The Anterior-posterior Functional Connectivity Disconnection in the Elderly with Subjective Memory Impairment and Amnestic Mild Cognitive Impairment

Author(s): Wuhai Tao, Jinping Sun, Xin Li, Wen Shao, Jing Pei, Caishui Yang, Wenxiao Wang, Kai Xu, Jun Wang*, Zhanjun Zhang*

Journal Name: Current Alzheimer Research

Volume 17 , Issue 4 , 2020

  Journal Home
Translate in Chinese
Become EABM
Become Reviewer

Abstract:

Background: Subjective Memory Impairment (SMI) may tremendously increase the risk of Alzheimer’s Disease (AD). The full understanding of the neuromechanism of SMI will shed light on the early intervention of AD.

Methods: In the current study, 23 Healthy Controls (HC), 22 SMI subjects and 24 amnestic Mild Cognitive Impairment (aMCI) subjects underwent the comprehensive neuropsychological assessment and the resting-state functional magnetic resonance imaging scan. The difference in the connectivity of the Default Mode Network (DMN) and Functional Connectivity (FC) from the Region of Interest (ROI) to the whole brain were compared, respectively.

Results: The results showed that HC and SMI subjects had significantly higher connectivity in the region of the precuneus area compared to aMCI subjects. However, from this region to the whole brain, SMI and aMCI subjects had significant FC decrease in the right anterior cingulum, left superior frontal and left medial superior frontal gyrus compared to HC. In addition, this FC change was significantly correlated with the cognitive function decline in participants.

Conclusion: Our study indicated that SMI subjects had relatively intact DMN connectivity but impaired FC between the anterior and posterior brain. The findings suggest that long-distance FC is more vulnerable than the short ones in the people with SMI.

Keywords: Subjective memory impairment , functional connectivity , default mode network , amnestic mild cognitive impairment , cognitive decline , aging.

