Advertisement

Altered functional connectivity associated with cognitive impairment in neuromyelitis optica spectrum disorder

  • Author Footnotes
    1 These authors contributed equally to this work.
    Yang Yang
    Footnotes
    1 These authors contributed equally to this work.
    Affiliations
    Department of Radiology, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215000, China
    Search for articles by this author
  • Author Footnotes
    1 These authors contributed equally to this work.
    Qianyun Rui
    Footnotes
    1 These authors contributed equally to this work.
    Affiliations
    Department of Neurology, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215000, China
    Search for articles by this author
  • Xiaojuan Wu
    Affiliations
    Department of Radiology, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215000, China
    Search for articles by this author
  • Xiang Chen
    Affiliations
    Department of Radiology, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215000, China
    Search for articles by this author
  • Shuting Han
    Affiliations
    Department of Radiology, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215000, China
    Search for articles by this author
  • Yan Yang
    Affiliations
    Department of Neurology, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215000, China
    Search for articles by this author
  • Xiaoyuan Wang
    Affiliations
    Department of Neurology, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215000, China
    Search for articles by this author
  • Peng Wu
    Affiliations
    Philips Healthcare, Shanghai 200072, China
    Search for articles by this author
  • Hui Dai
    Correspondence
    Corresponding authors at: Department of Radiology, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215000, China.
    Affiliations
    Department of Radiology, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215000, China

    Institute of Medical Imaging, Soochow University, Suzhou 215000, China
    Search for articles by this author
  • Qun Xue
    Correspondence
    Corresponding authors at: Department of Neurology, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215000, China.
    Affiliations
    Department of Neurology, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215000, China

    Clinical Research Center of Neurology, Jiangsu Institute of Clinical Immunology, The First Affiliated Hospital of Soochow University, Suzhou 215000, China
    Search for articles by this author
  • Yonggang Li
    Correspondence
    Corresponding authors at: Department of Radiology, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215000, China.
    Affiliations
    Department of Radiology, The First Affiliated Hospital of Soochow University, Suzhou, Jiangsu 215000, China

    Institute of Medical Imaging, Soochow University, Suzhou 215000, China

    National Clinical Research Center for Hematologic Diseases, The First Affiliated Hospital of Soochow University, Suzhou 215000, China
    Search for articles by this author
  • Author Footnotes
    1 These authors contributed equally to this work.
Published:August 13, 2022DOI:https://doi.org/10.1016/j.msard.2022.104113

      Highlights

      • Several connectivity were decreased in cognitively impaired patients with NMOSD.
      • Decreased connectivity were associated with worse cognitive performance.
      • Intranetwork connectivity in the pDMN were decreased in cognitively impaired patients.
      • Internetwork connectivity between SN and pDMN/rFPN were decreased in cognitively impaired patients.

      Abstract

      Background

      Cognitive impairment is one of the common symptoms in patients with neuromyelitis optica spectrum disorder (NMOSD). However, the underlying mechanism remains unclear. Resting-state functional magnetic resonance imaging (rs-fMRI) offers the opportunity to reveal the patterns of brain activity in patients with different cognitive states. Accordingly, this study investigated functional connectivity (FC) abnormalities within and between the main cognitive networks in cognitively impaired (CI) patients with NMOSD and their correlations with cognitive performance.

      Methods

      Thirty-four patients with NMOSD and 39 healthy controls (HC) were included. Neuropsychological evaluations and rs-fMRI scanning were performed. Patients were classified as CI (n = 16) or cognitively preserved (CP; n = 18) according to neuropsychological evaluations. Seven components representing six main cognitive networks were selected by group independent component analysis. The differences in inter- and intranetwork FC among CI, CP, and HC groups were assessed. The correlation between FC values and neuropsychological data in NMOSD was calculated.

      Results

      The CI group showed decreased intranetwork connectivity in the posterior default mode network (pDMN) compared with the HC group (P < 0.05, GRF corrected), and decreased internetwork connectivity between the salience network (SN) and pDMN, and between the SN and right frontoparietal network (rFPN) compared with CP and HC groups. The altered FC values were significantly correlated with cognitive performance in the whole NMOSD group.

