Alzheimer’s disease; cognition; cognitive reserve; functional MRI; intrinsic network connectivity; resting-state functional connectivity; Humans; Cognition; Neural Pathways; Nerve Net; Magnetic Resonance Imaging; Brain/diagnostic imaging; Alzheimer Disease/pathology; Cognitive Reserve; Brain; Neuroscience (all); Clinical Psychology; Geriatrics and Gerontology; Psychiatry and Mental Health; General Medicine; General Neuroscience
Abstract :
[en] BACKGROUND: Cognitive reserve (CR) explains inter-individual differences in the impact of the neurodegenerative burden on cognitive functioning. A residual model was proposed to estimate CR more accurately than previous measures. However, associations between residual CR markers (CRM) and functional connectivity (FC) remain unexplored.
OBJECTIVE: To explore the associations between the CRM and intrinsic network connectivity (INC) in resting-state networks along the neuropathological-continuum of Alzheimer's disease (ADN).
METHODS: Three hundred eighteen participants from the DELCODE cohort were stratified using cerebrospinal fluid biomarkers according to the A(myloid-β)/T(au)/N(eurodegeneration) classification. CRM was calculated utilizing residuals obtained from a multilinear regression model predicting cognition from markers of disease burden. Using an independent component analysis in resting-state fMRI data, we measured INC of resting-state networks, i.e., default mode network (DMN), frontoparietal network (FPN), salience network (SAL), and dorsal attention network. The associations of INC with a composite memory score and CRM and the associations of CRM with the seed-to-voxel functional connectivity of memory-related were tested in general linear models.
RESULTS: CRM was positively associated with INC in the DMN in the entire cohort. The A+T+N+ group revealed an anti-correlation between the SAL and the DMN. Furthermore, CRM was positively associated with anti-correlation between memory-related regions in FPN and DMN in ADN and A+T/N+.
CONCLUSION: Our results provide evidence that INC is associated with CRM in ADN defined as participants with amyloid pathology with or without cognitive symptoms, suggesting that the neural correlates of CR are mirrored in network FC in resting-state.
Disciplines :
Neurology
Author, co-author :
Ersoezlue, Ersin ✱; Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Germany ; Department of Gerontopsychiatry and Developmental Disorders, kbo-Isar-Amper-Klinikum Haar, University Teaching Hospital of LMU Munich, Germany
Perneczky, Robert ✱; Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Germany ; German Center for Neurodegenerative Diseases (DZNE) Munich, Germany ; Ageing Epidemiology (AGE) Research Unit, School of Public Health, Imperial College, London, UK ; Munich Cluster for Systems Neurology (SyNergy), Munich, Germany ; Sheffield Institute for Translational Neurology (SITraN), University of Sheffield, Sheffield, UK
Tato, Maia; Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Germany
Utecht, Julia; Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Germany
Kurz, Carolin; Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Germany
Häckert, Jan; Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Germany
Guersel, Selim; Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Germany
Burow, Lena; Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Germany
Koller, Gabriele; Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Germany
Stoecklein, Sophia; Department of Radiology, University Hospital, LMU Munich, Germany
Keeser, Daniel; Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Germany
Papazov, Boris; Department of Radiology, University Hospital, LMU Munich, Germany
Totzke, Marie; Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Germany
Ballarini, Tommaso; German Center for Neurodegenerative Diseases (DZNE) Bonn, Germany
Brosseron, Frederic; German Center for Neurodegenerative Diseases (DZNE) Bonn, Germany
Buerger, Katharina; German Center for Neurodegenerative Diseases (DZNE Munich), Munich, Germany ; Institute for Stroke and Dementia Research (ISD), University Hospital LMU Munich, Germany
Dechent, Peter; MR-Research in Neurosciences Department of Cognitive Neurology, Georg-August-University Goettingen, Germany
Dobisch, Laura; German Center for Neurodegenerative Diseases (DZNE) Magdeburg, Germany ; Institute of Cognitive Neurology and Dementia Research (IKND), Otto-von-Guericke University Magdeburg, Germany
Ewers, Michael; German Center for Neurodegenerative Diseases (DZNE Munich), Munich, Germany ; Institute for Stroke and Dementia Research (ISD), University Hospital LMU Munich, Germany
Fliessbach, Klaus; German Center for Neurodegenerative Diseases (DZNE) Bonn, Germany ; Medical Center of Neurodegenerative Disease and Geriatric Psychiatry, University of Bonn, Germany
Glanz, Wenzel; German Center for Neurodegenerative Diseases (DZNE) Magdeburg, Germany
Haynes, John Dylan; Bernstein Center for Computational Neuroscience Charité - Universitätsmedizin Berlin, Germany
HENEKA, Michael ; German Center for Neurodegenerative Diseases (DZNE) Bonn, Germany ; Medical Center of Neurodegenerative Disease and Geriatric Psychiatry, University of Bonn, Germany
