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• Investigation Reseach •
The functional connectivity of default mode network and hippocampus in Alzheimer's disease: A Meta-analysis based on SDM
LU Guanqin  ZHANG Shouzi  LI Rui 

Cite this article as: Lu GQ, Zhang SZ, Li R. The functional connectivity of default mode network and hippocampus in Alzheimer's disease: A Meta-analysis based on SDM[J]. Chin J Magn Reson Imaging, 2022, 13(3): 54-60. DOI:10.12015/issn.1674-8034.2022.03.011.


[Abstract] Objective Many researches have indicated that the default-mode network (DMN) and hippocampus were vulnerable to Alzheimer's disease (AD). However, the changes in resting-state functional connectivity (rsFC) patterns of the two systems vary across the progression of AD. We aimed to use meta analysis to explore rsFC changes of AD and mild cognitive impairment (MCI) based on the DMN and hippocampus as seeds.Materials and Methods A standardized meta analysis procedure was adopted to systematically review articles from PubMed and Web of Science. A total of 12 seed-based whole-brain voxel-wise rsFC studies were finally entered into meta analysis by using signed differential mapping (SDM).Results Compared with healthy controls (HC), we found AD show significantly decreased rsFC in the medial prefrontal cortex (MPFC) by using the hippocampus as the seed region. Using DMN regions as the seed, we found AD show decreased rsFC in the MPFC, rolandic operculum, hippocampus and parahippocampus; while MCI show decreased rsFC in right posterior cingulate cortex (PCC), also with increased connectivity in the right precentral gyrus.Conclusions Reduced rsFC between the hippocampus and MPFC of anterior DMN is an important imaging feature for AD, while MCI mostly impairs the connectivity of the PCC in the posterior DMN and shows compensatory enhancement in the precentral gyrus (sensorimotor area). The results clarified the different rsFC patterns of DMN and hippocampus alterations in AD and MCI, and provided imaging reference for the recognition of AD and the evaluation of intervention effect.
[Keywords] Alzheimer's disease；mild cognitive impairment；default-mode network；hippocampus；resting-state functional connectivity；Meta-analysis

LU Guanqin1, 2   ZHANG Shouzi3   LI Rui1, 2*  

1 CAS Key Laboratory of Mental Health, Institute of Psychology, Beijing 100101

2 Department of Psychology, University of Chinese Academy of Sciences, Beijing 100049

3 Beijing Geriatric Hospital, Beijing 100095

Li R, E-mail: lir@psych.ac.cn

Conflicts of interest   None.

ACKNOWLEDGMENTS National Natural Science Foundation of China (No. 61673374, 62177004).
Received  2021-11-08
Accepted  2022-02-18
DOI: 10.12015/issn.1674-8034.2022.03.011
Cite this article as: Lu GQ, Zhang SZ, Li R. The functional connectivity of default mode network and hippocampus in Alzheimer's disease: A Meta-analysis based on SDM[J]. Chin J Magn Reson Imaging, 2022, 13(3): 54-60. DOI:10.12015/issn.1674-8034.2022.03.011.

