke A., Spruth E.J., Wagner M., Wiltfang J., Yakupov R., Eriksdotter M., Westman E., Stepankova O., Vyslouzilova L., Düzel E., Jessen F., Teipel S.J., Ferreira D. Cholinergic white matter pathways along the Alzheimer’s disease continuum. Brain 2023. 146 (5): 2075–2088.Nickerson Poulin A., Guerci A., El Mestikawy S., Semba K. Vesicular glutamate transporter 3 immunoreactivity is present in cholinergic basal forebrain neurons projecting to the basolateral amygdala in rat. J. Comp. Neurol. 2006. 498: 690–711.Nicoll J.A., Buckland G.R., Harrison C.H., Page A., Harris S., Love S., Neal J.W., Holmes C., Boche D. Persistent neuropathological effects 14 yearsfollowing amyloid-beta immunization in Alzheimer’s disease. Brain 2019. 142: 2113–2126.Nimmrich V., Ebert U. Is Alzheimer’s disease a result of presynaptic failure? Synaptic dysfunctions induced by oligomeric beta-amyloid. Rev. Neurosci. 2009. 20: 1–12.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: 10129–10140.Okada K., Hashimoto K., Kobayashi K. Cholinergic regulation of object recognition memory. Front Behav Neurosci. 2022. 16: 996089.Okada K., Nishizawa K., Kobayashi T., Sakata S., Kobayashi K. Distinct roles of basal forebrain cholinergic neurons in spatial and object recognition memory. Sci. Rep. 2015. 5: 13158.Okada K., Okaichi H. Functional cooperation between the hippocampal subregions and the medial septum in unreinforced and reinforced spatial memory tasks. Behav Brain Res. 2010. 209 (2): 295–304.Olgiati P., Politis A.M., Papadimitriou G.N., De RonchiD., Serretti A. Genetics of late-onset Alzheimer’s disease: update from the alzgene database and analysis of shared pathways. Int. J. Alzheimers Dis. 2011. 2011: 832–379.Ohno M. Failures to reconsolidate memory in a mouse model of alzheimer’s disease. Neurobiol. Learn. Mem. 2009. 92. 455–459.Orobets K.S., Karamyshev A.L. Amyloid Precursor Protein and Alzheimer’s Disease. Int J Mol Sci. 2023. 24 (19): 14794.Pákáski M., Kálmán J. Interactions between the amyloid and cholinergic mechanisms in Alzheimer’s disease. Neurochem Int. 2008. 53 (5): 103–11.Palop J.J., Mucke L. Synaptic depression and aberrant excitatory network activity in Alzheimer’s disease: Two faces of the same coin? NeuroMolecular. Medicine 2010b. 12 (1): 48–55.Palop J.J., Chin J., Roberson E.D., Wang J., Thwin M.T., Bien-Ly N., Yoo J., Ho K.O., Yu G.Q., Kreitzer A., Finkbeiner S., Noebels J.L., Mucke L. Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of alzheimer’s disease. Neuron 2007. 55: 697–711.Palop J.J., Mucke L. Epilepsy and Cognitive Impairments in Alzheimer Disease. Arch. Neurol. 2009. 66 (4): 435–440.Palop J.J., Mucke L. Amyloid-beta-induced neuronal dysfunction in alzheimer’s disease: From synapses toward neural networks. Nat. Neurosci. 2010. 13: 812–818.Panza F., Lozupone M., Logroscino G., Imbimbo B.P. A critical appraisal of amyloid-beta-targeting therapies for Alzheimer disease. Nat. Rev. Neurol. 2019. 15: 73–88.Park G., Nhan H.S., Tyan S.H., Kawakatsu Y., Zhang C., Navarro M., Koo E.H. Caspase Activation and Caspase-Mediated Cleavage of APP Is Associated with Amyloid β-Protein-Induced Synapse Loss in Alzheimer’s Disease. Cell Rep. 2020. 31: 107839.Pereira C., Agostinho P., Moreira P.I., Cardoso S.M., Oliveira C.R. Alzheimer’s disease-associated neurotoxic mechanisms and neuroprotective strategies. Curr Drug Targets CNS Neurol. Disord. 2005. 4: 383–403.Pereira J.B., Hall S., Jalakas M., Grothe M.J., Strandberg O., Stomrud E., Westman E., van Westen D., Hansson O. Longitudinal degeneration of the basal forebrain predicts subsequent dementia in Parkinson’s disease. Neurobiol Dis. 2020. 