Janowitz, Daniel; Institute for Stroke and Dementia Research (ISD), University Hospital LMU Munich, Germany
Kilimann, Ingo; German Center for Neurodegenerative Diseases (DZNE) Rostock, Germany ; Department of Psychosomatic Medicine, Rostock University Medical Center, Rostock, Germany
Kleineidam, Luca; German Center for Neurodegenerative Diseases (DZNE) Bonn, Germany
Laske, Christoph; German Center for Neurodegenerative Diseases (DZNE) Tübingen, Germany ; Section for Dementia Research, Hertie Institute for Clinical Brain Research and Department of Psychiatry and Psychotherapy, University of Tübingen, Germany
Maier, Franziska; Department of Psychiatry, Medical Faculty of University of Cologne, Germany
Munk, Matthias H; German Center for Neurodegenerative Diseases (DZNE) Tübingen, Germany ; Section for Dementia Research, Hertie Institute for Clinical Brain Research and Department of Psychiatry and Psychotherapy, University of Tübingen, Germany
Peters, Oliver; Department of Psychiatry, Campus Benjamin Franklin, Charité-Universitätsmedizin Berlin, Germany ; German Center for Neurodegenerative Diseases (DZNE) Berlin, Germany
Priller, Josef; Department of Psychiatry and Psychotherapy, Charité Berlin, Germany ; Department of Psychiatry and Psychotherapy, School of Medicine Technical University of Munich, Germany ; University of Edinburgh and UK DRI Edinburgh, UK
Ramirez, Alfredo; German Center for Neurodegenerative Diseases (DZNE) Bonn, Germany ; Medical Center of Neurodegenerative Disease and Geriatric Psychiatry, University of Bonn, Germany ; Division of Neurogenetics and Molecular Psychiatry, Department of Psychiatry and Psychotherapy, Faculty of Medicine and University Hospital Cologne, Germany ; Department of Psychiatry & Glenn Biggs Institute for Alzheimer's and Neurodegenerative Diseases, San Antonio, TX, USA
Roeske, Sandra; German Center for Neurodegenerative Diseases (DZNE) Bonn, Germany
Roy, Nina; German Center for Neurodegenerative Diseases (DZNE) Bonn, Germany
Scheffler, Klaus; Department for Biomedical Magnetic Resonance, University of Tübingen, Germany
Schneider, Anja; German Center for Neurodegenerative Diseases (DZNE) Bonn, Germany ; Medical Center of Neurodegenerative Disease and Geriatric Psychiatry, University of Bonn, Germany
Schott, Björn H; German Center for Neurodegenerative Diseases (DZNE) Goettingen, Germany ; Department of Psychiatry and Psychotherapy, University Medical Center Goettingen, University of Goettingen, Germany ; Leibniz Institute for Neurobiology, Magdeburg, Germany
Spottke, Annika; German Center for Neurodegenerative Diseases (DZNE) Bonn, Germany ; Department of Neurology, University of Bonn, Germany
Spruth, Eike J; German Center for Neurodegenerative Diseases (DZNE) Berlin, Germany ; Department of Psychiatry and Psychotherapy, Charité Berlin, Germany
Teipel, Stefan; German Center for Neurodegenerative Diseases (DZNE) Rostock, Germany ; Department of Psychosomatic Medicine, Rostock University Medical Center, Rostock, Germany
Unterfeld, Chantal; Department of Psychiatry, Campus Benjamin Franklin, Charité-Universitätsmedizin Berlin, Germany
Wagner, Michael; German Center for Neurodegenerative Diseases (DZNE) Bonn, Germany ; Medical Center of Neurodegenerative Disease and Geriatric Psychiatry, University of Bonn, Germany
Wang, Xiao; Department of Psychiatry, Campus Benjamin Franklin, Charité-Universitätsmedizin Berlin, Germany
Wiltfang, Jens; German Center for Neurodegenerative Diseases (DZNE) Goettingen, Germany ; Department of Psychiatry and Psychotherapy, University Medical Center Goettingen, University of Goettingen, Germany ; Neurosciences and Signaling Group, Institute of Biomedicine (iBiMED), Department of Medical Sciences, University of Aveiro, Portugal
Wolfsgruber, Steffen; German Center for Neurodegenerative Diseases (DZNE) Bonn, Germany ; Medical Center of Neurodegenerative Disease and Geriatric Psychiatry, University of Bonn, Germany
Yakupov, Renat; German Center for Neurodegenerative Diseases (DZNE) Magdeburg, Germany
Duezel, Emrah; German Center for Neurodegenerative Diseases (DZNE) Magdeburg, Germany ; Institute of Cognitive Neurology and Dementia Research (IKND), Otto-von-Guericke University Magdeburg, Germany
Jessen, Frank; German Center for Neurodegenerative Diseases (DZNE) Bonn, Germany ; Department of Psychiatry, Medical Faculty of University of Cologne, Germany ; Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD) University of Cologne, Germany
Rauchmann, Boris-Stephan; Department of Psychiatry and Psychotherapy, University Hospital, LMU Munich, Germany ; German Center for Neurodegenerative Diseases (DZNE) Munich, Germany ; Sheffield Institute for Translational Neurology (SITraN), University of Sheffield, Sheffield, UK ; Department of Neuroradiology, University Hospital, LMU Munich, Germany
The DZNE-Longitudinal Cognitive Impairment and Dementia Study (DELCODE) study was funded by the German Center for Neurodegenerative Diseases (Deutsches Zentrum für Neurodegenerative Erkrankungen, DZNE), reference number BN012.