[1]
DeTure MA, Dickson DW. The neuropathological diagnosis of Alzheimer's disease[J]. Mol Neurodegener, 2019, 14(1): 32. DOI: 10.1186/s13024-019-0333-5.
[2]
Rasero J, Alonso-Montes C, Diez I, et al. Group-level progressive alterations in brain connectivity patterns revealed by diffusion-tensor brain networks across severity stages in Alzheimer's disease[J]. Front Aging Neurosci, 2017, 9: 215. DOI: 10.3389/fnagi.2017.00215.
[3]
Teipel S, Grothe MJ, Zhou J, et al. Measuring cortical connectivity in Alzheimer's disease as a brain neural network pathology: toward clinical applications[J]. J Int Neuropsychol Soc, 2016, 22(2): 138-163. DOI: 10.1017/S1355617715000995.
[4]
Jalilianhasanpour R, Beheshtian E, Sherbaf G, et al. Functional connectivity in neurodegenerative disorders: Alzheimer's disease and frontotemporal dementia[J]. Top Magn Reson Imaging, 2019, 28(6): 317-324. DOI: 10.1097/RMR.0000000000000223.
[5]
Watanabe H, Bagarinao E, Yokoi T, et al. Tau accumulation and network breakdown in Alzheimer's disease[J]. Adv Exp Med Biol, 2019, 1184: 231-240. DOI: 10.1007/978-981-32-9358-8_19.
[6]
Li R, Yu J, Zhang SZ, et al. Bayesian network analysis reveals alterations to default mode network connectivity in individuals at risk for Alzheimer's disease[J]. PLoS One, 2013, 8(12): e82104. DOI: 10.1371/journal.pone.0082104.
[7]
Zhong YF, Huang LY, Cai SP, et al. Altered effective connectivity patterns of the default mode network in Alzheimer's disease: an fMRI study[J]. Neurosci Lett, 2014, 578: 171-175. DOI: 10.1016/j.neulet.2014.06.043.
[8]
Greicius MD, Srivastava G, Reiss AL, et al. Default-mode network activity distinguishes Alzheimer's disease from healthy aging: evidence from functional MRI[J]. Proc Natl Acad Sci USA, 2004, 101(13): 4637-4642. DOI: 10.1073/pnas.0308627101.
[9]
Sohn WS, Yoo K, Na DL, et al. Progressive changes in hippocampal resting-state connectivity across cognitive impairment: a cross-sectional study from normal to Alzheimer disease[J]. Alzheimer Dis Assoc Disord, 2014, 28(3): 239-246. DOI: 10.1097/WAD.0000000000000027.
[10]
Xue JY, Guo H, Gao Y, et al. Altered directed functional connectivity of the Hippocampus in mild cognitive impairment and Alzheimer's disease: a resting-state fMRI study[J]. Front Aging Neurosci, 2019, 11: 326. DOI: 10.3389/fnagi.2019.00326.
[11]
Sullivan MD, Anderson JAE, Turner GR, et al. Intrinsic neurocognitive network connectivity differences between normal aging and mild cognitive impairment are associated with cognitive status and age[J]. Neurobiol Aging, 2019, 73: 219-228. DOI: 10.1016/j.neurobiolaging.2018.10.001.
[12]
Therriault J, Wang S, Mathotaarachchi S, et al. Rostral-caudal hippocampal functional convergence is reduced across the Alzheimer's disease spectrum[J]. Mol Neurobiol, 2019, 56(12): 8336-8344. DOI: 10.1007/s12035-019-01671-0.
[13]
Qi HH, Liu H, Hu HM, et al. Primary disruption of the memory-related subsystems of the default mode network in Alzheimer's disease: resting-state functional connectivity MRI study[J]. Front Aging Neurosci, 2018, 10: 344. DOI: 10.3389/fnagi.2018.00344.
[14]
Cai SP, Chong T, Peng YL, et al. Altered functional brain networks in amnestic mild cognitive impairment: a resting-state fMRI study[J]. Brain Imaging Behav, 2017, 11(3): 619-631. DOI: 10.1007/s11682-016-9539-0.
[15]