139: 104831.Perry E.K., Johnson M., Ekonomou A., Perry R.H., Ballard C., Attems J. Neurogenic abnormalities in Alzheimer’s disease differ between stages of neurogenesis and are partly related to cholinergic pathology. Neurobiol Dis. 2012. 47: 155–62.Perry T., Hodges H., Gray J.A. Behavioural, histological and immunocytochemical consequences following 192 IgG-saporin immunolesions of the basal forebrain cholinergic system. Brain Res. Bull. 2001. 54: 29–48.Petsche H., Stumpf C. Topographic and toposcopic study of origin and spread of the regular synchronized arousal pattern in the rabbit. Electroencephalography and Clinical Neurophysiology 1960. 12: 589–600.Petsche H., Gogolak G., Zwieten P.A. Rhythmicity of septal cell discharges at various levels of reticular excitation. EEG a. Clin. Neurophysiol. 1965. 19: 25–33.Peyrache A., Khamassi M., Benchenane K., Wiener S.I., Battaglia F.P. Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat. Neurosci. 2009. 12: 919–926.Pimplikar S.W., Nixon R.A., Robakis N.K., Shen J., Tsai L.-H. Amyloid-independent mechanisms in Alzheimer’s disease pathogenesis. J. Neurosci. 2010. 30: 14946–14954.Poppe L., Rué L., Timmers M., Lenaerts A., Storm A., Callaerts-Vegh Z., Courtand G., de Boer A., Smolders S., Van Damme P., Van Den Bosch L., D’Hooge R., De Strooper B., Robberecht W., Lemmens R. EphA4 loss improves social memory performance and alters dendritic spine morphology without changes in amyloid pathology in a mouse model of Alzheimer’s disease. Alzheimers Res. Ther. 2019. 11 (1):102.Price D.L., Tanzi R.E., Borchelt D.R., Sisodia S.S. Alzheimer’s disease: genetic studies and transgenic models. Annu. Rev. Genet. 1998. 32: 461–493.Plascencia-Villa G., Perry G. Preventive and Therapeutic Strategies in Alzheimer’s Disease: Focus on Oxidative Stress, Redox Metals, and Ferroptosis. Antioxid Redox Signal. 2021. 34 (8): 591–610.Puzzo D., Privitera L., Leznik E., Fà M., Staniszewski A., Palmeri A., Arancio O. Picomolar amyloid-beta positively modulates synaptic plasticity and memory in hippocampus. J. Neurosci. 2008. 28(53): 14537–14545.Qu X., Lin L., Yi W., Sun C., Chen Y., Chen Y. Early Changes in Transcriptomic Profiles in Synaptodendrosomes Reveal Aberrant Synaptic Functions in Alzheimer’s Disease. Int J Mol Sci. 2022. 23 (16): 8888.Querfurth H.W., LaFerla F.M. Alzheimer’s disease. N. Engl. J. Med. 2010. 362: 329–344.Rangachari V., Dean D. N., Rana P., Vaidya A., Ghosh P. Cause and Consequence of Aβ – Lipid Interactions in Alzheimer Disease PathogenesisBiochim Biophys Acta Biomembr. 2018. 1860 (9): 1652–1662.Raghanti M.A., Simic G., Watson S., Stimpson C.D., Hof P.R., Sherwood C.C. Comparative analysis of the nucleus basalis of Meynert among primates. Neuroscience 2011. 184: 1–15.Riascos D., Girgis D., Baker-Nigh A., Nicholas A., Geula C. Age-related calcium dysregulation may explain selective neuronal vulnerability in Alzheimer’s disease: The basal forebrain cholinergic model. Alzheim Demen. 2010. 6 (Suppl. 1): S386.Riascos D., de Leon D., Baker-Nigh A., Nicholas A., Yukhananov R., Bu J., Wu C.K., Geula C. Age-related loss of calcium buffering and selective neuronal vulnerability in Alzheimer’s disease. Acta Neuropathologica 2011. 122: 565–576.Richardson R.T., DeLong M.R. Context-dependent responses of primate nucleus basalis neurons in a go/no-go task. J. Neurosci. 1990. 