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Review

Altered Synaptic Plasticity: Plausible Mechanisms Associated With Viral Infections

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 733-752 | Received 25 May 2023, Accepted 27 Jul 2023, Published online: 22 Aug 2023

References

  • Wouk J , RechenchoskiDZ, RodriguesBCD, RibelatoEV, Faccin-GalhardiLC. Viral infections and their relationship to neurological disorders. Arch. Virol., 166(3), 733–753 (2021).
  • Swanson PA , McGavernDB. Viral diseases of the central nervous system. Curr. Opin. Virol., 11, 44–54 (2015).
  • Luethy LN , EricksonAK, JesudhasanPR, IkizlerM, DermodyTS, PfeifferJK. Comparison of three neurotropic viruses reveals differences in viral dissemination to the central nervous system. Virology, 487, 1–10 (2016).
  • Moses AV , BloomFE, PauzaCD, NelsonJA. Human immunodeficiency virus infection of human brain capillary endothelial cells occurs via a CD4/galactosylceramide-independent mechanism. Proc. Natl Acad. Sci., 90(22), 10474–10478 (1993).
  • Verma S , LoY, ChapagainMet al. West Nile virus infection modulates human brain microvascular endothelial cells tight junction proteins and cell adhesion molecules: transmigration across the in vitro blood-brain barrier. Virology, 385(2), 425–433 (2009).
  • Koyuncu OO , HogueIB, EnquistLW. Virus infections in the nervous system. Cell Host Microbe, 13(4), 379–393 (2013).
  • Challoner PB , SmithKT, ParkerJDet al. Plaque-associated expression of human herpesvirus 6 in multiple sclerosis. Proc. Natl Acad. Sci., 92(16), 7440–7444 (1995).
  • Jamieson GA , MaitlandNJ, WilcockGK, YatesCM, ItzhakiRF. Herpes simplex virus type 1 DNA is present in specific regions of brain from aged people with and without senile dementia of the Alzheimer type. J. Pathol., 167(4), 365–368 (1992).
  • Lin W-Y , LinM-S, WengY-Het al. Association of antiviral therapy with risk of Parkinson Disease in patients with chronic hepatitis C virus infection. JAMA Neurol., 76(9), 1019 (2019).
  • Morris RG , AndersonE, LynchGS, BaudryM. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature, 319(6056), 774–776 (1986).
  • Dorcet G , BenaiteauM, BostCet al. Two cases of late-onset anti-NMDAr auto-immune encephalitis after herpes simplex virus 1 encephalitis. Front. Neurol., 11, 38 (2020).
  • Nadim F , BucherD. Neuromodulation of neurons and synapses. Curr. Opin. Neurobiol., 29, 48–56 (2014).
  • Dando SJ , Mackay-SimA, NortonRet al. Pathogens penetrating the central nervous system: infection pathways and the cellular and molecular mechanisms of invasion. Clin. Microbiol. Rev., 27(4), 691–726 (2014).
  • Richter JD , KlannE. Making synaptic plasticity and memory last: mechanisms of translational regulation. Genes Dev., 23(1), 1–11 (2009).
  • Dittman JS , KreitzerAC, RegehrWG. Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J. Neurosci., 20(4), 1374–1385 (2000).
  • Varela JA , SenK, GibsonJ, FostJ, AbbottLF, NelsonSB. A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex. J. Neurosci., 17(20), 7926–7940 (1997).
  • Regehr WG , TankDW. The maintenance of LTP at hippocampal mossy fiber synapses is independent of sustained presynaptic calcium. Neuron, 7(3), 451–459 (1991).
  • Whitlock JR , HeynenAJ, ShulerMG, BearMF. Learning induces long-term potentiation in the hippocampus. Science, 313(5790), 1093–1097 (2006).
  • Hebb DO . The Organization of Behavior. (0 Edition). Psychology Press (2005).
  • Abraham WC , BearMF. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci., 19(4), 126–130 (1996).
  • Turrigiano GG , NelsonSB. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci., 5(2), 97–107 (2004).
  • Burrone J , O’ByrneM, MurthyVN. Multiple forms of synaptic plasticity triggered by selective suppression of activity in individual neurons. Nature, 420(6914), 414–418 (2002).
  • Abraham WC . Metaplasticity: tuning synapses and networks for plasticity. Nat. Rev. Neurosci., 9(5), 387 (2008).
  • Paulsen O . Natural patterns of activity and long-term synaptic plasticity. Curr. Opin. Neurobiol., 10(2), 172–180 (2000).
  • Watt AJ , SjöströmPJ, HäusserM, NelsonSB, TurrigianoGG. A proportional but slower NMDA potentiation follows AMPA potentiation in LTP. Nat. Neurosci., 7(5), 518–524 (2004).
  • Hayashi Y , ShiS-H, EstebanJA, PicciniA, PoncerJ-C, MalinowR. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science, 287(5461), 2262–2267 (2000).
  • Chen LW , YungKK, ChanYS. Co-localization of NMDA receptors and AMPA receptors in neurons of the vestibular nuclei of rats. Brain Res., 884(1–2), 87–97 (2000).