Perneczky R, Drzezga A, Diehl-Schmid J, Schmid G, Wohlschläger A, Kars S, Grimmer T, Wagenpfeil S, Monsch A, Kurz A (2006) Schooling mediates brain reserve in Alzheimer's disease: Findings of fluoro-deoxyglucose-positron emission tomography. J Neurol Neurosurg Psychiatry 77, 1060-1063.
Stern Y, Arenaza-Urquijo EM, Bartrés-Faz D, Belleville S, Cantilon M, Chetelat G, Ewers M, Franzmeier N, Kempermann G, Kremen WS, Okonkwo O, Scarmeas N, Soldan A, Udeh-Momoh C,Valenzuela M,Vemuri P,Vuoksimaa E, the Reserve, Resilience and Protective Factors PIA Empirical Definitions and Conceptual FrameworksWorkgroup (2020) Whitepaper: Defining and investigating cognitive reserve, brain reserve, and brain maintenance. Alzheimers Dement 16, 1305-1311.
Guo L-H, Alexopoulos P,Wagenpfeil S, Kurz A, Perneczky R, Alzheimer's Disease Neuroimaging Initiative (2013) Brain size and the compensation of Alzheimer's disease symptoms: A longitudinal cohort study. Alzheimers Dement 9, 580-586.
Perneczky R, Häussermann P, Drzezga A, Boecker H, Granert O, Feurer R, Förstl H, Kurz A (2009) Fluorodeoxy-glucose positron emission tomography correlates of impaired activities of daily living in dementia with Lewy bodies: Implications for cognitive reserve. Am J Geriatr Psychiatry 17, 188-195.
Spreng RN, Drzezga A, Diehl-Schmid J, Kurz A, Levine B, Perneczky R (2011) Relationship between occupation attributes and brain metabolism in frontotemporal dementia. Neuropsychologia 49, 3699-3703.
Chapko D, McCormack R, Black C, Staff R, Murray A (2018) Life-course determinants of cognitive reserve (CR) in cognitive aging and dementia-a systematic literature review. Aging Ment Health 22, 915-926.
Lee DH, Lee P, Seo SW, Roh JH, Oh M, Oh JS, Oh SJ, Kim JS, Jeong Y (2019) Neural substrates of cognitive reserve in Alzheimer's disease spectrum and normal aging. Neuroimage 186, 690-702.
Marques P, Moreira P, Magalhães R, Costa P, Santos N, Zihl J, Soares J, Sousa N (2016) The functional connectome of cognitive reserve. Hum Brain Mapp 37, 3310-3322.
Beyer L, Schnabel J, Kazmierczak P, Ewers M, Schönecker S, Prix C, Meyer-Wilmes J, Unterrainer M, Catak C, Pogarell O, Perneczky R, Albert NL, Bartenstein P, Danek A, Buerger K, Levin J, Rominger A, Brendel M (2019) Neuronal injury biomarkers for assessment of the individual cognitive reserve in clinically suspected Alzheimer's disease. Neuroimage Clin 24, 101949.
Reed BR, Mungas D, Farias ST, Harvey D, Beckett L, Widaman K, Hinton L, DeCarli C (2010) Measuring cognitive reserve based on the decomposition of episodic memory variance. Brain 133, 2196-2209.
van Loenhoud AC, van der Flier WM, Wink AM, Dicks E, Groot C, Twisk J, Barkhof F, Scheltens P, Ossenkoppele R, Alzheimer's Disease Neuroimaging Initiative (2019) Cognitive reserve and clinical progression in Alzheimer disease: A paradoxical relationship. Neurology 93, e334-e346.