10: 2528–2540.Rintoul G.L., Raymond L.A., Baimbridge K.G. Calcium buffering and protection from excitotoxic cell death by exogenous calbindin-D28k in HEK 293 cells. Cell Calcium 2001. 29: 277–287.Roland J.J., Savage L.M. The role of cholinergic and gabaergic medial septal/diagonal band cell populations in the emergence of diencephalic amnesia. Neuroscience 2009. 160: 32–41.Rubio S.E., Vega-Flores G., Martínez A., Bosch C., Pérez-Mediavilla A., del Río J., Gruart A., Delgado-García J.M., Soriano E., Pascual M. Accelerated aging of the GABAergic septohippocampal pathway and decreased hippocampal rhythms in a mouse model of Alzheimer’s disease. FASEB J. 2012. 26: 4458e4467Russo M. J., Cohen G., Campos J., Martin M.E., Clarens M.F., Sabe L., Barcelo E., Allegri R.F. Usefulness of discriminability and response bias indices for the evaluation of recognition memory in mild cognitive impairment and Alzheimer Disease. Dement. Geriatr. Cogn. Disord. 2017. 43 (1–2): 1–14.Russell C.L., Semerdjieva S., Empson R.M., Austen B.M., Beesley P.W., Alifragis P. Amyloid-β acts as a regulator of neurotransmitter release disrupting the interaction between synaptophysin and VAMP2. PLoS One 2012. 7(8): e43201.Salib M., Joshi A., Katona L., Howarth M., Micklem B.R., Somogyi P., Viney T.J. GABAergic Medial Septal Neurons with Low-Rhythmic Firing Innervating the Dentate Gyrus and Hippocampal Area CA3. J. Neurosci. 2019. 39 (23): 4527–4549.Samudra N., Ranasinghe K., Kirsch H., Rankin K., Miller B. Etiology and Clinical Significance of Network Hyperexcitability in Alzheimer’s Disease: Unanswered Questions and Next Steps. J. Alzheimers Dis. 2023. 92 (1):13–27.Sarkis R.A., Willment K.C., Gale S.A., Dworetzky B.A. Recurrent Epileptic Auras As a Presenting Symptom of Alzheimer’s Disease. Front Neurol. 2017. 8: 360.Sauseng P., Klimesch W., Heise K.F., Gruber W.R., Holz E., Karim A.A., Glennon M., Gerloff C., Birbaumer N., Hummel F.C. Brain oscillatory substrates of visual short-term memory capacity. Curr. Biol. 2009. 19 (21): 1846–1852.Savage S., Kehr J., Olson L., Mattsson A. Impaired social interaction and enhanced sensitivity to phencyclidine-induced deficits in novel object recognition in rats with cortical cholinergic denervation. Neuroscience 2011. 195: 60–69.Schmitz T.W., Nathan Spreng R. Alzheimer’s Disease Neuroimaging Initiative. Basal forebrain degeneration precedes and predicts the cortical spread of Alzheimer’s pathology. Nat Commun. 2016. 7: 13249.Schmitz T.W., Zaborszky L. Spatial topography of the basal forebrain cholinergic projections: Organization and vulnerability to degeneration. Handb. Clin. Neurol. 2021. 179: 159–173.Selkoe D.J. Alzheimer’s disease is a synaptic failure. Science 2002. 298: 789–791.Selkoe D.J. Preventing Alzheimer’s disease. Science 2012. 337: 1488–1492.Selkoe D.J., Hardy J. The amyloid hypothesis of Alzheimer’s disease at 25 years. EMBO Mol. Med. 2016. 8: 595–608.Serrano-Pozo A., Das S., Hyman B.T. APOE and Alzheimer’s disease: advances in genetics, pathophysiology, and therapeutic approaches. Lancet Neurol. 2021. 20 (1): 68–80.Sheline Y.I., Raichle M.E., Snyder A.Z., Morris J.C., Head D., Wang S., Mintun M.A. Amyloid plaques disrupt resting state default mode network connectivity in cognitively normal elderly. Biol. Psychiatry 2010. 67: 584–587.Shors T.J. From stem cells to grandmother cells: how neurogenesis relates to learning and memory. Cell Stem Cell 2008. 3: 253–8.Sirota A., Montgomery S., Fujisawa S., Isomura Y., Zugaro M., Buzsáki G. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 2008. 