Functional connectivity changes in two cortico-hippocampal networks of Alzheimer's disease continuum and their correlations with cognition: A SILCODE study
Restricted accessResearch articleFirst published online December, 2024
Functional connectivity changes in two cortico-hippocampal networks of Alzheimer's disease continuum and their correlations with cognition: A SILCODE study
The anterior-temporal (AT) and posterior-medial (PM) networks have been proposed to play pivotal roles in the memory processing associated with Alzheimer's disease (AD). Nevertheless, these two networks’ intrinsic functional coupling characteristics are still vague in different AD stages.
Objective
To explore the functional connectivity (FC) alterations within and across the AT&PM networks in patients with dementia of the Alzheimer's type (DAT), mild cognitive impairment (MCI), subjective cognitive decline (SCD), and normal controls (NC).
Methods
A total of 368 participants over 50 years old from the SILCODE study were recruited, including 99 NC, 134 SCD, 67 MCI, and 68 DAT patients. All the participants underwent a resting-state functional magnetic resonance imaging scan and a battery of neuropsychological tests. The 56 regions-of-interest of the AT&PM networks were defined broadly following existing literature. The FCs were calculated using DPABINet and compared among these four groups. Correlation analyses were performed on FCs and cognitive tests.
Results
Analysis of variance of all four groups showed significant alteration, mainly in the PM networks. Compared to NC, globally decreased FCs regarding AT&PM networks were observed in DAT and MCI patients, while globally increased FCs regarding AT&PM networks were observed in SCD. The decreased FCs in DAT were significantly correlated with the neuropsychological test on the memory domain.
Conclusions
The FC alteration showed different patterns across the AD continuum, especially in individuals with SCD. The elevated FCs in the AT&PM networks of SCD may implicate certain compensating processes in the early stage of AD.
ScheltensPDe StrooperBKivipeltoM, et al.Alzheimer's disease. Lancet2021; 397: 1577–1590.
2.
SquireLRZola-MorganS. The medial temporal lobe memory system. Science1991; 253: 1380–1386.
3.
La JoieRLandeauBPerrotinA, et al.Intrinsic connectivity identifies the hippocampus as a main crossroad between Alzheimer's and semantic dementia-targeted networks. Neuron2014; 81: 1417–1428.
4.
Cohn-SheehyBIRanganathC. Time regained: how the human brain constructs memory for time. Curr Opin Behav Sci2017; 17: 169–177.
5.
SquireLRGenzelLWixtedJT, et al.Memory consolidation. Cold Spring Harb Perspect Biol2015; 7: a021766.
6.
KahnIAndrews-HannaJRVincentJL, et al.Distinct cortical anatomy linked to subregions of the medial temporal lobe revealed by intrinsic functional connectivity. J Neurophysiol2008; 100: 129–139.
7.
GourNRanjevaJPCeccaldiM, et al.Basal functional connectivity within the anterior temporal network is associated with performance on declarative memory tasks. Neuroimage2011; 58: 687–697.
8.
RitcheyMLibbyLARanganathC. Cortico-hippocampal systems involved in memory and cognition: the PMAT framework. Prog Brain Res2015; 219: 45–64.
9.
RitcheyMMontchalMEYonelinasAP, et al.Delay-dependent contributions of medial temporal lobe regions to episodic memory retrieval. Elife2015; 4: e05025.
10.
Lambon RalphMACipolottiLManesF, et al.Taking both sides: do unilateral anterior temporal lobe lesions disrupt semantic memory?Brain2010; 133: 3243–3255.
11.
de FloresRDasSRXieL, et al.Medial temporal lobe networks in Alzheimer's disease: structural and molecular vulnerabilities. J Neurosci2022; 42: 2131–2141.
ParkYHJeongHYJangJW, et al.Disruption of the posterior medial network during the acute stage of transient global amnesia: a preliminary study. Clin EEG Neurosci2016; 47: 69–74.
14.
RanganathCRitcheyM. Two cortical systems for memory-guided behaviour. Nat Rev Neurosci2012; 13: 713–726.
15.
SeeleyWWCrawfordRKZhouJ, et al.Neurodegenerative diseases target large-scale human brain networks. Neuron2009; 62: 42–52.
16.
RitcheyMYonelinasAPRanganathC. Functional connectivity relationships predict similarities in task activation and pattern information during associative memory encoding. J Cogn Neurosci2014; 26: 1085–1099.
17.
JackCRJrBennettDABlennowK, et al.NIA-AA Research framework: toward a biological definition of Alzheimer's disease. Alzheimers Dement2018; 14: 535–562.