      Conclusion

      The disconnection within the pDMN and between the SN and pDMN or rFPN might suggest the neural substrates underlying cognitive impairment in NMOSD.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Multiple Sclerosis and Related Disorders
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Allen E.A.
        • Damaraju E.
        • Plis S.M.
        • Erhardt E.B.
        • Eichele T.
        • Calhoun V.D.
        Tracking whole-brain connectivity dynamics in the resting state.
        Cereb. Cortex. 2014; 24: 663-676https://doi.org/10.1093/cercor/bhs352
        • Blanc F.
        • Noblet V.
        • Jung B.
        • Rousseau F.
        • Renard F.
        • Bourre B.
        • Longato N.
        • Cremel N.
        • Di Bitonto L.
        • Kleitz C.
        • Collongues N.
        • Foucher J.
        • Kremer S.
        • Armspach J.P.
        • de Seze J.
        White matter atrophy and cognitive dysfunctions in neuromyelitis optica.
        PLoS One. 2012; 7: e33878https://doi.org/10.1371/journal.pone.0033878
        • Buckner R.L.
        • Andrews-Hanna J.R.
        • Schacter D.L.
        The brain's default network: anatomy, function, and relevance to disease.
        Ann. N. Y. Acad. Sci. 2008; 1124: 1-38https://doi.org/10.1196/annals.1440.011
        • Cai H.
        • Wang C.
        • Qian Y.
        • Zhang S.
        • Zhang C.
        • Zhao W.
        • Zhang T.
        • Zhang B.
        • Chen J.
        • Liu S.
        • Zhu J.
        • Yu Y.
        Large-scale functional network connectivity mediate the associations of gut microbiota with sleep quality and executive functions.
        Hum. Brain Mapp. 2021; 42: 3088-3101https://doi.org/10.1002/hbm.25419
        • Calhoun V.D.
        • Adali T.
        • Pearlson G.D.
        • Pekar J.J.
        Spatial and temporal independent component analysis of functional MRI data containing a pair of task-related waveforms.
        Hum. Brain Mapp. 2001; 13: 43-53https://doi.org/10.1002/hbm.1024
        • Camera V.
        • Messina S.
        • Elhadd K.T.
        • Sanpera-Iglesias J.
        • Mariano R.
        • Hacohen Y.
        • Dobson R.
        • Meletti S.
        • Wassmer E.
        • Lim M.J.
        • Huda S.
        • Hemingway C.
        • Leite M.I.
        • Ramdas S.
        • Palace J.
        Early predictors of disability of paediatric-onset AQP4-IgG-seropositive neuromyelitis optica spectrum disorders.
        J. Neurol. Neurosurg. Psychiatry. 2022; 93: 101-111https://doi.org/10.1136/jnnp-2021-327206
        • Chao-Gan Y.
        • Yu-Feng Z.
        DPARSF: A MATLAB toolbox for "pipeline" data analysis of resting-state fMRI.
        Front. Syst. Neurosci. 2010; 4https://doi.org/10.3389/fnsys.2010.00013
        • Chen Q.
        • Lv H.
        • Wang Z.
        • Wei X.
        • Zhao P.
        • Yang Z.
        • Gong S.
        • Wang Z.
        Brain structural and functional reorganization in tinnitus patients without hearing loss after sound therapy: a preliminary longitudinal study.
        Front. Neurosci. 2021; 15573858https://doi.org/10.3389/fnins.2021.573858
        • Czarnecka D.
        • Oset M.
        • Karlinska I.
        • Stasiolek M.
        Cognitive impairment in NMOSD-More questions than answers.
        Brain Behav. 2020; 10: e01842https://doi.org/10.1002/brb3.1842
        • Fox M.D.
        • Snyder A.Z.
        • Vincent J.L.
        • Corbetta M.
        • Van Essen D.C.
        • Raichle M.E.
        The human brain is intrinsically organized into dynamic, anticorrelated functional networks.
        Proc. Natl. Acad. Sci. U. S. A. 2005; 102: 9673-9678https://doi.org/10.1073/pnas.0504136102
        • Hamilton M.
        A rating scale for depression.
        J. Neurol. Neurosurg. Psychiatry. 1960; 23: 56-62https://doi.org/10.1136/jnnp.23.1.56
        • Han Y.
        • Liu Y.
        • Zeng C.
        • Luo Q.
        • Xiong H.
        • Zhang X.
        • Li Y.
        Functional connectivity alterations in neuromyelitis optica spectrum disorder: correlation with disease duration and cognitive impairment.
        Clin. Neuroradiol. 2020; 30: 559-568https://doi.org/10.1007/s00062-019-00802-3
        • Jandric D.
        • Lipp I.
        • Paling D.
        • Rog D.
        • Castellazzi G.
        • Haroon H.
        • Parkes L.
        • Parker G.J.M.
        • Tomassini V.
        • Muhlert N.