60: 683–697.Siskova Z., Justus D., Kaneko H., Friedrichs D., Henneberg N., Beutel T., Pitsch J., Schoch S., Becker A., von der Kammer H., Remy S. Dendritic structural degeneration is functionally linked to cellular hyperexcitability in a mouse model of alzheimer’s disease. Neuron 2014. 84 (5): 1023–1033.Sleegers K., Van Duijn C.M. Alzheimer’s disease: genes, pathogenesis and risk prediction. Community Genet. 2001. 4: 197–203.Squire L.R., Wixted J.T., Clark R.E. Recognition memory and the medial temporal lobe: A new perspective. Nat. Rev. Neurosci. 2007. 8: 872–883.Smilly J.F., Subramanian M., Mesulam M.M. Monoaminergic-cholinergic interactions in the primate basal forebrain. Neuroscience 1999. 93: 817–829.Snyder H.M., Sperling R.Jr. NIA-AA research framework: toward a biological definition of Alzheimer’s disease. Alzheimers Dement. 2018. 14: 535–562.Solas M., Francis P.T., Franco R., Ramirez M.J. CB2 receptor and amyloid pathology in frontal cortex of Alzheimer’s disease patients. Neurobiol. Aging 2013. 34: 805–808.Soler H., Dorca-Arévalo J., González M., Rubio S.E., Ávila J., Soriano E., Pascual M. The GABAergic septohippocampal connection is impaired in a mouse model of tauopathy. Neurobiol Aging 2017. 49: 40–51.Solopova E., Romero-Fernandez W., Harmsen H., Ventura-Antunes L., Wang E., Shostak A., Maldonado J., Donahue M.J., Schultz D., Coyne T.M., Charidimou A., Schrag M. Fatal iatrogenic cerebral beta-amyloid-related arteritis in a woman treated with lecanemab for Alzheimer’s disease. Nat. Commun. 2023. 14(1): 8220.Sotty F., Danik M., Manseau F., Laplante F., Quirion R., Williams S. Distinct electrophysiological properties of glutamatergic, cholinergic and GABAergic rat septohippocampal neurons: novel implications for hippocampal rhythmicity. J. Physiol. 2003. 551: 927–943.Case D.T., Burton S.D., Gedeon J.Y., Williams S.G., Urban N.N., Seal R.P. Layer- and cell type-selective co-transmission by a basal forebrain cholinergic projection to the olfactory bulb. Nat. Commun. 2017. 8: 652.Sperling R.A., Laviolette P.S., O’Keefe K., O’Brien J., Rentz D.M., Pihlajamaki M., Marshall G., Hyman B.T., Selkoe D.J., Hedden T., Buckner R.L., Becker J.A., Johnson K.A. Amyloid deposition is associated with impaired default network function in older persons without dementia. Neuron 2009. 63 (2): 178–188.Sridharan D., Knudsen E. I. g oscillations in the midbrain spatial attention network: linking circuits to function. Curr. Opin. Neurobiol. 2015. 31: 189–198.Srivastava S., Ahmad R., Khare S.K. Alzheimer’s disease and its treatment by different approaches: A review. Eur J Med Chem. 2021. 216: 113320.Stensrud M.J., Chaudhry F.A., Leergaard T.B., Bjaalie J.G., Gundersen V. Vesicular glutamate transporter-3 in the rodent brain: Vesicular colocalization with vesicular gamma-aminobutyric acid transporter. J. Comp. Neurol. 2013. 521: 3042–3056.Stewart M., Fox S. E. Do septal neurons pace the hippocampal theta rhythm? Trends in Neurosciences 1990. 13: 163–169.Struyfs H., Van Hecke W., Veraart J., Sijbers J., Slaets S., De Belder M., Parizel P.M., Engelborghs S. Diffusion kurtosis imaging: a possible MRI biomarker for ad diagnosis? J. Alzheimers Dis. 2015. 48: 937–948.Subramaniam S., Blake D.T., Constantinidis C. Cholinergic deep brain stimulation for memory and cognitive disorders. J Alzheimers Dis. 2021. 83 (2): 491–503.Sweeney J.E., Lamour Y., Bassant M.H. Arousal-dependent properties of medial septal neurons in the ananesthetized rat. Neuroscience 1992, 48, 353–362.Suresh S., Singh S A., Rushendran R, Vellapandian C., Prajapati B. Alzheimer’s disease: the role of extrinsic factors in its development, an investigation of the environmental enigma. Front Neurol. 