  • Götz T , KraushaarU, GeigerJ, LübkeJ, BergerT, JonasP. Functional properties of AMPA and NMDA receptors expressed in identified types of basal ganglia neurons. J. Neurosci., 17(1), 204–215 (1997).
  • Beneyto M , Meador-WoodruffJH. Expression of transcripts encoding AMPA receptor subunits and associated postsynaptic proteins in the macaque brain. J. Comp. Neurol., 468(4), 530–554 (2004).
  • Groc L , HeineM, CognetLet al. Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors. Nat. Neurosci., 7(7), 695–696 (2004).
  • Goebel DJ , PooschMS. NMDA receptor subunit gene expression in the rat brain: a quantitative analysis of endogenous mRNA levels of NR1Com, NR2A, NR2B, NR2C, NR2D and NR3A. Mol. Brain Res., 69(2), 164–170 (1999).
  • Bayer KU , LeBelÉ, McDonaldGL, O’LearyH, SchulmanH, DeKoninck P. Transition from reversible to persistent binding of CaMKII to postsynaptic sites and NR2B. J. Neurosci., 26(4), 1164–1174 (2006).
  • Jahr CE , StevensCF. Calcium permeability of the N-methyl-D-aspartate receptor channel in hippocampal neurons in culture. Proc. Natl Acad. Sci., 90(24), 11573–11577 (1993).
  • Daniels BP , HolmanDW, Cruz-OrengoL, JujjavarapuH, DurrantDM, KleinRS. Viral pathogen-associated molecular patterns regulate blood–brain barrier integrity via competing innate cytokine signals. mBio, 5(5), e01476–14 (2014).
  • Abdullahi AM , SarmastST, SinghR. Molecular Biology and epidemiology of neurotropic viruses. Cureus, 12(8), e9674 (2020).
  • Johnson RT . Acute Encephalitis. Clin. Infect. Dis., 23(2), 219–226 (1996).
  • Marttila RJ , RinneUK. Herpes simplex virus antibodies in patients with Parkinson’s disease. J. Neurol. Sci., 35(2–3), 375–379 (1978).
  • Vlajinac H , DzoljicE, MaksimovicJ, MarinkovicJ, SipeticS, KosticV. Infections as a risk factor for Parkinson’s disease: a case–control study. Int. J. Neurosci., 123(5), 329–332 (2013).
  • Langer-Gould A , WuJ, LucasRet al. Epstein-Barr virus, cytomegalovirus, and multiple sclerosis susceptibility: a multiethnic study. Neurology, 89(13), 1330–1337 (2017).
  • Jakhmola S , SkMF, ChatterjeeA, JainK, KarP, JhaHC. A plausible contributor to multiple sclerosis; presentation of antigenic myelin protein epitopes by major histocompatibility complexes. Comput. Biol. Med., 148, DOI: 10.1016/j.compbiomed.2022.105856 (2022).
  • Wandinger K-P , JabsW, SiekhausAet al. Association between clinical disease activity and Epstein–Barr virus reactivation in MS. Neurology, 55(2), 178–184 (2000).
  • Bergström T . Herpesviruses—a rationale for antiviral treatment in multiple sclerosis. Antiviral Res., 41(1), 1–19 (1999).
  • Manouchehrinia A , TanasescuR, KareemHet al. Prevalence of a history of prior varicella/herpes zoster infection in multiple sclerosis. J. Neurovirol., 23(6), 839–844 (2017).
  • Akanuma H , UenoS, TanakaS, MatsudaN, KanaiK. Mollaret Meningitis Caused by Varicella-Zoster Virus: A Case Report. Cureus, 14(11), e31834 (2022).
  • Gelman BB , LisinicchiaJG, ChenTet al. Prefrontal dopaminergic and enkephalinergic synaptic accommodation in HIV-associated neurocognitive disorders and encephalitis. J. Neuroimmune Pharmacol., 7(3), 686–700 (2012).
  • Verma A , BergerJR. ALS syndrome in patients with HIV-1 infection. J. Neurol. Sci., 240(1–2), 59–64 (2006).
  • Andersen O , LygnerP-E, BergströmT, AnderssonM, VablneA. Viral infections trigger multiple sclerosis relapses: a prospective seroepidemiological study. J. Neurol., 240(7), 417–422 (1993).
  • Patel DC , WallisG, DahleEJet al. Hippocampal TNFα signaling contributes to seizure generation in an infection-induced mouse model of limbic epilepsy. eneuro, 4(2), DOI: 10.1523/ENEURO.0105-17.2017 (2017).
  • Theodore WH , EpsteinL, GaillardWD, ShinnarS, WainwrightMS, JacobsonS. Human herpes virus 6B: a possible role in epilepsy?Epilepsia, 49(11), 1828–1837 (2008).
  • Beatman EL , MasseyA, ShivesKDet al. Alpha-Synuclein Expression Restricts RNA Viral Infections in the Brain. J. Virol., 90(6), 2767–2782 (2016).
  • Chen J , TsaiV, ParkerWE, AronicaE, BaybisM, CrinoPB. Detection of human papillomavirus in human focal cortical dysplasia type IIB. Ann. Neurol., 72(6), 881–892 (2012).
  • Wickersham IR , FinkeS, ConzelmannK-K, CallawayEM. Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat. Methods, 4(1), 47–49 (2007).
