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Published in: Alzheimer's Research & Therapy 1/2018

Open Access 01-12-2018 | Research

Functional connectivity in cognitive control networks mitigates the impact of white matter lesions in the elderly

Authors: Gloria Benson, Andrea Hildebrandt, Catharina Lange, Claudia Schwarz, Theresa Köbe, Werner Sommer, Agnes Flöel, Miranka Wirth

Published in: Alzheimer's Research & Therapy | Issue 1/2018

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Abstract

Background

Cerebrovascular pathology, quantified by white matter lesions (WML), is known to affect cognition in aging, and is associated with an increased risk of dementia. The present study aimed to investigate whether higher functional connectivity in cognitive control networks mitigates the detrimental effect of WML on cognition.

Methods

Nondemented older participants (≥ 50 years; n = 230) underwent cognitive evaluation, fluid-attenuated inversion recovery (FLAIR) magnetic resonance imaging (MRI), and resting state functional magnetic resonance imaging (fMRI). Total WML volumes were quantified algorithmically. Functional connectivity was assessed in preselected higher-order resting state networks, namely the fronto-parietal, the salience, and the default mode network, using global and local measures. Latent moderated structural equations modeling examined direct and interactive relationships between WML volumes, functional connectivity, and cognition.

Results

Larger WML volumes were associated with worse cognition, having a greater impact on executive functions (β = −0.37, p < 0.01) than on memory (β = −0.22, p < 0.01). Higher global functional connectivity in the fronto-parietal network and higher local connectivity between the salience network and medial frontal cortex significantly mitigated the impact of WML on executive functions, (unstandardized coefficients: b = 2.39, p = 0.01; b = 3.92, p = 0.01) but not on memory (b = -5.01, p = 0.51, b = 2.01, p = 0.07, respectively). No such effects were detected for the default mode network.