Tahmasian M, Pasquini L, Scherr M, et al. The lower hippocampus global connectivity, the higher its local metabolism in Alzheimer disease[J]. Neurology, 2015, 84(19): 1956-1963. DOI: 10.1212/WNL.0000000000001575.
[16]
Das SR, Pluta J, Mancuso L, et al. Anterior and posterior MTL networks in aging and MCI[J]. Neurobiol Aging, 2015, 36Suppl 1(0 1): S141-S150, S150.e1. DOI: 10.1016/j.neurobiolaging.2014.03.041.
[17]
Qi ZG, Wu X, Wang ZQ, et al. Impairment and compensation coexist in amnestic MCI default mode network[J]. Neuroimage, 2010, 50(1): 48-55. DOI: 10.1016/j.neuroimage.2009.12.025.
[18]
Gardini S, Venneri A, Sambataro F, et al. Increased functional connectivity in the default mode network in mild cognitive impairment: a maladaptive compensatory mechanism associated with poor semantic memory performance[J]. J Alzheimers Dis, 2015, 45(2): 457-470. DOI: 10.3233/JAD-142547.
[19]
Damoiseaux JS, Prater KE, Miller BL, et al. Functional connectivity tracks clinical deterioration in Alzheimer's disease[J]. Neurobiol Aging, 2012, 33(4): 828.e19-828.e30. DOI: 10.1016/j.neurobiolaging.2011.06.024.
[20]
Chiesa PA, Cavedo E, Lista S, et al. Revolution of resting-state functional neuroimaging genetics in Alzheimer's disease[J]. Trends Neurosci, 2017, 40(8): 469-480. DOI: 10.1016/j.tins.2017.06.002.
[21]
Ranganath C, Ritchey M. Two cortical systems for memory-guided behaviour[J]. Nat Rev Neurosci, 2012, 13(10): 713-726. DOI: 10.1038/nrn3338.
[22]
Zhuo JJ, Fan LZ, Liu Y, et al. Connectivity profiles reveal a transition subarea in the parahippocampal region that integrates the anterior temporal-posterior medial systems[J]. J Neurosci, 2016, 36(9): 2782-2795. DOI: 10.1523/JNEUROSCI.1975-15.2016.
[23]
Hughes RE, Nikolic K, Ramsay RR. One for all? hitting multiple Alzheimer's disease targets with one drug[J]. Front Neurosci, 2016, 10: 177. DOI: 10.3389/fnins.2016.00177.
[24]
Matthews PM, Hampshire A. Clinical concepts emerging from fMRI functional connectomics[J]. Neuron, 2016, 91(3): 511-528. DOI: 10.1016/j.neuron.2016.07.031.
[25]
Tam A, Dansereau C, Badhwar A, et al. Common effects of amnestic mild cognitive impairment on resting-state connectivity across four independent studies[J]. Front Aging Neurosci, 2015, 7: 242. DOI: 10.3389/fnagi.2015.00242.
[26]
Bellec P, Benhajali Y, Carbonell F, et al. Impact of the resolution of brain parcels on connectome-wide association studies in fMRI[J]. Neuroimage, 2015, 123: 212-228. DOI: 10.1016/j.neuroimage.2015.07.071.
[27]
Miller SL, Fenstermacher E, Bates J, et al. Hippocampal activation in adults with mild cognitive impairment predicts subsequent cognitive decline[J]. J Neurol Neurosurg Psychiatry, 2008, 79(6): 630-635. DOI: 10.1136/jnnp.2007.124149.
[28]
Xu P, Chen A, Li Y, et al. Medial prefrontal cortex in neurological diseases[J]. Physiol Genomics, 2019, 51(9): 432-442. DOI: 10.1152/physiolgenomics.00006.2019.
[29]
Hafkemeijer A, van der Grond J, Rombouts SA. Imaging the default mode network in aging and dementia[J]. Biochim Biophys Acta, 2012, 1822(3): 431-441. DOI: 10.1016/j.bbadis.2011.07.008.
[30]
Serra L, Cercignani M, Mastropasqua C, et al. Longitudinal changes in functional brain connectivity predicts conversion to Alzheimer's disease[J]. J Alzheimers Dis, 2016, 51(2): 377-389. DOI: 10.3233/JAD-150961.
[31]
Ibrahim B, Suppiah S, Ibrahim N, et al. Diagnostic power of resting-state fMRI for detection of network connectivity in Alzheimer's disease and mild cognitive impairment: a systematic review[J]. Hum Brain Mapp, 2021, 42(9): 2941-2968. DOI: 10.1002/hbm.25369.