18.
JanssenOJansenWJVosSJB, et al.Characteristics of subjective cognitive decline associated with amyloid positivity. Alzheimers Dement2021; 18: 1832–1845.
19.
JessenFWolfsgruberSKleineindamL, et al.Subjective cognitive decline and stage 2 of Alzheimer disease in patients from memory centers. Alzheimers Dement2022; 19: 487–497.
20.
ShaoKHuXKleineidamL, et al.Amyloid and SCD jointly predict cognitive decline across Chinese and German cohorts. Alzheimers Dement2024; 20: 5926–5939.
21.
JessenFAmariglioREBuckleyRF, et al.The characterisation of subjective cognitive decline. Lancet Neurol2020; 19: 271–278.
22.
JessenFAmariglioREvan BoxtelM, et al.A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer's disease. Alzheimers Dement2014; 10: 844–852.
23.
HrybouskiSDasSRXieL, et al.Aging and Alzheimer's disease have dissociable effects on local and regional medial temporal lobe connectivity. Brain Commun2023; 5: fcad245.
24.
BerronDVogelJWInselPS, et al.Early stages of tau pathology and its associations with functional connectivity, atrophy and memory. Brain2021; 144: 2771–2783.
25.
MaassABerronDHarrisonTM, et al.Alzheimer's pathology targets distinct memory networks in the ageing brain. Brain2019; 142: 2492–2509.
26.
AdamsJNMaassAHarrisonTM, et al.Cortical tau deposition follows patterns of entorhinal functional connectivity in aging. Elife2019; 8: e49132.
27.
GourNFelicianODidicM, et al.Functional connectivity changes differ in early and late-onset Alzheimer's disease. Hum Brain Mapp2014; 35: 2978–2994.
28.
ZhouYDoughertyJHJrHubnerKF, et al. Abnormal connectivity in the posterior cingulate and hippocampus in early Alzheimer's disease and mild cognitive impairment. Alzheimers Dement2008; 4: 265–270.
29.
DasSRPlutaJMancusoL, et al.Anterior and posterior MTL networks in aging and MCI. Neurobiol Aging2015; 36: S141–S150. S150.e1.
30.
YaoZZhangYLinL, et al.Abnormal cortical networks in mild cognitive impairment and Alzheimer's disease. PLoS Comput Biol2010; 6: e1001006.
31.
LiXWangXSuL, et al.Sino Longitudinal Study on Cognitive Decline (SILCODE): protocol for a Chinese longitudinal observational study to develop risk prediction models of conversion to mild cognitive impairment in individuals with subjective cognitive decline. BMJ Open2019; 9: e028188.
32.
ChenGLiuCYangK, et al.Beneficial effects of brain reserve on cognition in individuals with subjective cognitive decline from the SILCODE study. J Alzheimers Dis2020; 75: 1203–1210.
33.
JackCRJrAlbertMSKnopmanDS, et al.Introduction to the recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement2011; 7: 257–262.
34.
PetersenRC. Mild cognitive impairment as a diagnostic entity. J Intern Med2004; 256: 183–194.
35.
BondiMWEdmondsECJakAJ, et al.Neuropsychological criteria for mild cognitive impairment improves diagnostic precision, biomarker associations, and progression rates. J Alzheimers Dis2014; 42: 275–289.
36.
OldfieldRC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia1971; 9: 97–113.
37.
JenkinsonMBannisterPBradyM, et al.Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage2002; 17: 825–841.
38.
LiHJiaJYangZ. Mini-Mental State Examination in elderly Chinese: a population-based normative study. J Alzheimers Dis2016; 53: 487–496.
39.
ChenKLXuYChuAQ, et al.Validation of the Chinese version of Montreal Cognitive Assessment Basic for screening mild cognitive impairment. J Am Geriatr Soc2016; 64: e285–e290.
40.
ZhaoQLvYZhouY, et al.Short-term delayed recall of auditory verbal learning test is equivalent to long-term delayed recall for identifying amnestic mild cognitive impairment. PLoS One2012; 7: e51157.
41.
ZhaoQGuoQLiF, et al.The Shape Trail Test: application of a new variant of the Trail making test. PLoS One2013; 8: e57333.
42.
GuoQJinLHongZ. A specific phenomenon of animal fluency test in Chinese elderly. Chinese Mental Health J2007; 21: 622–625.
43.
GuoQHongZShiW. Boston Naming test in Chinese Elderly, patient with mild cognitive impairment and Alzheimer’s dementia. Chinese Mental Health J2006; 20: 81–84.
44.