2023. 14: 1303111.Takács K., Varga B., Grolmusz V. PDB_Amyloid: an extended live amyloid structure list from the PDB. FEBS Open Bio 2018. 9 (1): 185–190.Takeuchi Y., Nagy A. J., Barcsai L., Li Q., Ohsawa M., Mizuseki K., Berényi A. The Medial Septum as a Potential Target for Treating Brain Disorders Associated With Oscillopathies. Front. Neural Circuits. 2021. 15: 15:701080.Terry A.V., Buccafusco J.J. The cholinergic hypothesis of age and Alzheimer’s disease-related cognitive deficits: recent challenges and their implications for novel drug development. J Pharm Exp Ther. 2003. 306: 821–7.Terry R.D., Masliah E., Salmon D.P., Butters N., DeTeresa R., Hill R., Hansen L.A., Katzman R. Physical basis of cognitive alterations in Alzheimer’s disease: Synapse loss is the major correlate of cognitive impairment. Ann. Neurol. 1991. 30: 572–580.Thal D.R., Rub U., Orantes M., Braak H. Phases of a beta-deposition in the human brain and its relevance for the development of AD. Neurology 2002. 58: 1791–1800.Tinsley C.J., Fontaine-Palmer N.S., Vincent M., Endean E.P., Aggleton J.P., Brown M.W., Warburton E.C. Differing time dependencies of object recognition memory impairments produced by nicotinic and muscarinic cholinergic antagonism in perirhinal cortex. Learn. Mem. 2011. 18 (7): 484–492.Tort A.B.L., Komorowski R.W., Manns J.R., Kopell N.J., Eichenbaum H. Theta-γ coupling increases during the learning of item-contextassociations. Proc. Natl. Acad. Sci. U S A 2009. 106: 20942–20947.Toth K., Borhegyi Z., Freund T.F. Postsynaptic targets of GABAergic hippocampal neurons in the medial septum-diagonal band of broca com-plex. J. Neurosci. 1993. 13: 3712–3724.Toth K., Freund T.F., Miles R. Disinhibition of rat hippocampalpyramidal cells by GABAergic afferents from the septum. J. Physiol. (Lond.) 1997. 500: 463–474.Tiraboschi P., Hansen L.A., Alford M., Masliah E., Thal L.J., Corey-Bloom J. The decline in synapses and cholinergic activity is asynchronous in Alzheimer’s disease. Neurology 2000. 55 (9): 1278–83.Turnbull I.M., McGeer P.L., Beattie L., Calne D., Pate B. Stimulation of the basal nucleus of Meynert in senile dementia of Alzheimer’s type. Stereot Funct. Neuros. 1985. 48: 216–21.Twarowski B., Herbet M. Inflammatory Processes in Alzheimer’s Disease – Pathomechanism, Diagnosis and Treatment: A Review. Int J Mol Sci. 2023. 24 (7): 6518.Torres E.M., Perry T.A., Blockland A., Wilkinson L.S., Wiley R.G., Lappi D.A., Dunnet S.B. Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system. Neuroscience 1994. 63: 95–122.Unal G., Crump M.G., Viney T.J., Éltes T., Katona L., Klausberger T., Somogyi P. Spatio-temporal specialization of gabaergic septo-hippocampal neurons for rhythmic network activity. Brain Struc. Funct. 2018. 223 (5): 2409–2432.Van Cauwenberghe C., Van Broeckhoven C., Sleegers K. The genetic landscape of Alzheimer disease: clinical implications and perspectives. Genet Med. 2016. 18 (5): 421–30.van der Hiele K., Vein A.A., van der Welle A., van der Grond J., Westendorp R.G., Bollen E.L., van Buchem M.A., van Dijk J.G., Middelkoop H.A. EEG and MRI correlates of mild cognitive impairment and Alzheimer’s disease. Neurobiol. Aging 2007. 28 (9): 1322–1329.van der Zee E.A., Luiten P.G. Muscarinic acetylcholine receptors in the hippocampus, neocortex and amygdala: A review of immunocytochemical localization in relation to learning and memory. Prog. Neurobiol. 