[32]
Liang LY, Zhao LH, Wei YC, et al. Structural and functional hippocampal changes in subjective cognitive decline from the community[J]. Front Aging Neurosci, 2020, 12: 64. DOI: 10.3389/fnagi.2020.00064.
[33]
Wang Y, Risacher SL, West JD, et al. Altered default mode network connectivity in older adults with cognitive complaints and amnestic mild cognitive impairment[J]. J Alzheimers Dis, 2013, 35(4): 751-760. DOI: 10.3233/JAD-130080.
[34]
Wang XN, Sheng C, Han Y. Progress of biomarkers for subjective cognitive decline[J]. J Med Postgrad, 2015, 28(4): 423-426. DOI: 10.16571/j.cnki.1008-8199.2015.04.023.
[35]
Si T, Xing GQ, Han Y. Subjective cognitive decline and related cognitive deficits[J]. Front Neurol, 2020, 11: 247. DOI: 10.3389/fneur.2020.00247.
[36]
Xu XW, Li WK, Tao ML, et al. Effective and accurate diagnosis of subjective cognitive decline based on functional connection and graph theory view[J]. Front Neurosci, 2020, 14: 577887. DOI: 10.3389/fnins.2020.577887.
[37]
Eyler LT, Elman JA, Hatton SN, et al. Resting state abnormalities of the default mode network in mild cognitive impairment: a systematic review and meta-analysis[J]. J Alzheimers Dis, 2019, 70(1): 107-120. DOI: 10.3233/JAD-180847.
[38]
Badhwar A, Tam A, Dansereau C, et al. Resting-state network dysfunction in Alzheimer's disease: a systematic review and meta-analysis[J]. Alzheimers Dement (Amst), 2017, 8: 73-85. DOI: 10.1016/j.dadm.2017.03.007.
[39]
Hohenfeld C, Werner CJ, Reetz K. Resting-state connectivity in neurodegenerative disorders: is there potential for an imaging biomarker?[J]. Neuroimage Clin, 2018, 18: 849-870. DOI: 10.1016/j.nicl.2018.03.013.
[40]
Yeo BT, Krienen FM, Sepulcre J, et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity[J]. J Neurophysiol, 2011, 106(3): 1125-1165. DOI: 10.1152/jn.00338.2011.
[41]
Dillen KNH, Jacobs HIL, Kukolja J, et al. Aberrant functional connectivity differentiates retrosplenial cortex from posterior cingulate cortex in prodromal Alzheimer's disease[J]. Neurobiol Aging, 2016, 44: 114-126. DOI: 10.1016/j.neurobiolaging.2016.04.010.
[42]
Wang ZQ, Xia MR, Dai ZJ, et al. Differentially disrupted functional connectivity of the subregions of the inferior parietal lobule in Alzheimer's disease[J]. Brain Struct Funct, 2015, 220(2): 745-762. DOI: 10.1007/s00429-013-0681-9.
[43]
Soman SM, Raghavan S, Rajesh PG, et al. Does resting state functional connectivity differ between mild cognitive impairment and early Alzheimer's dementia?[J]. J Neurol Sci, 2020, 418: 117093. DOI: 10.1016/j.jns.2020.117093.
[44]
Gili T, Cercignani M, Serra L, et al. Regional brain atrophy and functional disconnection across Alzheimer's disease evolution[J]. J Neurol Neurosurg Psychiatry, 2011, 82(1): 58-66. DOI: 10.1136/jnnp.2009.199935.
[45]
Wang K, Liang M, Wang L, et al. Altered functional connectivity in early Alzheimer's disease: a resting-state fMRI study[J]. Hum Brain Mapp, 2007, 28(10): 967-978. DOI: 10.1002/hbm.20324.
[46]
Kim J, Kim YH, Lee JH. Hippocampus-precuneus functional connectivity as an early sign of Alzheimer's disease: a preliminary study using structural and functional magnetic resonance imaging data[J]. Brain Res, 2013, 1495: 18-29. DOI: 10.1016/j.brainres.2012.12.011.
[47]