  • Dhingra V , LiX, LiuY, FuZF. Proteomic profiling reveals that rabies virus infection results in differential expression of host proteins involved in ion homeostasis and synaptic physiology in the central nervous system. J. Neurovirol., 13(2), 107–117 (2007).
  • Song Y , HouJ, QiaoBet al. Street rabies virus causes dendritic injury and F-actin depolymerization in the hippocampus. J. Gen. Virol., 94(2), 276–283 (2013).
  • Crick J , BrownF. An interfering component of rabies virus which contains RNA. J. Gen. Virol., 22(1), 147–151 (1974).
  • van den Pol AN . Polio, still lurking in the shadows. J. Neurosci., 33(3), 855–862 (2013).
  • Siva Venkatesh IP , BhaskarM, BasuA. Japanese encephalitis viral infection modulates proinflammatory cyto/chemokine profile in primary astrocyte and cell line of astrocytic origin. Metab. Brain Dis., 37(5), 1487–1502 (2022).
  • Ghoshal A , DasS, GhoshSet al. Proinflammatory mediators released by activated microglia induces neuronal death in Japanese encephalitis. Glia, 55(5), 483–496 (2007).
  • Jurgens HA , AmancherlaK, JohnsonRW. Influenza infection induces neuroinflammation, alters hippocampal neuron morphology, and impairs cognition in adult mice. J. Neurosci., 32(12), 3958–3968 (2012).
  • Becker JH , LinJJ, DoernbergMet al. Assessment of cognitive function in patients after COVID-19 infection. JAMA Netw. Open, 4(10), e2130645 (2021).
  • Samudyata , OliveiraAO, MalwadeSet al. SARS-CoV-2 promotes microglial synapse elimination in human brain organoids. Mol. Psychiatry, 27(10), 3939–3950 (2022).
  • Schmidt C , FastK, GryschokNet al. Neuronal plasticity in patients with Herpes simplex encephalitis: functional brain MRI studies and neuropsychological testing during the acute stage and at follow-up. Aktuelle Neurol., 34(Suppl. 2), s–2007-988017 (2007).
  • Piacentini R , CivitelliL, RipoliCet al. HSV-1 promotes Ca2+-mediated APP phosphorylation and Aβ accumulation in rat cortical neurons. Neurobiol. Aging, 32(12), 2323.e13–2323.e26 (2011).
  • Gershon AA , ChenJ, DavisLet al. Latency of varicella zoster virus in dorsal root, cranial, and enteric ganglia in vaccinated children. Trans. Am. Clin. Climatol. Assoc., 123, 17–33; discussion 33–35 (2012).
  • Devlin ME , GildenDH, MahalingamR, DuelandAN, CohrsR. Peripheral blood mononuclear cells of the elderly contain varicella-zoster virus DNA. J. Infect. Dis., 165(4), 619–622 (1992).
  • Sinzger C , DigelM, JahnG. Cytomegalovirus Cell Tropism. In: Human Cytomegalovirus (Volume 325).ShenkTE, StinskiMF ( Eds). Springer, Berlin, Germany, 63–83 (2008).
  • Cheeran MC-J , JiangZ, HuS, NiHT, PalmquistJM, LokensgardJR. Cytomegalovirus infection and interferon-γ modulate major histocompatibility complex class I expression on neural stem cells. J. Neurovirol., 14(5), 437–447 (2008).
  • Lang HLE , JacobsenH, IkemizuSet al. A functional and structural basis for TCR cross-reactivity in multiple sclerosis. Nat. Immunol., 3(10), 940–943 (2002).
  • Lövheim H , OlssonJ, WeidungBet al. Interaction between cytomegalovirus and herpes simplex virus Type 1 associated with the risk of Alzheimer’s disease development. J. Alzheimers Dis., 61(3), 939–945 (2018).
  • Saurav S , TanwarJ, AhujaK, MotianiRK. Dysregulation of host cell calcium signaling during viral infections: emerging paradigm with high clinical relevance. Mol. Aspects Med., 81, DOI: 10.1016/j.mam.2021.101004 (2021).
  • Lannuzel A , LledoP-M, LamghitniaHO, VincentJ-D, TardieuM. HIV-1 Envelope Proteins gp120 and gp160 potentiate NMDA-induced [Ca2+]i increase, Alter [Ca2+]i homeostasis and induce neurotoxicity in human embryonic neurons. Eur. J. Neurosci., 7(11), 2285–2293 (1995).
  • Zhou Y , LiuJ, XiongH. HIV-1 glycoprotein 120 enhancement of n-methyl-d-aspartate NMDA receptor-mediated excitatory postsynaptic currents: implications for HIV-1-associated neural injury. J. Neuroimmune Pharmacol., 12(2), 314–326 (2017).
  • Ali F , GerhardDM, SweasyKet al. Ketamine disinhibits dendrites and enhances calcium signals in prefrontal dendritic spines. Nat. Commun., 11(1), 72 (2020).
  • Olmo IG , CarvalhoTG, CostaVVet al. Zika virus promotes neuronal cell death in a non-cell autonomous manner by triggering the release of neurotoxic factors. Front. Immunol., 8, 1016 (2017).