Conclusion

Higher functional connectivity in fronto-parietal and salience networks may protect against detrimental effects of WML on executive functions, the cognitive domain that was predominantly affected by cerebrovascular pathology. These results highlight the crucial role of cognitive control networks as a neural substrate of cognitive reserve in older individuals.
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Literature
1.
go back to reference Prins ND, Scheltens P. White matter hyperintensities, cognitive impairment and dementia: an update. Nat Rev Neurol. 2015;11:157–65.CrossRef Prins ND, Scheltens P. White matter hyperintensities, cognitive impairment and dementia: an update. Nat Rev Neurol. 2015;11:157–65.CrossRef
2.
go back to reference Raz N, Rodrigue KM. Differential aging of the brain: patterns, cognitive correlates and modifiers. Neurosci Biobehav Rev. 2006;30:730–48.CrossRef Raz N, Rodrigue KM. Differential aging of the brain: patterns, cognitive correlates and modifiers. Neurosci Biobehav Rev. 2006;30:730–48.CrossRef
3.
go back to reference Wirth M, Haase CM, Villeneuve S, Vogel J, Jagust WJ. Neuroprotective pathways: lifestyle activity, brain pathology, and cognition in cognitively normal older adults. Neurobiol Aging. 2014;35:1873–82.CrossRef Wirth M, Haase CM, Villeneuve S, Vogel J, Jagust WJ. Neuroprotective pathways: lifestyle activity, brain pathology, and cognition in cognitively normal older adults. Neurobiol Aging. 2014;35:1873–82.CrossRef
4.
go back to reference Au R, Massaro JM, Wolf PA, Young ME, Beiser A, Seshadri S, et al. Association of white matter hyperintensity volume with decreased cognitive functioning: The Framingham Heart Study. Arch Neurol. 2006;63:246–50.CrossRef Au R, Massaro JM, Wolf PA, Young ME, Beiser A, Seshadri S, et al. Association of white matter hyperintensity volume with decreased cognitive functioning: The Framingham Heart Study. Arch Neurol. 2006;63:246–50.CrossRef
5.
go back to reference Tullberg M, Fletcher E, DeCarli C, Mungas D, Reed BR, Harvey DJ, et al. White matter lesions impair frontal lobe function regardless of their location. Neurology. 2004;63:246–53.CrossRef Tullberg M, Fletcher E, DeCarli C, Mungas D, Reed BR, Harvey DJ, et al. White matter lesions impair frontal lobe function regardless of their location. Neurology. 2004;63:246–53.CrossRef
6.
go back to reference Birdsill AC, Koscik RL, Jonaitis EM, Johnson SC, Okonkwo OC, Hermann BP, et al. Regional white matter hyperintensities: aging, Alzheimer’s disease risk, and cognitive function. Neurobiol Aging. 2014;35:769–76.CrossRef Birdsill AC, Koscik RL, Jonaitis EM, Johnson SC, Okonkwo OC, Hermann BP, et al. Regional white matter hyperintensities: aging, Alzheimer’s disease risk, and cognitive function. Neurobiol Aging. 2014;35:769–76.CrossRef
7.
go back to reference Wirth M, Villeneuve S, Haase CM, Madison CM, Oh H, Landau SM, et al. Associations between Alzheimer disease biomarkers, neurodegeneration, and cognition in cognitively normal older people. JAMA Neurol. 2013;70:1512–9.PubMedPubMedCentral Wirth M, Villeneuve S, Haase CM, Madison CM, Oh H, Landau SM, et al. Associations between Alzheimer disease biomarkers, neurodegeneration, and cognition in cognitively normal older people. JAMA Neurol. 2013;70:1512–9.PubMedPubMedCentral
8.
go back to reference Debette S, Markus HS. The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ. 2010;341:1–9.CrossRef Debette S, Markus HS. The clinical importance of white matter hyperintensities on brain magnetic resonance imaging: systematic review and meta-analysis. BMJ. 2010;341:1–9.CrossRef
9.
go back to reference Nebes R, Meltzer C, Whyte E, Scanlon J, Halligan E, Saxton J, et al. The relation of white matter hyperintensities to cognitive performance in the normal old: education matters. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn. 2006;13:326–40.CrossRef Nebes R, Meltzer C, Whyte E, Scanlon J, Halligan E, Saxton J, et al. The relation of white matter hyperintensities to cognitive performance in the normal old: education matters. Neuropsychol Dev Cogn B Aging Neuropsychol Cogn. 2006;13:326–40.CrossRef