Allen G, Barnard H, McColl R, et al. Reduced hippocampal functional connectivity in Alzheimer disease[J]. Arch Neurol, 2007, 64(10): 1482-1487. DOI: 10.1001/archneur.64.10.1482.
[48]
Kenny ER, Blamire AM, Firbank MJ, et al. Functional connectivity in cortical regions in dementia with Lewy bodies and Alzheimer's disease[J]. Brain, 2012, 135(Pt 2): 569-581. DOI: 10.1093/brain/awr327.
[49]
Wang L, Zang YF, He Y, et al. Changes in hippocampal connectivity in the early stages of Alzheimer's disease: evidence from resting state fMRI[J]. Neuroimage, 2006, 31(2): 496-504. DOI: 10.1016/j.neuroimage.2005.12.033.
[50]
Zhang YW, Zhao ZL, Qi ZG, et al. Local-to-remote cortical connectivity in amnestic mild cognitive impairment[J]. Neurobiol Aging, 2017, 56: 138-149. DOI: 10.1016/j.neurobiolaging.2017.04.016.
[51]
Cera N, Esposito R, Cieri F, et al. Altered cingulate cortex functional connectivity in normal aging and mild cognitive impairment[J]. Front Neurosci, 2019, 13: 857. DOI: 10.3389/fnins.2019.00857.
[52]
Han SD, Arfanakis K, Fleischman DA, et al. Functional connectivity variations in mild cognitive impairment: associations with cognitive function[J]. J Int Neuropsychol Soc, 2012, 18(1): 39-48. DOI: 10.1017/S1355617711001299.
[53]
Jobson DD, Hase Y, Clarkson AN, et al. The role of the medial prefrontal cortex in cognition, ageing and dementia[J]. Brain Commun, 2021, 3(3): fcab125. DOI: 10.1093/braincomms/fcab125.
[54]
Josef Golubic S, Aine CJ, Stephen JM, et al. MEG biomarker of Alzheimer's disease: absence of a prefrontal generator during auditory sensory gating[J]. Hum Brain Mapp, 2017, 38(10): 5180-5194. DOI: 10.1002/hbm.23724.
[55]
Li R, Zhang J, Wu X, et al. Brain-wide resting-state connectivity regulation by the hippocampus and medial prefrontal cortex is associated with fluid intelligence[J]. Brain Struct Funct, 2020, 225(5): 1587-1600. DOI: 10.1007/s00429-020-02077-8.
[56]
Preston AR, Eichenbaum H. Interplay of hippocampus and prefrontal cortex in memory[J]. Curr Biol, 2013, 23(17): R764-R773. DOI: 10.1016/j.cub.2013.05.041.
[57]
Mitra A, Snyder AZ, Hacker CD, et al. Human cortical-hippocampal dialogue in wake and slow-wave sleep[J]. Proc Natl Acad Sci USA, 2016, 113(44): E6868-E6876. DOI: 10.1073/pnas.1607289113.
[58]
Li WK, Xu XW, Wang ZX, et al. Multiple connection pattern combination from single-mode data for mild cognitive impairment identification[J]. Front Cell Dev Biol, 2021, 9: 782727. DOI: 10.3389/fcell.2021.782727.
[59]
Yıldırım E, Soncu Büyükişcan E. Default mode network connectivity in alzheimers disease[J]. Turk Psikiyatri Derg, 2019, 30(4): 279-286.
[60]
Braak H, Braak E. Neuropathological stageing of alzheimer-related changes[J]. Acta Neuropathol, 1991, 82(4): 239-259. DOI: 10.1007/BF00308809.
[61]
Ziontz J, Adams JN, Harrison TM, et al. Hippocampal connectivity with retrosplenial cortex is linked to neocortical tau accumulation and memory function[J]. J Neurosci, 2021, 41(42): 8839-8847. DOI: 10.1523/JNEUROSCI.0990-21.2021.
[62]
Hoenig MC, Bischof GN, Seemiller J, et al. Networks of tau distribution in Alzheimer's disease[J]. Brain, 2018, 141(2): 568-581. DOI: 10.1093/brain/awx353.
[63]
Li XZ, Li TQ, Andreasen N, et al. Ratio of Aβ42/P-tau181p in CSF is associated with aberrant default mode network in AD[J]. Sci Rep, 2013, 3: 1339. DOI: 10.1038/srep01339.
[64]