[1]
Sperling RA, Aisen PS, Beckett LA, et al. Toward defining the preclinical stages of Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimers Dement 2011; 7(3): 280-92.
[http://dx.doi.org/10.1016/j.jalz.2011.03.003] [PMID: 21514248]
[2]
Jessen F, Amariglio RE, van Boxtel M, et al. Subjective Cognitive Decline Initiative (SCD-I) Working Group. A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer’s disease. Alzheimers Dement 2014; 10(6): 844-52.
[http://dx.doi.org/10.1016/j.jalz.2014.01.001] [PMID: 24798886]
[3]
Stewart R, Godin O, Crivello F, et al. Subjective cognitive decline in preclinical Alzheimer’s disease.Longitudinal neuroimaging correlates of subjective memory impairment: 4-year prospective community study. Br J Psychiatry 2011; 198(3): 199-205.
[http://dx.doi.org/10.1192/bjp.bp.110.078683] [PMID: 21357878]
[4]
Stewart R, Godin o, Crivello F, et al. Longitudinal neuroimaging correlates of subjective memory impairment: 4-year prospective community study. Brit J Psychiat 198(3): 199-205.
[5]
Ryu SY, Lim EY, Na S, et al. Hippocampal and entorhinal structures in subjective memory impairment:A combined MRI volumetric and DTI study. Int Psychogeriatr 2017; 29(5): 785-92.
[http://dx.doi.org/10.1017/S1041610216002349] [PMID: 28067183]
[6]
Schultz SA, Oh JM, Koscik RL, et al. Subjective memory complaints, cortical thinning, and cognitive dysfunction in middle-aged adults at risk for AD. Alzheimers Dement (Amst) 2015; 1(1): 33-40.
[http://dx.doi.org/10.1016/j.dadm.2014.11.010] [PMID: 25938132]
[7]
Li XY, Tang ZC, Sun Y, Tian J, Liu ZY, Han Y. White matter degeneration in subjective cognitive decline: a diffusion tensor imaging study. Oncotarget 2016; 7(34): 54405-14.
[http://dx.doi.org/10.18632/oncotarget.10091] [PMID: 27384675]
[8]
Shu N, Wang X, Bi Q, Zhao T, Han Y. Disrupted topologic efficiency of white matter structural connectome in individuals with subjective cognitive decline. Radiology 2018; 286(1): 229-38.
[PMID: 28799862]
[9]
Jeong HS, Park JS, Song IU, Chung YA, Rhie SJ. Changes in cognitive function and brain glucose metabolism in elderly women with subjective memory impairment: A 24-month prospective pilot study. Acta Neurol Scand 2017; 135(1): 108-14.
[http://dx.doi.org/10.1111/ane.12569] [PMID: 26861213]
[10]
Snitz BE, Lopez OL, McDade E, et al. Amyloid-β imaging in older adults presenting to a memory clinic with subjective cognitive decline: A pilot study. J Alzheimers Dis 2015; 48(1): S151-9.
[http://dx.doi.org/10.3233/JAD-150113] [PMID: 26402082]
[11]
Delbeuck X, Van der Linden M, Collette F. Alzheimer’s disease as a disconnection syndrome? Neuropsychol Rev 2003; 13(2): 79-92.
[http://dx.doi.org/10.1023/A:1023832305702] [PMID: 12887040]
[12]
Sheline YI, Raichle ME. Resting state functional connectivity in preclinical Alzheimer’s disease. Biol Psychiatry 2013; 74(5): 340-7.
[http://dx.doi.org/10.1016/j.biopsych.2012.11.028] [PMID: 23290495]
[13]
Dillen KN, Jacobs HI, Kukolja J, et al. Functional disintegration of the default mode network in prodromal Alzheimer’s disease. Oncotarget 2017;; 7(34):: 54405--14.
[http://dx.doi.org/10.3233/JAD-161120]
[14]
Hafkemeijer A, Altmann-Schneider I, Oleksik AM, et al. Increased functional connectivity and brain atrophy in elderly with subjective memory complaints. Brain Connect 2013; 3(4): 353-62.
[http://dx.doi.org/10.1089/brain.2013.0144] [PMID: 23627661]
[15]
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 Alzheimers Dis 2013; 35(4): 751-60.
[http://dx.doi.org/10.3233/JAD-130080] [PMID: 23481685]
[16]
Liu Y, Yu C, Zhang X, et al. Impaired long distance functional connectivity and weighted network architecture in Alzheimer’s disease. Cereb Cortex 2014; 24(6): 1422-35.
[http://dx.doi.org/10.1093/cercor/bhs410] [PMID: 23314940]
[17]