10.
go back to reference Saczynski JS, Jonsdottir MK, Sigurdsson S, Eiriksdottir G, Jonsson PV, Garcia ME, et al. White matter lesions and cognitive performance: the role of cognitively complex leisure activity. J Gerontol A Biol Sci Med Sci. 2008;63:848–54.CrossRef Saczynski JS, Jonsdottir MK, Sigurdsson S, Eiriksdottir G, Jonsson PV, Garcia ME, et al. White matter lesions and cognitive performance: the role of cognitively complex leisure activity. J Gerontol A Biol Sci Med Sci. 2008;63:848–54.CrossRef
11.
go back to reference Stern Y. What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc. 2002;8:448–60.CrossRef Stern Y. What is cognitive reserve? Theory and research application of the reserve concept. J Int Neuropsychol Soc. 2002;8:448–60.CrossRef
12.
go back to reference Bartrés-Faz D, Arenaza-Urquijo EM. Structural and functional imaging correlates of cognitive and brain reserve hypotheses in healthy and pathological aging. Brain Topogr. 2011;24:340–57.CrossRef Bartrés-Faz D, Arenaza-Urquijo EM. Structural and functional imaging correlates of cognitive and brain reserve hypotheses in healthy and pathological aging. Brain Topogr. 2011;24:340–57.CrossRef
13.
go back to reference Barulli D, Stern Y. Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn Sci. 2013;17:502–9.CrossRef Barulli D, Stern Y. Efficiency, capacity, compensation, maintenance, plasticity: emerging concepts in cognitive reserve. Trends Cogn Sci. 2013;17:502–9.CrossRef
14.
15.
go back to reference Dufouil C, Alpérovitch A, Tzourio C. Influence of education on the relationship between white matter lesions and cognition. Neurol Int. 2003;60:831–6. Dufouil C, Alpérovitch A, Tzourio C. Influence of education on the relationship between white matter lesions and cognition. Neurol Int. 2003;60:831–6.
16.
go back to reference Zieren N, Duering M, Peters N, Reyes S, Jouvent E, Hervé D, et al. Education modifies the relation of vascular pathology to cognitive function: cognitive reserve in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Neurobiol Aging. 2013;34:400–7.CrossRef Zieren N, Duering M, Peters N, Reyes S, Jouvent E, Hervé D, et al. Education modifies the relation of vascular pathology to cognitive function: cognitive reserve in cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy. Neurobiol Aging. 2013;34:400–7.CrossRef
17.
go back to reference Brickman AM, Siedlecki KL, Muraskin J, Manly JJ, Luchsinger JA, Yeung LK, et al. White matter hyperintensities and cognition: testing the reserve hypothesis. Neurobiol Aging. 2011;32:1588–98.CrossRef Brickman AM, Siedlecki KL, Muraskin J, Manly JJ, Luchsinger JA, Yeung LK, et al. White matter hyperintensities and cognition: testing the reserve hypothesis. Neurobiol Aging. 2011;32:1588–98.CrossRef
18.
go back to reference Griebe M, Amann M, Hirsch JG, Achtnichts L, Hennerici MG, Gass A, et al. Reduced functional reserve in patients with age-related white matter changes: a preliminary fMRI study of working memory. PLoS One. 2014;9:e103359.CrossRef Griebe M, Amann M, Hirsch JG, Achtnichts L, Hennerici MG, Gass A, et al. Reduced functional reserve in patients with age-related white matter changes: a preliminary fMRI study of working memory. PLoS One. 2014;9:e103359.CrossRef
19.
go back to reference Fernández-Cabello S, Valls-Pedret C, Schurz M, Vidal-Piñeiro D, Sala-Llonch R, Bargallo N, et al. White matter hyperintensities and cognitive reserve during a working memory task: a functional magnetic resonance imaging study in cognitively normal older adults. Neurobiol Aging. 2016;48:23–33 Elsevier Inc.CrossRef Fernández-Cabello S, Valls-Pedret C, Schurz M, Vidal-Piñeiro D, Sala-Llonch R, Bargallo N, et al. White matter hyperintensities and cognitive reserve during a working memory task: a functional magnetic resonance imaging study in cognitively normal older adults. Neurobiol Aging. 2016;48:23–33 Elsevier Inc.CrossRef
20.