        Mechanisms of network changes in cognitive impairment in multiple sclerosis.
        Neurology. 2021; 97: e1886-e1897https://doi.org/10.1212/WNL.0000000000012834
        • Kim S.H.
        • Park E.Y.
        • Park B.
        • Hyun J.W.
        • Park N.Y.
        • Joung A.
        • Lee S.H.
        • Kim H.J.
        Multimodal magnetic resonance imaging in relation to cognitive impairment in neuromyelitis optica spectrum disorder.
        Sci. Rep. 2017; 7: 9180https://doi.org/10.1038/s41598-017-08889-9
        • Leech R.
        • Sharp D.J.
        The role of the posterior cingulate cortex in cognition and disease.
        Brain. 2014; 137: 12-32https://doi.org/10.1093/brain/awt162
        • Lerman C.
        • Gu H.
        • Loughead J.
        • Ruparel K.
        • Yang Y.
        • Stein E.A.
        Large-scale brain network coupling predicts acute nicotine abstinence effects on craving and cognitive function.
        JAMA Psychiatry. 2014; 71: 523-530https://doi.org/10.1001/jamapsychiatry.2013.4091
        • Liu Y.
        • Fu Y.
        • Schoonheim M.M.
        • Zhang N.
        • Fan M.
        • Su L.
        • Shen Y.
        • Yan Y.
        • Yang L.
        • Wang Q.
        • Zhang N.
        • Yu C.
        • Barkhof F.
        • Shi F.D.
        Structural MRI substrates of cognitive impairment in neuromyelitis optica.
        Neurology. 2015; 85: 1491-1499https://doi.org/10.1212/wnl.0000000000002067
        • Lucas J.A.
        • Ivnik R.J.
        • Smith G.E.
        • Ferman T.J.
        • Willis F.B.
        • Petersen R.C.
        • Graff-Radford N.R.
        Mayo's Older African Americans normative studies: norms for Boston Naming Test, controlled oral word association, category fluency, animal naming, token test, WRAT-3 reading, trail making test, stroop test, and judgment of line orientation.
        Clin. Neuropsychol. 2005; 19: 243-269https://doi.org/10.1080/13854040590945337
        • Mantini D.
        • Perrucci M.G.
        • Del Gratta C.
        • Romani G.L.
        • Corbetta M.
        Electrophysiological signatures of resting state networks in the human brain.
        Proc. Natl. Acad. Sci. U. S. A. 2007; 104: 13170-13175https://doi.org/10.1073/pnas.0700668104
        • Menon V.
        Large-scale brain networks and psychopathology: a unifying triple network model.
        Trends Cogn. Sci. 2011; 15: 483-506https://doi.org/10.1016/j.tics.2011.08.003
        • Mueller S.
        • Costa A.
        • Keeser D.
        • Pogarell O.
        • Berman A.
        • Coates U.
        • Reiser M.F.
        • Riedel M.
        • Moller H.J.
        • Ettinger U.
        • Meindl T.
        The effects of methylphenidate on whole brain intrinsic functional connectivity.
        Hum. Brain Mapp. 2014; 35: 5379-5388https://doi.org/10.1002/hbm.22557
        • Oertel F.C.
        • Schliesseit J.
        • Brandt A.U.
        • Paul F.
        Cognitive impairment in neuromyelitis optica spectrum disorders: a review of clinical and neuroradiological features.
        Front Neurol. 2019; 10: 608https://doi.org/10.3389/fneur.2019.00608
        • Power J.D.
        • Cohen A.L.
        • Nelson S.M.
        • Wig G.S.
        • Barnes K.A.
        • Church J.A.
        • Vogel A.C.
        • Laumann T.O.
        • Miezin F.M.
        • Schlaggar B.L.
        • Petersen S.E.
        Functional network organization of the human brain.
        Neuron. 2011; 72: 665-678https://doi.org/10.1016/j.neuron.2011.09.006
        • Saczynski J.S.
        • Inouye S.K.
        • Guess J.
        • Jones R.N.
        • Fong T.G.
        • Nemeth E.
        • Hodara A.
        • Ngo L.
        • Marcantonio E.R.
        The montreal cognitive assessment: creating a crosswalk with the mini-mental state examination.
        J. Am. Geriatr. Soc. 2015; 63: 2370-2374https://doi.org/10.1111/jgs.13710
        • Saji E.
        • Arakawa M.
        • Yanagawa K.
        • Toyoshima Y.
        • Yokoseki A.
        • Okamoto K.
        • Otsuki M.
        • Akazawa K.
        • Kakita A.
        • Takahashi H.
        • Nishizawa M.
        • Kawachi I.
        Cognitive impairment and cortical degeneration in neuromyelitis optica.
        Ann. Neurol. 2013; 73: 65-76https://doi.org/10.1002/ana.23721
        • Savoldi F.
        • Rocca M.A.
        • Valsasina P.
        • Riccitelli G.C.
        • Mesaros S.
        • Drulovic J.