  • Sama DM , MohmmadAbdul H, FurmanJLet al. Inhibition of soluble tumor necrosis factor ameliorates synaptic alterations and Ca2+ dysregulation in aged rats. PLOS ONE, 7(5), e38170 (2012).
  • Adam-Vizi V , StarkovAA. Calcium and mitochondrial reactive oxygen species generation: how to read the facts. J. Alzheimers Dis., 20(Suppl. 2), S413–S426 (2010).
  • Kramer T , EnquistLW. Alphaherpesvirus infection disrupts mitochondrial transport in neurons. Cell Host Microbe, 11(5), 504–514 (2012).
  • Li Z , OkamotoK-I, HayashiY, ShengM. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell, 119(6), 873–887 (2004).
  • Delille HK , BonekampNA, SchraderM. Peroxisomes and disease – an overview. Int. J. Biomed. Sci. IJBS, 2(4), 308–314 (2006).
  • Berger J , DorningerF, Forss-PetterS, KunzeM. Peroxisomes in brain development and function. Biochim. Biophys. Acta BBA - Mol. Cell Res., 1863(5), 934–955 (2016).
  • Ferdinandusse S , DenisS, MooyerPAWet al. Clinical and biochemical spectrum of D-bifunctional protein deficiency. Ann. Neurol., 59(1), 92–104 (2006).
  • Sasabe J , SuzukiM, ImanishiN, AisoS. Activity of D-amino acid oxidase is widespread in the human central nervous system. Front. Synaptic Neurosci., 6, 14 (2014).
  • Abe Y , NishimuraY, NakamuraKet al. Peroxisome deficiency impairs BDNF signaling and memory. Front. Cell Dev. Biol., 8, DOI: 10.3389/fcell.2020.567017 (2020).
  • Cai W , YangT, LiuHet al. Peroxisome proliferator-activated receptor γ (PPARγ): a master gatekeeper in CNS injury and repair. Prog. Neurobiol., 163–164, 27–58 (2018).
  • Warden A , TruittJ, MerrimanMet al. Localization of PPAR isotypes in the adult mouse and human brain. Sci. Rep., 6(1), DOI: 10.1038/srep27618 (2016).
  • Kawahara M , KurodaY. Molecular mechanism of neurodegeneration induced by Alzheimer’s β-amyloid protein: channel formation and disruption of calcium homeostasis. Brain Res. Bull., 53(4), 389–397 (2000).
  • Yakunin E , MoserA, LoebVet al. α-Synuclein abnormalities in mouse models of peroxisome biogenesis disorders. J. Neurosci. Res., 88(4), 866–876 (2010).
  • Santos MJ , QuintanillaRA, ToroAet al. Peroxisomal proliferation protects from β-Amyloid neurodegeneration. J. Biol. Chem., 280(49), 41057–41068 (2005).
  • Goodenowe DB , SenanayakeV. Relation of serum plasmalogens and APOE genotype to cognition and dementia in older persons in a cross-sectional study. Brain Sci., 9(4), 92 (2019).
  • Murtas G , CaldinelliL, CappellettiP, SacchiS, PollegioniL. Human d-amino acid oxidase: The inactive G183R variant. Biochim. Biophys. Acta BBA - Proteins Proteomics, 1866(7), 822–830 (2018).
  • Sargsyan Y , BickmeyerU, GibhardtCS, Streckfuss-BömekeK, BogeskiI, ThomsS. Peroxisomes contribute to intracellular calcium dynamics in cardiomyocytes and non-excitable cells. Life Sci. Alliance, 4(9), e202000987 (2021).
  • Bloodgood BL , GiesselAJ, SabatiniBL. Biphasic synaptic Ca influx arising from compartmentalized electrical signals in dendritic spines. PLoS Biol., 7(9), e1000190 (2009).
  • Hu D , SerranoF, OuryTD, KlannE. Aging-dependent alterations in synaptic plasticity and memory in mice that overexpress extracellular superoxide dismutase. J. Neurosci., 26(15), 3933–3941 (2006).
  • Fanelli F , SepeS, D’AmelioMet al. Age-dependent roles of peroxisomes in the hippocampus of a transgenic mouse model of Alzheimer’s disease. Mol. Neurodegener., 8(1), 8 (2013).
  • Dixit E , BoulantS, ZhangYet al. Peroxisomes are signaling platforms for antiviral innate immunity. Cell, 141(4), 668–681 (2010).
  • Cook KC , MorenoJA, JeanBeltran PM, CristeaIM. Peroxisome Plasticity at the Virus–Host Interface. Trends Microbiol., 27(11), 906–914 (2019).
  • Indari O , RaniA, BaralBet al. Modulation of peroxisomal compartment by Epstein-Barr virus. Microb. Pathog., 174, DOI: 10.1016/j.micpath.2022.105946 (2022).
  • Selkoe DJ . Alzheimer disease: mechanistic understanding predicts novel therapies. Ann. Intern. Med., 140(8), 627 (2004).
  • Zhao C , StrobinoK, MoonYPet al. APOE ε 4 modifies the relationship between infectious burden and poor cognition. Neurol. Genet., 6(4), e462 (2020).
  • Bojarski L , HermsJ, KuznickiJ. Calcium dysregulation in Alzheimer’s disease. Neurochem. Int., 52(4–5), 621–633 (2008).