go back to reference Serra L, Mancini M, Cercignani M, Di Domenico C, Spanò B, Giulietti G, et al. Network-based substrate of cognitive reserve in Alzheimer’s disease. J Alzheimers Dis. 2016;55:421–30.CrossRef Serra L, Mancini M, Cercignani M, Di Domenico C, Spanò B, Giulietti G, et al. Network-based substrate of cognitive reserve in Alzheimer’s disease. J Alzheimers Dis. 2016;55:421–30.CrossRef
21.
go back to reference Cole MW, Yarkoni T, Repovs G, Anticevic A, Braver TS. Global connectivity of prefrontal cortex predicts cognitive control and intelligence. J Neurosci. 2012;32:8988–99.CrossRef Cole MW, Yarkoni T, Repovs G, Anticevic A, Braver TS. Global connectivity of prefrontal cortex predicts cognitive control and intelligence. J Neurosci. 2012;32:8988–99.CrossRef
22.
go back to reference Elman JA, Oh H, Madison CM, Baker SL, Vogel JW, Marks SM, et al. Neural compensation in older people with brain amyloid-β deposition. Nat Neurosci. 2014;17:1316–8.CrossRef Elman JA, Oh H, Madison CM, Baker SL, Vogel JW, Marks SM, et al. Neural compensation in older people with brain amyloid-β deposition. Nat Neurosci. 2014;17:1316–8.CrossRef
23.
go back to reference Franzmeier N, Duering M, Weiner M, Dichgans M, Ewers M. Left frontal cortex connectivity underlies cognitive reserve in prodromal Alzheimer disease. Neurology. 2017;88:1054–61.CrossRef Franzmeier N, Duering M, Weiner M, Dichgans M, Ewers M. Left frontal cortex connectivity underlies cognitive reserve in prodromal Alzheimer disease. Neurology. 2017;88:1054–61.CrossRef
24.
go back to reference Arenaza-Urquijo EM, Landeau B, La Joie R, Mevel K, Mézenge F, Perrotin A, et al. Relationships between years of education and gray matter volume, metabolism and functional connectivity in healthy elders. Neuroimage. 2013;83C:450–7.CrossRef Arenaza-Urquijo EM, Landeau B, La Joie R, Mevel K, Mézenge F, Perrotin A, et al. Relationships between years of education and gray matter volume, metabolism and functional connectivity in healthy elders. Neuroimage. 2013;83C:450–7.CrossRef
25.
go back to reference Menon V. Salience Network. Brain Mapp An Encycl Ref. 2015;2:597–611. Menon V. Salience Network. Brain Mapp An Encycl Ref. 2015;2:597–611.
26.
go back to reference Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189–98.CrossRef Folstein MF, Folstein SE, McHugh PR. “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res. 1975;12:189–98.CrossRef
27.
go back to reference Knopman DS, Petersen RC. Mild cognitive impairment and mild dementia: a clinical perspective. Mayo Clin Proc. 2014;89:1452–9.CrossRef Knopman DS, Petersen RC. Mild cognitive impairment and mild dementia: a clinical perspective. Mayo Clin Proc. 2014;89:1452–9.CrossRef
28.
go back to reference Kerti L, Witte AV, Winkler A, Grittner U, Rujescu D, Flöel A. Higher glucose levels associated with lower memory and reduced hippocampal microstructure. Neurology. 2013;81:1746–52.CrossRef Kerti L, Witte AV, Winkler A, Grittner U, Rujescu D, Flöel A. Higher glucose levels associated with lower memory and reduced hippocampal microstructure. Neurology. 2013;81:1746–52.CrossRef
29.
go back to reference Köbe T, Witte AV, Schnelle A, Grittner U, Tesky VA, Pantel J, et al. Vitamin B-12 concentration, memory performance, and hippocampal structure in patients with mild cognitive impairment. Am J Clin Nutr. 2016;103:1045–54.CrossRef Köbe T, Witte AV, Schnelle A, Grittner U, Tesky VA, Pantel J, et al. Vitamin B-12 concentration, memory performance, and hippocampal structure in patients with mild cognitive impairment. Am J Clin Nutr. 2016;103:1045–54.CrossRef
30.
go back to reference Lezak MD, Howieson DB, Loring DW, Hannay HJ, Fischer JS. Neuropsychological assessment. 4th ed; New York, Oxford: Oxford University Press; 2004. Lezak MD, Howieson DB, Loring DW, Hannay HJ, Fischer JS. Neuropsychological assessment. 4th ed; New York, Oxford: Oxford University Press; 2004.
31.
go back to reference Reitan R. Validity of the Trail Making Test as an indicator of organic brain damage. Percept Mot Skills. 1958;8:271–6.CrossRef Reitan R. Validity of the Trail Making Test as an indicator of organic brain damage. Percept Mot Skills. 1958;8:271–6.CrossRef