Zhang H-Y, Wang S-J, Xing J, et al. Detection of PCC functional connectivity characteristics in resting-state fMRI in mild Alzheimer’s disease. Behav Brain Res 2009; 197(1): 103-8.
[http://dx.doi.org/10.1016/j.bbr.2008.08.012] [PMID: 18786570]
[18]
Dillen KNH, Jacobs HIL, Kukolja J, et al. Aberrant functional connectivity differentiates retrosplenial cortex from posterior cingulate cortex in prodromal Alzheimer’s disease. Neurobiol Aging 2016; 44: 114-26.
[http://dx.doi.org/10.1016/j.neurobiolaging.2016.04.010] [PMID: 27318139]
[19]
Yasuno F, Kazui H, Yamamoto A, et al. Resting-state synchrony between the retrosplenial cortex and anterior medial cortical structures relates to memory complaints in subjective cognitive impairment. Neurobiol Aging 2015; 36(6): 2145-52.
[http://dx.doi.org/10.1016/j.neurobiolaging.2015.03.006] [PMID: 25862421]
[20]
Li X, Ma C, Zhang J, et al. Beijing Ageing Brain Rejuvenation Initiative. Prevalence of and potential risk factors for mild cognitive impairment in community-dwelling residents of Beijing. J Am Geriatr Soc 2013; 61(12): 2111-9.
[http://dx.doi.org/10.1111/jgs.12552] [PMID: 24479143]
[21]
Petersen RC, Smith GE, Waring SC, Ivnik RJ, Tangalos EG, Kokmen E. Mild cognitive impairment: Clinical characterization and outcome. Arch Neurol 1999; 56(3): 303-8.
[http://dx.doi.org/10.1001/archneur.56.3.303] [PMID: 10190820]
[22]
Rosenberg SJ, Ryan JJ, Prifitera A. rey auditory-verbal learning test performance of patients with and without memory impairment. J Clin Psychol 1984; 40(3): 785-7.
[http://dx.doi.org/10.1002/1097-4679(198405)40:3<785:AID-JCLP2270400325>3.0.CO;2-4] [PMID: 6746989]
[23]
Shin M-S, Park S-Y, Park S-R, Seol S-H, Kwon JS. Clinical and empirical applications of the Rey-Osterrieth complex figure test. Nat Protoc 2006; 1(2): 892-9.
[http://dx.doi.org/10.1038/nprot.2006.115] [PMID: 17406322]
[24]
Guo Q, Zhao Q, Chen M, Ding D, Hong Z. A comparison study of mild cognitive impairment with 3 memory tests among Chinese individuals. Alzheimer Dis Assoc Disord 2009; 23(3): 253-9.
[http://dx.doi.org/10.1097/WAD.0b013e3181999e92]
[25]
Zhao QD, Ding Q, Guo JA, Mortimer CI, Salmon CD. Shanghai community brain health initiative pilot study: Neuropsychological results Alzheimer’s Dementia. J Alzheimer’s Assoc 2009; 5(4): P14-5.
[26]
Greicius MD, Srivastava G, Reiss AL, Menon V. Default-mode network activity distinguishes Alzheimer’s disease from healthy aging: Evidence from functional MRI. Proc Natl Acad Sci USA 2004; 101(13): 4637-42.
[http://dx.doi.org/10.1073/pnas.0308627101] [PMID: 15070770]
[27]
Utevsky AV, Smith DV, Huettel SA. Precuneus is a functional core of the default-mode network. J Neurosci 2014; 34(3): 932-40.
[http://dx.doi.org/10.1523/JNEUROSCI.4227-13.2014] [PMID: 24431451]
[28]
López-Sanz D, Garcés P. Maestú, Network disruption in the preclinical stages of Alzheimer’s disease: From subjective cognitive decline to mild cognitive impairment. Int J Neural Syst 2017; 27(8)1750041
[http://dx.doi.org/10.1142/S0129065717500411] [PMID: 28958179]
[29]
Rabin LA, Chi SY, Wang C, Fogel J, Kann SJ, Aronov A. Prospective memory on a novel clinical task in older adults with mild cognitive impairment and subjective cognitive decline. Neuropsychol Rehabil 2014; 24(6): 868-93.
[http://dx.doi.org/10.1080/09602011.2014.915855] [PMID: 24875614]
[30]
Garcia-Ptacek S, Eriksdotter M, Jelic V, Porta-Etessam J, Kåreholt I, Manzano Palomo S. Subjective cognitive impairment: Towards early identification of Alzheimer disease. Neurologia 2016; 31(8): 562-71.
[http://dx.doi.org/10.1016/j.nrl.2013.02.007] [PMID: 23601758]
[31]
Burmester B, Leathem J, Merrick P. Subjective cognitive complaints and objective cognitive function in aging: A systematic review and meta-analysis of recent cross-sectional findings. Neuropsychol Rev 2016; 26(4): 376-93.
[http://dx.doi.org/10.1007/s11065-016-9332-2] [PMID: 27714573]
[32]