1999. 58: 409–471.Vandecasteele M., Varga V., Berényi A., Papp E., Barthó P., Venance L., Freund T.F., Buzsáki G. Optogenetic Activation of Septal Cholinergic Neurons Suppresses SharpWave Ripples and Enhances Theta Oscillations in the Hippocampus. Proc. Natl. Acad. Sci. USA 2014. 111: 13535–13540.Vega-Flores G., Rubio S.E., Jurado-Parras M.T., Gomez-Climent M.A., Hampe C.S., Manto M., Soriano E., Pascual M., Gruart A., Delgado-Garcia J.M. The gabaergic septohippocampal pathway is directly involved in internal processes related to operant reward learning. Cereb. Cortex 2014. 24: 2093–2107.Varga V., Hangya B., Kranitz K., Ludanyi A., Zemankovics R., Katona I., Shigemoto R., Freund T.F., Borhegyi Z. The presence of pacemaker HCN channels identifies theta rhythmic GABAergic neurons in the medial septum. J. Physiol. 2008. 586: 3893–3915.Varga C., Golshani P., Soltesz I. Frequency-invariant temporal ordering of interneuronal discharges during hippocampal oscillations in awake mice. Proc. Nat. Acad. Sci. USA. 2012. 109: E2726–E2734.Varga C., Oijala M., Lish J., Szabo G.G., Bezaire M., Marchionni I., Golshani P., Soltesz I. Functional fission of parvalbumin interneuron classes during fast network events. eLife 2014. 3: e04006.Varga E., Juhász G., Bozsó Z., Penke B., Fülöp L., Szegedi V. Abeta(1-42) enhances neuronal excitability in the CA1 via NR2B subunit-containing NMDA receptors. Neural Plast. 2014. 2014:584314.Varga E., Juhász G., Bozsó Z., Penke B., Fülöp L., Szegedi V. Amyloid-β1-42 Disrupts Synaptic Plasticity by Altering Glutamate Recycling at the Synapse. J Alzheimers Dis. 2015. 45 (2): 449–56.Vasic V., Barth K., Schmidt M.H.H. Neurodegeneration and Neuro-Regeneration – Alzheimer’s Disease and Stem Cell Therapy. Int J Mol Sci. 2019. 20 (17): 4272.Vega-Flores G., Rubio S.E., Jurado-Parras M.T., Gomez-Climent M.A., Hampe C.S., Manto M., Soriano E., Pascual M., Gruart A., Delgado-Garcia J.M. The gabaergic septohippocampal pathway is directly involved in internal processes related to operant reward learning. Cereb. Cortex 2014. 24: 2093–2107.Viney T.J., Salib M., Joshi A., Unal G., Berry N., Somogyi P. Shared rhythmic subcortical gabaergic input to the entorhinal cortex and presubiculum. eLife 2018. 7: e34395.Vinogradova O.S. Expression, control and probable functional significance of the neuronal theta-rhythm. Progr. Neurobiol. 1995. 45: 523–583.Vinogradova O.S., Brazhnik E.S., Kitchigina V.F., Stafekhina V.S. Acetylcholine, theta-rhythm and activity of hippocampal neurons in the rabbit. -II. Septal input. Neuroscience 1993. 53: 971–979.Vinogradova O.S. Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 2001. 11: 578–598.Vinogradova O.S., Kitchigina V.F., Zenchenko C.I. Pacemaker neurons of the forebrain medial septal area and theta rhythm of the hippocampus. Membr. Cell. Biol. 1998. 11 (6): 715–25.Vogt D.L., Thomas D., Galvan V., Bredesen D.E., Lamb B.T., Pimplikar S.W. Abnormal neuronal networks and seizure susceptibility in mice overexpressing the APP intracellular domain. Neurobiol Aging 2011. 32 (9): 1725–1729.Wang X.J. Pacemaker neurons for the theta rhythm and their synchronization in the septohippocampal reciprocal loop. J. Neurophysiol. 2002. 87: 889–900.Wander C.M., Li Y.D., Bao H., Asrican B., Luo Y.J., Sullivan H.A., Chao T.H., Zhang W.T., Chéry S.L., Tart D.S., Chen Z.K., Shih Y.I., Wickersham I.R., Cohen T.J., Song J. Compensatory remodeling of a septo-hippocampal GABAergic network in the triple transgenic Alzheimer’s mouse model. J Transl Med. 2023. 