32.
go back to reference Woodard JL, Axelrod BN. Wechsler Memory Scale–Revised. Psychol Assess. 1987;7:445–9.CrossRef Woodard JL, Axelrod BN. Wechsler Memory Scale–Revised. Psychol Assess. 1987;7:445–9.CrossRef
33.
go back to reference Koss E, Ober BA, Delis DC, Friedland RP. The Stroop color-word test: indicator of dementia severity. Int J Neurosci. 1984;24:53–61. CrossRef Koss E, Ober BA, Delis DC, Friedland RP. The Stroop color-word test: indicator of dementia severity. Int J Neurosci. 1984;24:53–61. CrossRef
34.
go back to reference Wechsler D. WAIS-R manual: Wechsler adult intelligence scale-revised. Psychological Corporation. 1981. Wechsler D. WAIS-R manual: Wechsler adult intelligence scale-revised. Psychological Corporation. 1981.
36.
go back to reference Schmidt P, Gaser C, Arsic M, Buck D, Förschler A, Berthele A, et al. An automated tool for detection of FLAIR-hyperintense white-matter lesions in multiple sclerosis. Neuroimage. 2012;59:3774–83 Elsevier Inc.CrossRef Schmidt P, Gaser C, Arsic M, Buck D, Förschler A, Berthele A, et al. An automated tool for detection of FLAIR-hyperintense white-matter lesions in multiple sclerosis. Neuroimage. 2012;59:3774–83 Elsevier Inc.CrossRef
37.
go back to reference Lange C, Suppa P, Maurer A, Ritter K, Pietrzyk U, Steinhagen-Thiessen E, et al. Mental speed is associated with the shape irregularity of white matter MRI hyperintensity load. Brain Imaging Behav. 2017;11:1720–730CrossRef Lange C, Suppa P, Maurer A, Ritter K, Pietrzyk U, Steinhagen-Thiessen E, et al. Mental speed is associated with the shape irregularity of white matter MRI hyperintensity load. Brain Imaging Behav. 2017;11:1720–730CrossRef
38.
go back to reference Malone IB, Leung KK, Clegg S, Barnes J, Whitwell JL, Ashburner J, et al. Accurate automatic estimation of total intracranial volume: a nuisance variable with less nuisance. NeuroImage. 2015;104:366–72.CrossRef Malone IB, Leung KK, Clegg S, Barnes J, Whitwell JL, Ashburner J, et al. Accurate automatic estimation of total intracranial volume: a nuisance variable with less nuisance. NeuroImage. 2015;104:366–72.CrossRef
39.
go back to reference D’Agostino RB, Vasan RS, Pencina MJ, Wolf PA, Cobain M, Massaro JM, et al. General cardiovascular risk profile for use in primary care: The Framingham heart study. Circulation. 2008;117:743–53.CrossRef D’Agostino RB, Vasan RS, Pencina MJ, Wolf PA, Cobain M, Massaro JM, et al. General cardiovascular risk profile for use in primary care: The Framingham heart study. Circulation. 2008;117:743–53.CrossRef
40.
go back to reference Whitfield-Gabrieli S, Nieto-Castanon A. Conn: A functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. 2012;2:125–41.CrossRef Whitfield-Gabrieli S, Nieto-Castanon A. Conn: A functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. 2012;2:125–41.CrossRef
41.
go back to reference Behzadi Y, Restom K, Liau J, Liu TT. A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage. 2007;37:90–101.CrossRef Behzadi Y, Restom K, Liau J, Liu TT. A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage. 2007;37:90–101.CrossRef
42.
go back to reference Cole MW, Repovs G, Anticevic A. The frontoparietal control system: a central role in mental health. Neuroscientist. 2014;20:652–64.CrossRef Cole MW, Repovs G, Anticevic A. The frontoparietal control system: a central role in mental health. Neuroscientist. 2014;20:652–64.CrossRef
43.
go back to reference Bressler SL, Menon V. Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn Sci. 2010;14:277–90CrossRef Bressler SL, Menon V. Large-scale brain networks in cognition: emerging methods and principles. Trends Cogn Sci. 2010;14:277–90CrossRef
44.
go back to reference Franzmeier N, Caballero MÁA, Taylor ANW, Simon-Vermot L, Buerger K, Ertl-Wagner B, et al. Resting-state global functional connectivity as a biomarker of cognitive reserve in mild cognitive impairment. Brain Imaging Behav. 2017;11:368–82.CrossRef Franzmeier N, Caballero MÁA, Taylor ANW, Simon-Vermot L, Buerger K, Ertl-Wagner B, et al. Resting-state global functional connectivity as a biomarker of cognitive reserve in mild cognitive impairment. Brain Imaging Behav. 2017;11:368–82.CrossRef