Kurt P, Yener G, Oguz M. Impaired digit span can predict further cognitive decline in older people with subjective memory complaint: A preliminary result. Aging Ment Health 2011; 15(3): 364-9.
[http://dx.doi.org/10.1080/13607863.2010.536133] [PMID: 21491221]
[33]
Pasquini L, Benson G, Grothe MJ, et al. Alzheimer’s Disease Neuroimaging Initiative. Individual correspondence of amyloid-β and intrinsic connectivity in the posterior default mode network across stages of Alzheimer’s disease. J Alzheimers Dis 2017; 58(3): 763-73.
[http://dx.doi.org/10.3233/JAD-170096] [PMID: 28482640]
[34]
Tao W, Li X, Zhang J, Chen Y, Ma C, Liu Z, et al. Inflection point in course of mild cognitive impairment: Increased functional connectivity of default mode network. J Alzheimer's Dis 2017; 60(2): 679-90.
[35]
Fransson P, Marrelec G. The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: Evidence from a partial correlation network analysis. Neuroimage 2008; 42(3): 1178-84.
[PMID: 18598773]
[36]
Viviano RP, Hayes JM, Pruitt PJ, et al. Aberrant memory system connectivity and working memory performance in subjective cognitive decline. Neuroimage 2019; 185: 556-64.
[http://dx.doi.org/10.1016/j.neuroimage.2018.10.015] [PMID: 30308246]
[37]
Schmidt SA, Carpenter-Thompson J, Husain FT. Connectivity of precuneus to the default mode and dorsal attention networks: A possible invariant marker of long-term tinnitus. Neuroimage Clin 2017; 16: 196-204.
[http://dx.doi.org/10.1016/j.nicl.2017.07.015] [PMID: 28794980]
[38]
Cavanna AE, Trimble MR. The precuneus: A review of its functional anatomy and behavioural correlates. Brain 2006; 129(Pt 3): 564-83.
[http://dx.doi.org/10.1093/brain/awl004] [PMID: 16399806]
[39]
Dennis EL, Thompson PM. Functional brain connectivity using fMRI in aging and Alzheimer’s disease. Neuropsychol Rev 2014; 24(1): 49-62.
[http://dx.doi.org/10.1007/s11065-014-9249-6] [PMID: 24562737]
[40]
Mutlu J, Landeau B, Tomadesso C, et al. Connectivity disruption, atrophy, and hypometabolism within posterior cingulate networks in Alzheimer’s disease. Front Neurosci 2016; 10: 582.
[http://dx.doi.org/10.3389/fnins.2016.00582] [PMID: 28066167]
[41]
Grajski KA, Bressler SL. Differential default-mode network functional connectivity and morphometric changes in Alzheimer’s disease. bioRxiv 2017; 232: 165.
[42]
Grothe MJ, Barthel H, Sepulcre J, Dyrba M, Sabri O, Teipel SJ. Alzheimer’s Disease Neuroimaging Initiative. In vivo staging of regional amyloid deposition. Neurology 2017; 89(20): 2031-8.
[http://dx.doi.org/10.1212/WNL.0000000000004643] [PMID: 29046362]
[43]
Larivière S, Lavigne KM, Woodward TS, Gerretsen P, Graff-Guerrero A, Menon M. Altered functional connectivity in brain networks underlying self-referential processing in delusions of reference in schizophrenia. Psychiat Res Neuroimag 2017; 263: 32-43.
[http://dx.doi.org/10.1016/j.pscychresns.2017.03.005] [PMID: 28315577]
[44]
Qin P, Northoff G. How is our self related to midline regions and the default-mode network? Neuroimage 2011; 57(3): 1221-33.
[http://dx.doi.org/10.1016/j.neuroimage.2011.05.028] [PMID: 21609772]
[45]
Kolling N, Wittmann MK, Behrens TE, Boorman ED, Mars RB, Rushworth MF. Value, search, persistence and model updating in anterior cingulate cortex. Nat Neurosci 2016; 19(10): 1280-5.
[http://dx.doi.org/10.1038/nn.4382] [PMID: 27669988]
[46]
Franzmeier N, Duering M, Weiner M, Dichgans M, Ewers M. Alzheimer’s Disease Neuroimaging Initiative (ADNI). Left frontal cortex connectivity underlies cognitive reserve in prodromal Alzheimer disease. Neurology 2017; 88(11): 1054-61.
[http://dx.doi.org/10.1212/WNL.0000000000003711] [PMID: 28188306]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 17
ISSUE: 4
Year: 2020
Page: [373 - 381]
Pages: 9
DOI: 10.2174/1567205017666200525015017
Price: $65

Article Metrics

PDF: 24
HTML: 4