21 (1): 258.Wang X.J. Pacemaker neurons for the theta rhythm and their synchronization in the septohippocampal reciprocal loop. J. Neurophysiol. 2002. 87: 889–900.Wang J., Fang Y., Wang X., Yang H., Yu X., Wang H. Enhanced g activity and cross-frequency interaction of resting-state electroencephalographic oscillations in patients with Alzheimer’s disease. Front. Aging Neurosci. 2017. 9: 243.Weinstein D.E., Burrola P., Kilpatrick T.J. Increased proliferation of precursor cells in the adult rat brain after targeted lesioning. Brain Res. 1996. 743: 11–16.Whitehouse P.J., Price D.L., Clark A.W., Coyle J.T., DeLong M.R. Alzheimer disease: evidence for selective loss of cholinergic neurons in the nucleus basalis. Ann. Neurol. 1981. 10: 122–126.Whitehouse P.J., Struble R.G., Clark A.W., Price D.L. Alzheimer disease: plaques, tangles, and the basal forebrain. Ann. Neurol. 1982a. 12 (5): 494.Whitehouse P.J., Price D.L., Struble R.G., Clark A.W., Coyle J.T., Delon M.R. Alzheimer’s disease and senile dementia: loss of neurons in the basal forebrain. Science 1982b. 215: 1237e1239.Wilson H., de Natale E.R., Politis M. Nucleus basalis of Meynert degeneration predicts cognitive impairment in Parkinson’s disease. Handbook of Clinical Neurology. 2021. Chapter 12. 179: 19–205. https: //doi.org/10.1016/B978-0-12-819975-6.00010-8.Wilson M.A., Fadel J.R. Cholinergic regulation of fear learning and extinction. J. Neurosci. Res. 2017. 95 (3): 836–852.Winters B.D., Bussey T.J. Removal of cholinergic input to perirhinal cortex disrupts object recognition but not spatial working memory in the rat. Eur. J. Neurosci. 2005. 21: 2263–2270.Wu H., Williams J., Nathans J. Complete morphologies of basal forebrain cholinergic neurons in the mouse. Elife 2014. 3: e02444.Zhang W., Liu W., Patel B., Chen Y., Wang K., Yang A., Meng F., Wagle Shukla A., Cen S., Yu J., Ramirez-Zamora A., Zhang J. Case report: deep brain stimulation of the nucleus basalis of Meynert for advanced Alzheimer’s disease. Front. Hum. Neurosci. 2021. 15: 645584.Zhao N., Liu C.C., Qiao W., Bu G. Apolipoprotein E, Receptors, and Modulation of Alzheimer’s Disease. Biol. Psychiatry 2018. 83: 347–357.Zhu Y., Le Peng J.H., Chen Y., Chen F. Current anti-Alzheimer’s disease effect of natural products and their principal targets, J. Integr. Neurosci. 2019. 18: 327e339.Zhuang Q.S., Zheng H., Gu X.D., Shen L., Ji H.F. Detecting the genetic link between Alzheimer’s disease and obesity using bioinformatics analysis of GWAS data. Oncotarget 2017. 8: 55915–55919.Yang Q., Song D., Qing H. Neural changes in alzheimer’s disease from circuit to molecule: Perspective of optogenetics. Neurosci. Biobehav. Rev. 2017. 79: 110–118.Yang T., Li S., Xu H., Walsh D.M., Selkoe D.J. Large soluble oligomers of amyloid beta-protein from Alzheimer brain are far less neuroactive than the smaller oligomers to which they dissociate. J. Neurosci. 2017. 37: 152–163.Yang Q., Song D., Qing H. Neural changes in Аlzheimer’s disease from circuit to molecule: Perspective of optogenetics. Neurosci. Biobehav. Rev. 2017. 79: 110–118.Ypsilanti A.R., Girao da Cruz M.T., Burgess A., Aubert I. The length of hippocampal cholinergic fibers is reduced in the aging brain. Neurobiol. Aging 2008. 29: 1666e1679.Yuki D., Sugiura Y., Zaima N., Akatsu H., Takei S., Yao I., Maesako M., Kinoshita A., Yamamoto T., Kon R., Sugiyama K., Setou M. DHA-PC and PSD-95 decrease after loss of synaptophysin and before neuronal loss in patients with alzheimer’s disease. Sci. Rep. 2014. 4: 7130.