YuJLiJHuangX. The Beijing version of the Montreal Cognitive Assessment as a brief screening tool for mild cognitive impairment: a community-based study. BMC Psychiatry2012; 12: 156.
45.
MajMD'EliaLSatzP, et al.Evaluation of two new neuropsychological tests designed to minimize cultural bias in the assessment of HIV-1 seropositive persons: a WHO study. Arch Clin Neuropsychol1993; 8: 123–135.
46.
YanC-GZangY-F. DPARSF: a MATLAB toolbox for “pipeline” data analysis of resting-state fMRI. Front Syst Neurosci2010; 4: 13.
47.
YanC-GWangX-DZuoX-N, et al.DPABI: data processing & analysis for (resting-state) brain imaging. Neuroinformatics2016; 14: 339–351.
48.
FristonKJWilliamsSHowardR, et al.Movement-related effects in fMRI time-series. Magn Reson Med1996; 35: 346–355.
49.
MurphyKFoxMD. Towards a consensus regarding global signal regression for resting state functional connectivity MRI. Neuroimage2017; 154: 169–173.
50.
HanFChenJBelkin-RosenA, et al.Reduced coupling between cerebrospinal fluid flow and global brain activity is linked to Alzheimer disease-related pathology. PLoS Biol2021; 19: e3001233.
51.
LibbyLAEkstromADRaglandJD, et al.Differential connectivity of perirhinal and parahippocampal cortices within human hippocampal subregions revealed by high-resolution functional imaging. J Neurosci2012; 32: 6550–6560.
52.
PervaizUVidaurreDWoolrichMW, et al.Optimising network modelling methods for fMRI. Neuroimage2020; 211: 116604.
53.
YanC-GWangXDLuB, et al.DPABINet: a toolbox for brain network and graph theoretical analyses. Sci Bull (Beijing)2024; 69: 1628–1631.
54.
YanC-GCheungBKellyC, et al.A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics. NeuroImage2013; 76: 183–201.
55.
WangYWChenXYanC-G. Comprehensive evaluation of harmonization on functional brain imaging for multisite data-fusion. Neuroimage2023; 274: 120089.
56.
MorrisJCRoeCMXiongC, et al.APOE Predicts amyloid-beta but not tau Alzheimer pathology in cognitively normal aging. Ann Neurol2010; 67: 122–131.
57.
SalamiAWahlinAKaboodvandN, et al.Longitudinal evidence for dissociation of anterior and posterior MTL resting-state connectivity in aging: links to perfusion and memory. Cereb Cortex2016; 26: 3953–3963.
58.
WangSRitcheyMLibbyL, et al.Functional connectivity based parcellation of the human medial temporal lobe. Neurobiol Learn Mem2016; 134: 123–134.
59.
CrossonB. The role of the thalamus in declarative and procedural linguistic memory processes. Front Psychol2021; 12: 682199.
60.
GosseriesOYuQLaRocqueJJ, et al.Parietal-occipital interactions underlying control- and representation-related processes in working memory for nonspatial visual features. J Neurosci2018; 38: 4357–4366.
61.
MionMPattersonKAcosta-CabroneroJ, et al.What the left and right anterior fusiform gyri tell us about semantic memory. Brain2010; 133: 3256–3268.
62.
BrownTIUncapherMRChowTE, et al.Cognitive control, attention, and the other race effect in memory. PLoS One2017; 12: e0173579.
63.
WangYRisacherSLWestJD, et al.Altered default mode network connectivity in older adults with cognitive complaints and amnestic mild cognitive impairment. J Alzheimers Dis2013; 35: 751–760.
64.
DillenKNHJacobsHILKukoljaJ, et al.Functional disintegration of the default mode network in prodromal Alzheimer's disease. J Alzheimers Dis2017; 59: 169–187.
65.
SharmaNMurariGVandermorrisS, et al.Functional connectivity between the posterior default mode network and parahippocampal gyrus is disrupted in older adults with subjective cognitive decline and correlates with subjective memory ability. J Alzheimers Dis2021; 82: 435–445.
66.
DasSRPlutaJMancusoL, et al.Increased functional connectivity within medial temporal lobe in mild cognitive impairment. Hippocampus2013; 23: 1–6.
67.
ChenJDuanXShuH, et al.Differential contributions of subregions of medial temporal lobe to memory system in amnestic mild cognitive impairment: insights from fMRI study. Sci Rep2016; 6: 26148.
68.
Grill-SpectorKKourtziZKanwisherN. The lateral occipital complex and its role in object recognition. Vision Res2001; 41: 1409–1422.
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