45.
go back to reference Muthén L, Muthén B. Mplus user’s guide. 8th ed: Los Angeles CA: Muthén & Muthén 2017. Muthén L, Muthén B. Mplus user’s guide. 8th ed: Los Angeles CA: Muthén & Muthén 2017.
46.
go back to reference Hessler J, Jahn T, Kurz A, Bickel H. The MWT-B as an estimator of premorbid intelligence in MCI and dementia. Z Neuropsychol. 2013;24:129–37.CrossRef Hessler J, Jahn T, Kurz A, Bickel H. The MWT-B as an estimator of premorbid intelligence in MCI and dementia. Z Neuropsychol. 2013;24:129–37.CrossRef
47.
go back to reference Flöel A, Witte a V, Lohmann H, Wersching H, Ringelstein EB, Berger K, et al. Lifestyle and memory in the elderly. Neuroepidemiology. 2008;31:39–47 [cited 2014 Mar 15].CrossRef Flöel A, Witte a V, Lohmann H, Wersching H, Ringelstein EB, Berger K, et al. Lifestyle and memory in the elderly. Neuroepidemiology. 2008;31:39–47 [cited 2014 Mar 15].CrossRef
48.
go back to reference Frey I, Berg A, Grathwohl D, Keul J. Freiburger Fragebogen zur kSrperlichen Aktivit it- Entwicklung, PriJfung und Anwendung. Soz Praventivmed. 1999;44:55–64.CrossRef Frey I, Berg A, Grathwohl D, Keul J. Freiburger Fragebogen zur kSrperlichen Aktivit it- Entwicklung, PriJfung und Anwendung. Soz Praventivmed. 1999;44:55–64.CrossRef
49.
go back to reference Hu LT, Bentler PM. Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Struct Equ Model. 1999;6:1–55.CrossRef Hu LT, Bentler PM. Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Struct Equ Model. 1999;6:1–55.CrossRef
50.
go back to reference Cook RD. Detection of influential observation in linear regression. Technometrics. 1977;19:15–8. Cook RD. Detection of influential observation in linear regression. Technometrics. 1977;19:15–8.
51.
go back to reference Klein A, Moosbrugger H. Maximum likelihood estimation of latent interaction effects with the LMS method. Psychometrika. 2000;65:457–74.CrossRef Klein A, Moosbrugger H. Maximum likelihood estimation of latent interaction effects with the LMS method. Psychometrika. 2000;65:457–74.CrossRef
52.
go back to reference Smith EE, Salat DH, Jeng J, McCreary CR, Fischl B, Schmahmann JD, et al. Correlations between MRI white matter lesion location and executive function and episodic memory. Neurology. 2011;76:1492–9.CrossRef Smith EE, Salat DH, Jeng J, McCreary CR, Fischl B, Schmahmann JD, et al. Correlations between MRI white matter lesion location and executive function and episodic memory. Neurology. 2011;76:1492–9.CrossRef
53.
go back to reference Gunning-Dixon FM, Raz N. The cognitive correlates of white matter abnormalities in normal aging: a quantitative review. Neuropsychology. 2000;14:224–32.CrossRef Gunning-Dixon FM, Raz N. The cognitive correlates of white matter abnormalities in normal aging: a quantitative review. Neuropsychology. 2000;14:224–32.CrossRef
54.
go back to reference Franzmeier N, Hartmann JC, Taylor ANW, Caballero MÁA, Simon-Vermot L, Buerger K, et al. Left frontal hub connectivity during memory performance supports reserve in aging and mild cognitive impairment. J Alzheimers Dis. 2017;59:1381–92.CrossRef Franzmeier N, Hartmann JC, Taylor ANW, Caballero MÁA, Simon-Vermot L, Buerger K, et al. Left frontal hub connectivity during memory performance supports reserve in aging and mild cognitive impairment. J Alzheimers Dis. 2017;59:1381–92.CrossRef
55.
go back to reference Franzmeier N, Düzel E, Jessen F, Buerger K, Levin J, Duering M, et al. Left frontal hub connectivity delays cognitive impairment in autosomal-dominant and sporadic Alzheimer’s disease. Brain. 2018;141:1186–200. Franzmeier N, Düzel E, Jessen F, Buerger K, Levin J, Duering M, et al. Left frontal hub connectivity delays cognitive impairment in autosomal-dominant and sporadic Alzheimer’s disease. Brain. 2018;141:1186–200.
56.