  • Querfurth HW , SelkoeDJ. Calcium ionophore increases amyloid beta peptide production by cultured cells. Biochemistry, 33(15), 4550–4561 (1994).
  • Pierrot N , GhisdalP, CaumontA-S, OctaveJ-N. Intraneuronal amyloid-β1–42 production triggered by sustained increase of cytosolic calcium concentration induces neuronal death: calcium increase and intraneuronal Aβ1–42 production. J. Neurochem., 88(5), 1140–1150 (2004).
  • Snyder EM , NongY, AlmeidaCGet al. Regulation of NMDA receptor trafficking by amyloid-β. Nat. Neurosci., 8(8), 1051–1058 (2005).
  • Mucke L , MasliahE, YuG-Qet al. High-Level neuronal Expression of Aβ1–42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J. Neurosci., 20(11), 4050–4058 (2000).
  • Hong S , Beja-GlasserVF, NfonoyimBMet al. Complement and microglia mediate early synapse loss in Alzheimer mouse models. Science, 352(6286), 712–716 (2016).
  • Stephan BCM , HunterS, HarrisDet al. The neuropathological profile of mild cognitive impairment (MCI): a systematic review. Mol. Psychiatry, 17(11), 1056–1076 (2012).
  • Tzeng N-S , ChungC-H, LinF-Het al. Anti-herpetic Medications and Reduced Risk of Dementia in Patients with Herpes Simplex Virus Infections—a Nationwide, Population-Based Cohort Study in Taiwan. Neurotherapeutics, 15(2), 417–429 (2018).
  • Piacentini R , LiPuma DD, RipoliCet al. Herpes Simplex Virus type-1 infection induces synaptic dysfunction in cultured cortical neurons via GSK-3 activation and intraneuronal amyloid-β protein accumulation. Sci. Rep., 5(1), DOI: 10.1038/srep15444 (2015).
  • Piekut T , HurłaM, BanaszekNet al. Infectious agents and Alzheimer’s disease. J. Integr. Neurosci., 21(2), 073 (2022).
  • Sadasivan S , ZaninM, O’BrienK, Schultz-CherryS, SmeyneRJ. Induction of Microglia Activation after Infection with the Non-Neurotropic A/CA/04/2009 H1N1 Influenza Virus. PLOS ONE, 10(4), e0124047 (2015).
  • Dickerson F , StallingsC, SullensAet al. Association between cognitive functioning, exposure to Herpes Simplex Virus type 1, and the COMT Val158Met genetic polymorphism in adults without a psychiatric disorder. Brain Behav. Immun., 22(7), 1103–1107 (2008).
  • Jonker I , KleinHC, DuivisHE, YolkenRH, RosmalenJGM, SchoeversRA. Association between exposure to HSV1 and cognitive functioning in a general population of adolescents. The TRAILS study. PLOS ONE, 9(7), e101549 (2014).
  • Nimgaonkar VL , YolkenRH, WangTet al. Temporal cognitive decline associated with exposure to infectious agents in a population-based, aging cohort. Alzheimer Dis. Assoc. Disord., 30(3), 216–222 (2016).
  • Barnes LL , CapuanoAW, AielloAEet al. Cytomegalovirus infection and risk of Alzheimer Disease in older black and white individuals. J. Infect. Dis., 211(2), 230–237 (2015).
  • Streit WJ , BraakH, XueQ-S, BechmannI. Dystrophic (senescent) rather than activated microglial cells are associated with tau pathology and likely precede neurodegeneration in Alzheimer’s disease. Acta Neuropathol. (Berl.), 118(4), 475–485 (2009).
  • Warren-Gash C , ForbesHJ, WilliamsonEet al. Human herpesvirus infections and dementia or mild cognitive impairment: a systematic review and meta-analysis. Sci. Rep., 9(1), 4743 (2019).
  • Tiwari D , SrivastavaG, IndariO, TripathiV, SiddiqiMI, JhaHC. An in-silico insight into the predictive interaction of Apolipoprotein-E with Epstein-Barr virus proteins and their probable role in mediating Alzheimer’s disease. J. Biomol. Struct. Dyn.1–9 (2022).
  • Lupia T , MiliaMG, AtzoriCet al. Presence of Epstein–Barr virus DNA in cerebrospinal fluid is associated with greater HIV RNA and inflammation. AIDS, 34(3), 373–380 (2020).
  • Patra P , RaniA, SharmaN, MukherjeeC, JhaHC. Unraveling the connection of Epstein–Barr Virus and Its glycoprotein M146–157 peptide with neurological ailments. ACS Chem. Neurosci., 14(13), 2450–2460 (2023).
  • Zhang Z , ZhangS, FuPet al. Roles of glutamate receptors in Parkinson’s disease. Int. J. Mol. Sci., 20(18), 4391 (2019).
  • Tozzi A , SciaccalugaM, LoffredoVet al. Dopamine-dependent early synaptic and motor dysfunctions induced by α-synuclein in the nigrostriatal circuit. Brain, 144(11), 3477–3491 (2021).
  • Picconi B , CentonzeD, HåkanssonKet al. Loss of bidirectional striatal synaptic plasticity in L-DOPA–induced dyskinesia. Nat. Neurosci., 6(5), 501–506 (2003).