Wang L, Brier MR, Snyder AZ, et al. Cerebrospinal fluid Aβ42, phosphorylated Tau181, and resting-state functional connectivity[J]. JAMA Neurol, 2013, 70(10): 1242-1248. DOI: 10.1001/jamaneurol.2013.3253.
[65]
Schultz AP, Chhatwal JP, Hedden T, et al. Phases of hyperconnectivity and hypoconnectivity in the default mode and salience networks track with amyloid and tau in clinically normal individuals[J]. J Neurosci, 2017, 37(16): 4323-4331. DOI: 10.1523/JNEUROSCI.3263-16.2017.
[66]
Jones DT, Graff-Radford J, Lowe VJ, et al. Tau, amyloid, and cascading network failure across the Alzheimer's disease spectrum[J]. Cortex, 2017, 97: 143-159. DOI: 10.1016/j.cortex.2017.09.018.
[67]
Zhao T, Quan MN, Jia JP. Functional connectivity of default mode network subsystems in the presymptomatic stage of autosomal dominant Alzheimer's disease[J]. J Alzheimers Dis, 2020, 73(4): 1435-1444. DOI: 10.3233/JAD-191065.
[68]
Wang SM, Kim NY, Kang DW, et al. A comparative study on the predictive value of different resting-state functional magnetic resonance imaging parameters in preclinical Alzheimer's disease[J]. Front Psychiatry, 2021, 12: 626332. DOI: 10.3389/fpsyt.2021.626332.
[69]
Ge XT, Zhang D, Qiao YC, et al. Association of tau pathology with clinical symptoms in the subfields of hippocampal formation[J]. Front Aging Neurosci, 2021, 13: 672077. DOI: 10.3389/fnagi.2021.672077.
[70]
Park KH, Noh Y, Choi EJ, et al. Functional connectivity of the Hippocampus in early- and vs. late-onset Alzheimer's disease[J]. J Clin Neurol, 2017, 13(4): 387-393. DOI: 10.3988/jcn.2017.13.4.387.
[71]
Lee PL, Chou KH, Chung CP, et al. Posterior cingulate cortex network predicts Alzheimer's disease progression[J]. Front Aging Neurosci, 2020, 12: 608667. DOI: 10.3389/fnagi.2020.608667.
[72]
Yu EY, Liao ZL, Mao DW, et al. Directed functional connectivity of posterior cingulate cortex and whole brain in Alzheimer's disease and mild cognitive impairment[J]. Curr Alzheimer Res, 2017, 14(6): 628-635. DOI: 10.2174/1567205013666161201201000.
[73]
Sörensen A, Blazhenets G, Rücker G, et al. Prognosis of conversion of mild cognitive impairment to Alzheimer's dementia by voxel-wise Cox regression based on FDG PET data[J]. Neuroimage Clin, 2019, 21: 101637. DOI: 10.1016/j.nicl.2018.101637.
[74]
Min J, Zhou XX, Zhou F, et al. A study on changes of the resting-state brain function network in patients with amnestic mild cognitive impairment[J]. Braz J Med Biol Res, 2019, 52(5): e8244. DOI: 10.1590/1414-431X20198244.
[75]
Behfar Q, Behfar SK, von Reutern B, et al. Graph theory analysis reveals resting-state compensatory mechanisms in healthy aging and prodromal Alzheimer's disease[J]. Front Aging Neurosci, 2020, 12: 576627. DOI: 10.3389/fnagi.2020.576627.
[76]
Lenzi D, Serra L, Perri R, et al. Single domain amnestic MCI: a multiple cognitive domains fMRI investigation[J]. Neurobiol Aging, 2011, 32(9): 1542-1557. DOI: 10.1016/j.neurobiolaging.2009.09.006.
[77]
Wang M, Yan ZZ, Xiao SY, et al. A novel metabolic connectome method to predict progression to mild cognitive impairment[J]. Behav Neurol, 2020, 2020: 2825037. DOI: 10.1155/2020/2825037.
[78]
Sendi MSE, Zendehrouh E, Fu ZN, et al. Disrupted dynamic functional network connectivity among cognitive control networks in the progression of Alzheimer's disease[J]. Brain Connect, 2021, DOI: . DOI: 10.1089/brain.2020.0847.

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