go back to reference Arenaza-Urquijo EM, Wirth M, Chételat G. Cognitive reserve and lifestyle: moving towards preclinical Alzheimer’s disease. Front Aging Neurosci. 2015;7:134.CrossRef Arenaza-Urquijo EM, Wirth M, Chételat G. Cognitive reserve and lifestyle: moving towards preclinical Alzheimer’s disease. Front Aging Neurosci. 2015;7:134.CrossRef
57.
go back to reference Menon V, Uddin LQ. Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct. 2010;214:655–67.CrossRef Menon V, Uddin LQ. Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct. 2010;214:655–67.CrossRef
58.
go back to reference Liu J, Xia M, Dai Z, Wang X, Liao X, Bi Y, et al. Intrinsic brain hub connectivity underlies individual differences in spatial working memory. Cereb Cortex. 2017;27:5496–508. Liu J, Xia M, Dai Z, Wang X, Liao X, Bi Y, et al. Intrinsic brain hub connectivity underlies individual differences in spatial working memory. Cereb Cortex. 2017;27:5496–508.
59.
go back to reference Pinter D, Enzinger C, Fazekas F. Cerebral small vessel disease, cognitive reserve and cognitive dysfunction. J Neurol. 2015;262:2411–9.CrossRef Pinter D, Enzinger C, Fazekas F. Cerebral small vessel disease, cognitive reserve and cognitive dysfunction. J Neurol. 2015;262:2411–9.CrossRef
60.
go back to reference Arenaza-Urquijo EM, Vemuri P. Resistance vs resilience to Alzheimer disease. Neurol Int. 2018;90:695–703. Arenaza-Urquijo EM, Vemuri P. Resistance vs resilience to Alzheimer disease. Neurol Int. 2018;90:695–703.
61.
go back to reference Antonenko D, Külzow N, Sousa A, Prehn K, Grittner U, Flöel A. Neuronal and behavioral effects of multi-day brain stimulation and memory training. Neurobiol Aging. 2018;61:245–54.CrossRef Antonenko D, Külzow N, Sousa A, Prehn K, Grittner U, Flöel A. Neuronal and behavioral effects of multi-day brain stimulation and memory training. Neurobiol Aging. 2018;61:245–54.CrossRef
62.
go back to reference Meinzer M, Lindenberg R, Phan MT, Ulm L, Volk C, Flöel A. Transcranial direct current stimulation in mild cognitive impairment: behavioral effects and neural mechanisms. Alzheimers Dement. 2015;11:1032–40.CrossRef Meinzer M, Lindenberg R, Phan MT, Ulm L, Volk C, Flöel A. Transcranial direct current stimulation in mild cognitive impairment: behavioral effects and neural mechanisms. Alzheimers Dement. 2015;11:1032–40.CrossRef
63.
go back to reference Passow S, Thurm F, Li SC. Activating developmental reserve capacity via cognitive training or non-invasive brain stimulation: potentials for promoting fronto-parietal and hippocampal-striatal network functions in old age. Front Aging Neurosci. 2017;9:33. Passow S, Thurm F, Li SC. Activating developmental reserve capacity via cognitive training or non-invasive brain stimulation: potentials for promoting fronto-parietal and hippocampal-striatal network functions in old age. Front Aging Neurosci. 2017;9:33.
64.
go back to reference Bullmore E, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci. 2009;10:186–98.CrossRef Bullmore E, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci. 2009;10:186–98.CrossRef
65.
go back to reference Taylor ANW, Kambeitz-Ilankovic L, Gesierich B, Simon-Vermot L, Franzmeier N, Araque Caballero M, et al. Tract-specific white matter hyperintensities disrupt neural network function in Alzheimer’s disease. Alzheimer’s Dement. 2017;13:225–35. Taylor ANW, Kambeitz-Ilankovic L, Gesierich B, Simon-Vermot L, Franzmeier N, Araque Caballero M, et al. Tract-specific white matter hyperintensities disrupt neural network function in Alzheimer’s disease. Alzheimer’s Dement. 2017;13:225–35.
Metadata
Title
Functional connectivity in cognitive control networks mitigates the impact of white matter lesions in the elderly
Authors
Gloria Benson
Andrea Hildebrandt
Catharina Lange
Claudia Schwarz
Theresa Köbe
Werner Sommer
Agnes Flöel
Miranka Wirth
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Alzheimer's Research & Therapy / Issue 1/2018
Electronic ISSN: 1758-9193
DOI
https://doi.org/10.1186/s13195-018-0434-3

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