        • Radaelli M.
        • Filippi M.
        Functional brain connectivity abnormalities and cognitive deficits in neuromyelitis optica spectrum disorder.
        Mult. Scler. 2020; 26: 795-805https://doi.org/10.1177/1352458519845109
        • Sporns O.
        Network attributes for segregation and integration in the human brain.
        Curr. Opin. Neurobiol. 2013; 23: 162-171https://doi.org/10.1016/j.conb.2012.11.015
        • Steinberg B.A.
        • Bieliauskas L.A.
        • Smith G.E.
        • Ivnik R.J.
        Mayo's Older Americans Normative studies: age- and IQ-adjusted norms for the trail-making test, the stroop test, and MAE controlled oral word association test.
        Clin. Neuropsychol. 2005; 19: 329-377https://doi.org/10.1080/13854040590945210
        • Teng C.
        • Liu T.
        • Zhang N.
        • Zhong Y.
        • Wang C.
        Cognitive behavioral therapy may rehabilitate abnormally functional communication pattern among the triple-network in major depressive disorder: a follow-up study.
        J. Affect. Disord. 2022; 304: 28-39https://doi.org/10.1016/j.jad.2022.02.050
        • Thompson E.
        Hamilton rating scale for anxiety (HAM-A).
        Occup. Med. 2015; 65 (Lond): 601https://doi.org/10.1093/occmed/kqv054
        • Wingerchuk D.M.
        • Banwell B.
        • Bennett J.L.
        • Cabre P.
        • Carroll W.
        • Chitnis T.
        • de Seze J.
        • Fujihara K.
        • Greenberg B.
        • Jacob A.
        • Jarius S.
        • Lana-Peixoto M.
        • Levy M.
        • Simon J.H.
        • Tenembaum S.
        • Traboulsee A.L.
        • Waters P.
        • Wellik K.E.
        • Weinshenker B.G.
        • International Panel for, N.M.O.D.
        International consensus diagnostic criteria for neuromyelitis optica spectrum disorders.
        Neurology. 2015; 85: 177-189https://doi.org/10.1212/WNL.0000000000001729
        • Xin F.
        • Lei X.
        Competition between frontoparietal control and default networks supports social working memory and empathy.
        Soc. Cogn. Affect. Neurosci. 2015; 10: 1144-1152https://doi.org/10.1093/scan/nsu160
        • Yan C.G.
        • Wang X.D.
        • Zuo X.N.
        • Zang Y.F.
        DPABI: data processing & analysis for (resting-state) brain imaging.
        Neuroinformatics. 2016; 14: 339-351https://doi.org/10.1007/s12021-016-9299-4
        • Yang K.
        • Shen B.
        • Li D.K.
        • Wang Y.
        • Zhao J.
        • Zhao J.
        • Yu W.B.
        • Liu Z.Y.
        • Tang Y.L.
        • Liu F.T.
        • Yu H.
        • Wang J.
        • Guo Q.H.
        • Wu J.J.
        Cognitive characteristics in Chinese non-demented PD patients based on gender difference.
        Transl. Neurodegener. 2018; 7https://doi.org/10.1186/s40035-018-0120-1
        • Yang Y.
        • Rui Q.
        • Han S.
        • Wu X.
        • Wang X.
        • Wu P.
        • Shen Y.
        • Dai H.
        • Xue Q.
        • Li Y.
        Reduced GABA levels in the medial prefrontal cortex are associated with cognitive impairment in patients with NMOSD.
        Mult. Scler. Relat. Disord. 2022; 58103496https://doi.org/10.1016/j.msard.2022.103496
        • Zhang N.
        • Li Y.J.
        • Fu Y.
        • Shao J.H.
        • Luo L.L.
        • Yang L.
        • Shi F.D.
        • Liu Y.
        Cognitive impairment in Chinese neuromyelitis optica.
        Mult. Scler. 2015; 21: 1839-1846https://doi.org/10.1177/1352458515576982
        • Zhao Q.
        • Guo Q.
        • Li F.
        • Zhou Y.
        • Wang B.
        • Hong Z.
        The shape trail test: application of a new variant of the trail making test.
        PLoS One. 2013; 8: e57333https://doi.org/10.1371/journal.pone.0057333
        • Zheng Q.
        • Chen X.
        • Xie M.
        • Fu J.
        • Han Y.
        • Wang J.
        • Zeng C.
        • Li Y.
        Altered structural networks in neuromyelitis optica spectrum disorder related with cognition impairment and clinical features.
        Mult. Scler. Relat. Disord. 2021; 48102714https://doi.org/10.1016/j.msard.2020.102714
        • Zhou J.
        • Gennatas E.D.
        • Kramer J.H.
        • Miller B.L.
        • Seeley W.W.
        Predicting regional neurodegeneration from the healthy brain functional connectome.
        Neuron. 2012; 73: 1216-1227https://doi.org/10.1016/j.neuron.2012.03.004