  • Sanchez-Catasus CA , BohnenNI, D’CruzN, MüllerMLTM. Striatal acetylcholine–dopamine imbalance in Parkinson Disease: in vivo neuroimaging study with dual-tracer PET and dopaminergic PET–informed correlational tractography. J. Nucl. Med., 63(3), 438–445 (2022).
  • Croisier E , MoranLB, DexterDT, PearceRK, GraeberMB. Microglial inflammation in the parkinsonian substantia nigra: relationship to alpha-synuclein deposition. J. Neuroinflammation, 2(1), 14 (2005).
  • Meisen WH , WohlebES, Jaime-RamirezACet al. The Impact of Macrophage- and Microglia-Secreted TNFα on Oncolytic HSV-1 Therapy in the Glioblastoma Tumor Microenvironment. Clin. Cancer Res., 21(14), 3274–3285 (2015).
  • Woulfe J , GrayMT, GaneshMS, MiddeldorpJM. Human serum antibodies against EBV latent membrane protein 1 cross-react with α-synuclein. Neurol. - Neuroimmunol. Neuroinflammation, 3(4), e239 (2016).
  • Olsen LK , DowdE, McKernanDP. A role for viral infections in Parkinson’s etiology?Neuronal Signal., 2(2), DOI: 10.1042/NS20170166 (2018).
  • Picconi B , PisaniA, BaroneIet al. Pathological Synaptic Plasticity in the Striatum: Implications for Parkinson’s Disease. Neurotoxicology, 26(5), 779–783 (2005).
  • Leta V , Rodríguez-ViolanteM, AbundesAet al. Parkinson’s disease and POST–COVID-19 syndrome: the Parkinson’s LONG-COVID spectrum. Mov. Disord., 36(6), 1287–1289 (2021).
  • Weissenborn K , EnnenJC, BokemeyerMet al. Monoaminergic neurotransmission is altered in hepatitis C virus infected patients with chronic fatigue and cognitive impairment. Gut, 55(11), 1624–1630 (2006).
  • Fletcher NF , WilsonGK, MurrayJet al. Hepatitis C virus infects the endothelial cells of the blood–brain barrier. Gastroenterology, 142(3), 634–643.e6 (2012).
  • Huang Y-Z , EdwardsMJ, RounisE, BhatiaKP, RothwellJC. Theta Burst Stimulation of the Human Motor Cortex. Neuron, 45(2), 201–206 (2005).
  • Amato MP , ZipoliV, PortaccioE. Cognitive changes in multiple sclerosis. Expert Rev. Neurother., 8(10), 1585–1596 (2008).
  • Nisticò R , MoriF, FeligioniM, NicolettiF, CentonzeD. Synaptic plasticity in multiple sclerosis and in experimental autoimmune encephalomyelitis. Philos. Trans. R. Soc. B Biol. Sci., 369(1633), DOI: 10.1098/rstb.2013.0162 (2014).
  • Errico F , NisticòR, NapolitanoFet al. Persistent increase of d-aspartate in d-aspartate oxidase mutant mice induces a precocious hippocampal age-dependent synaptic plasticity and spatial memory decay. Neurobiol. Aging, 32(11), 2061–2074 (2011).
  • Tang S-C , ArumugamTV, XuXet al. Pivotal role for neuronal Toll-like receptors in ischemic brain injury and functional deficits. Proc. Natl Acad. Sci., 104(34), 13798–13803 (2007).
  • Ma Y , LiJ, ChiuIet al. Toll-like receptor 8 functions as a negative regulator of neurite outgrowth and inducer of neuronal apoptosis. J. Cell Biol., 175(2), 209–215 (2006).
  • Rossi S , StuderV, MottaCet al. Inflammation inhibits GABA transmission in multiple sclerosis. Mult. Scler. J., 18(11), 1633–1635 (2012).
  • Monti G , GiovanniniG, MarudiAet al. Anti-NMDA receptor encephalitis presenting as new onset refractory status epilepticus in COVID-19. Seizure, 81, 18–20 (2020).
  • Dalmau J . NMDA receptor encephalitis and other antibody-mediated disorders of the synapse: The 2016 Cotzias Lecture. Neurology, 87(23), 2471–2482 (2016).
  • Lancaster E , LeypoldtF, TitulaerMJet al. Immunoglobulin G antibodies to the N-Methyl-D-aspartate receptor are distinct from immunoglobulin A and immunoglobulin M responses. Ann. Neurol., 77(1), 183 (2015).
  • Jackson AC , SenGuptaSK, SmithJF. Pathogenesis of Venezuelan equine encephalitis virus infection in mice and hamsters. Vet. Pathol., 28(5), 410–418 (1991).
  • Ma H , AlbeJR, GillilandTet al. Long-term persistence of viral RNA and inflammation in the CNS of macaques exposed to aerosolized Venezuelan equine encephalitis virus. PLOS Pathog., 18(6), e1009946 (2022).
  • Salimi H , CainMD, JiangXet al. Encephalitic alphaviruses exploit caveolae-mediated transcytosis at the blood-brain barrier for CNS entry. mBio., 11(1), e02731–19 (2020).
  • Ak AK , MendezMD. Herpes Simplex Encephalitis. In: StatPearls.StatPearls Publishing, FL, USA (2022).
  • Chen C-S , YaoY-C, LinS-Cet al. Retrograde Axonal Transport: a Major Transmission Route of Enterovirus 71 in Mice. J. Virol., 81(17), 8996–9003 (2007).
  • Fogarty MJ , MuEWH, LavidisNA, NoakesPG, BellinghamMC. Motor areas show altered dendritic structure in an amyotrophic lateral sclerosis mouse model. Front. Neurosci., 11, 609 (2017).
  • Fogarty MJ , MuEWH, NoakesPG, LavidisNA, BellinghamMC. Marked changes in dendritic structure and spine density precede significant neuronal death in vulnerable cortical pyramidal neuron populations in the SOD1G93A mouse model of amyotrophic lateral sclerosis. Acta Neuropathol. Commun., 4(1), 77 (2016).
  • Fogarty M . Amyotrophic lateral sclerosis as a synaptopathy. Neural Regen. Res., 14(2), 189 (2019).
  • Misra UK , TanCT, KalitaJ. Viral encephalitis and epilepsy. Epilepsia, 49, 13–18 (2008).
  • Fotheringham J , AkhyaniN, VortmeyerAet al. Detection of active human herpesvirus–6 Infection in the brain: correlation with polymerase chain reaction detection in cerebrospinal fluid. J. Infect. Dis., 195(3), 450–454 (2007).
  • Hashimoto T , VolkDW, EgganSMet al. Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J. Neurosci., 23(15), 6315–6326 (2003).
  • Kim JV , KangSS, DustinML, McGavernDB. Myelomonocytic cell recruitment causes fatal CNS vascular injury during acute viral meningitis. Nature, 457(7226), 191–195 (2009).
  • Wright WF , PintoCN, PalisocK, BaghliS. Viral (aseptic) meningitis: a review. J. Neurol. Sci., 398, 176–183 (2019).
  • Logan SAE , MacMahonE. Viral meningitis. BMJ, 336(7634), 36–40 (2008).
  • Mueller NH , GildenDH, CohrsRJ, MahalingamR, NagelMA. Varicella zoster virus infection: clinical features, molecular pathogenesis of disease, and latency. Neurol. Clin., 26(3), 675–697 (2008).
  • Kelly MJ , BenjaminLA, CartwrightKet al. Epstein–Barr virus coinfection in cerebrospinal fluid is associated with increased mortality in Malawian adults with bacterial meningitis. J. Infect. Dis., 205(1), 106–110 (2012).
  • Marshall C , ClarkZT, MincklerMR. Aseptic viral meningitis secondary to herpes simplex virus 2 genital infection. Cureus, 13(4), e14535 (2021).
  • Bergstrom T , LyckeE. Neuroinvasion by herpes simplex virus. An in vitro model for characterization of neurovirulent strains. J. Gen. Virol., 71(2), 405–410 (1990).
  • Forsgren M , SköldenbergB, AureliusE, GilleE. Neurologic morbidity after herpes simplex virus Type 2 meningitis: a retrospective study of 40 patients. Scand. J. Infect. Dis., 34(4), 278–283 (2002).
  • Drevets WC , ÖngürD, PriceJL. Neuroimaging abnormalities in the subgenual prefrontal cortex: implications for the pathophysiology of familial mood disorders. Mol. Psychiatry, 3(3), 220–226 (1998).
  • Alzheimer’s Disease Neuroimaging Initiative . TohkaJ, MoradiE, HuttunenH. Comparison of feature selection techniques in machine learning for anatomical brain MRI in dementia. Neuroinformatics, 14(3), 279–296 (2016).
  • Anazodo UC , FingerE, KwanBYMet al. Using simultaneous PET/MRI to compare the accuracy of diagnosing frontotemporal dementia by arterial spin labelling MRI and FDG-PET. NeuroImage Clin., 17, 405–414 (2018).
  • Rocher AB , ChaponF, BlaizotX, BaronJ-C, ChavoixC. Resting-state brain glucose utilization as measured by PET is directly related to regional synaptophysin levels: a study in baboons. Neuroimage, 20(3), 1894–1898 (2003).
  • Young PNE , EstarellasM, CoomansEet al. Imaging biomarkers in neurodegeneration: current and future practices. Alzheimers Res. Ther., 12(1), 49 (2020).
  • Jakhmola S , JhaHC. Reduce the risk of dementia; early diagnosis of Alzheimer’s disease. In: Machine Intelligence and Signal Analysis (Volume 748).TanveerM, PachoriRB ( Eds). Springer, Singapore, 621–632 (2019).
  • Gobbi LC , KnustH, KörnerMet al. Identification of three novel radiotracers for imaging aggregated tau in Alzheimer’s disease with positron emission tomography. J. Med. Chem., 60(17), 7350–7370 (2017).
  • Klunk WE , EnglerH, NordbergAet al. Imaging brain amyloid in Alzheimer’s disease with Pittsburgh Compound-B: Imaging Amyloid in AD with PIB. Ann. Neurol., 55(3), 306–319 (2004).
  • Finnema SJ , NabulsiNB, EidTet al. Imaging synaptic density in the living human brain. Sci. Transl. Med., 8(348), 348ra96 (2016).
  • Frisoni GB , PievaniM, TestaCet al. The topography of grey matter involvement in early and late onset Alzheimer’s disease. Brain, 130(3), 720–730 (2007).
  • Jack CR , DicksonDW, ParisiJEet al. Antemortem MRI findings correlate with hippocampal neuropathology in typical aging and dementia. Neurology, 58(5), 750–757 (2002).
  • Manelis A , PaynterCA, WheelerME, RederLM. Repetition related changes in activation and functional connectivity in hippocampus predict subsequent memory. Hippocampus, 23(1), 53–65 (2013).
  • Boucher S , ArribaratG, CartiauxBet al. Diffusion tensor imaging tractography of white matter tracts in the equine brain. Front. Vet. Sci., 7, 382 (2020).
  • Soares JM , MarquesP, AlvesV, SousaN. A hitchhiker’s guide to diffusion tensor imaging. Front. Neurosci., 7, (2013).
  • Wang Y , XuC, ParkJ-Het al. Diagnosis and prognosis of Alzheimer’s disease using brain morphometry and white matter connectomes. NeuroImage Clin., 23, DOI: 10.1016/j.nicl.2019.101859 (2019).
  • Neffati S , BenAbdellafou K, JaffelI, TaoualiO, BouzraraK. An improved machine learning technique based on downsized KPCA for Alzheimer’s disease classification. Int. J. Imaging Syst. Technol., 29(2), 121–131 (2019).
  • Carmo RLD , AlvesSimão AK, AmaralLLFDet al. Neuroimaging of emergent and reemergent infections. Radiographics, 39(6), 1649–1671 (2019).
  • Sanford R , AncesBM, MeyerhoffDJet al. Longitudinal trajectories of brain volume and cortical thickness in treated and untreated primary human immunodeficiency virus infection. Clin. Infect. Dis., 67(11), 1697–1704 (2018).
  • Noble DJ , ScoffingsD, AjithkumarT, WilliamsMV, JefferiesSJ. Fast imaging employing steady-state acquisition (FIESTA) MRI to investigate cerebrospinal fluid (CSF) within dural reflections of posterior fossa cranial nerves. Br. J. Radiol., 89(1067), DOI: 10.1259/bjr.20160392 (2016).
  • Ashburner J , FristonKJ. Voxel-based morphometry the methods. Neuroimage, 11(6), 805–821 (2000).
  • Collins DL , HolmesCJ, PetersTM, EvansAC. Automatic 3-D model-based neuroanatomical segmentation. Hum. Brain Mapp., 3(3), 190–208 (1995).
  • Järnum H , EskildsenSF, SteffensenEGet al. Longitudinal MRI study of cortical thickness, perfusion, and metabolite levels in major depressive disorder: longitudinal study of advanced MRI in depression. Acta Psychiatr. Scand., 124(6), 435–446 (2011).
  • Domingues RB , FinkMC, TsanaclisAMet al. Diagnosis of herpes simplex encephalitis by magnetic resonance imaging and polymerase chain reaction assay of cerebrospinal fluid. J. Neurol. Sci., 157(2), 148–153 (1998).
  • Baskin HJ , HedlundG. Neuroimaging of herpesvirus infections in children. Pediatr. Radiol., 37(10), 949 (2007).
  • Ali M , SafrielY, SohiJ, LlaveA, WeathersS. West Nile virus infection: MR imaging findings in the nervous system. AJNR Am. J. Neuroradiol., 26(2), 289–297 (2005).
  • Phukan P , SarmaK, SharmaBK, BoruahDK, GogoiBB, ChuunthangD. MRI spectrum of Japanese Encephalitis in Northeast India: a cross-sectional study. J. Neurosci. Rural Pract., 12, 281–289 (2021).
  • Matschke J , LütgehetmannM, HagelCet al. Neuropathology of patients with COVID-19 in Germany: a post-mortem case series. Lancet Neurol., 19(11), 919–929 (2020).
  • Douaud G , LeeS, Alfaro-AlmagroFet al. SARS-CoV-2 is associated with changes in brain structure in UK Biobank. Nature, 604(7907), 697–707 (2022).
  • Manca R , DeMarco M, IncePG, VenneriA. Heterogeneity in regional damage detected by neuroimaging and neuropathological studies in older adults with COVID-19: a cognitive-neuroscience systematic review to inform the long-term impact of the virus on neurocognitive trajectories. Front. Aging Neurosci., 13, DOI: 10.3389/fnagi.2021.646908 (2021).
  • Grasso D , CastoraniG, BorreggineC, SimeoneA, DeBlasi R. Cerebral amyloid angiopathy related inflammation: a little known but not to be underestimated disease. Radiol. Case Rep., 16(9), 2514–2521 (2021).
  • Tiwari D , JhaHC. Detection and Analysis of Human Brain Disorders. In: Machine Intelligence and Signal Analysis (Volume 748).TanveerM, PachoriRB ( Eds). Springer, Singapore, 717–726 (2019).
  • Hohenfeld C , WernerCJ, ReetzK. Resting-state connectivity in neurodegenerative disorders: is there potential for an imaging biomarker?NeuroImage Clin., 18, 849–870 (2018).

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