Brier MR, Thomas JB, Snyder AZ, Benzinger TL, Zhang D, Raichle ME, Holtzman DM, Morris JC, Ances BM (2012) Loss of intranetwork and internetwork resting state functional connections with Alzheimer's disease progression. J Neurosci 32, 8890-8899.
Greicius MD, Srivastava G, Reiss AL, Menon V (2004) Default-mode network activity distinguishes Alzheimer's disease from healthy aging: Evidence from functional MRI. Proc Natl Acad Sci U S A 101, 4637-4642.
Smallwood J, Bernhardt BC, Leech R, Bzdok D, Jefferies E, Margulies DS (2021) The default mode network in cognition: A topographical perspective. Nat Rev Neurosci 22, 503-513.
Chhatwal JP, Schultz AP, Johnson KA, Hedden T, Jaimes S, Benzinger TLS, Jack C Jr, Ances BM, Ringman JM, Marcus DS, Ghetti B, Farlow MR, Danek A, Levin J, Yakushev I, Laske C, Koeppe RA, Galasko DR, Xiong C, Masters CL, Schofield PR, Kinnunen KM, Salloway S, Martins RN, McDade E, Cairns NJ, Buckles VD, Morris JC, Bateman R, Sperling RA, Dominantly Inherited Alzheimer Network (2018) Preferential degradation of cognitive networks differentiates Alzheimer's disease from ageing. Brain 141, 1486-1500.
He X, Qin W, Liu Y, Zhang X, Duan Y, Song J, Li K, Jiang T, Yu C (2014) Abnormal salience network in normal aging and in amnestic mild cognitive impairment and Alzheimer's disease. Hum Brain Mapp 35, 3446-3464.
Weiler M, de Campos BM, Teixeira CV de L, Casseb RF, Carletti-Cassani AFMK, Vicentini JE, Magalhães TNC, Talib LL, Forlenza OV, Balthazar MLF (2017) Intranetwork and internetwork connectivity in patients with Alzheimer disease and the association with cerebrospinal fluid biomarker levels. J Psychiatry Neurosci 42, 366-377.
Li R, Wu X, Fleisher AS, Reiman EM, Chen K, Yao L (2012) Attention-related networks in Alzheimer's disease: A resting functional MRI study. Hum Brain Mapp 33, 1076-1088.
Mutlu J, Landeau B, Gaubert M, de La Sayette V, Desgranges B, Chételat G (2017) Distinct influence of specific versus global connectivity on the different Alzheimer's disease biomarkers. Brain 140, 3317-3328.
Zhou J, Greicius MD, Gennatas ED, Growdon ME, Jang JY, Rabinovici GD, Kramer JH, Weiner M, Miller BL, Seeley WW (2010) Divergent network connectivity changes in behavioural variant frontotemporal dementia and Alzheimer's disease. Brain 133, 1352-1367.
Perneczky R, Kempermann G, Korczyn AD, Matthews FE, Ikram MA, Scarmeas N, Chetelat G, Stern Y, Ewers M (2019) Translational research on reserve against neurodegenerative disease: Consensus report of the International Conference on Cognitive Reserve in the Dementias and the Alzheimer's Association Reserve, Resilience and Protective Factors Professional Interest Area working groups. BMC Med 17, 47.
Bozzali M, Dowling C, Serra L, SpanoB, Torso M, Marra C, Castelli D, Dowell NG, Koch G, Caltagirone C, Cercignani M (2015) The impact of cognitive reserve on brain functional connectivity in Alzheimer's disease. J Alzheimers Dis 44, 243-250.
Arenaza-Urquijo EM, Landeau B, La Joie R, Mevel K, Mézenge F, Perrotin A, Desgranges B, Bartrés-Faz D, Eustache F, Chételat G (2013) Relationships between years of education and gray matter volume, metabolism and functional connectivity in healthy elders. Neuroimage 83, 450-457.
Perry A, Wen W, Kochan NA, Thalamuthu A, Sachdev PS, Breakspear M (2017) The independent influences of age and education on functional brain networks and cognition in healthy older adults. Hum Brain Mapp 38, 5094-5114.
Bastin C, Yakushev I, Bahri MA, Fellgiebel A, Eustache F, Landeau B, Scheurich A, Feyers D, Collette F, Chételat G, Salmon E (2012) Cognitive reserve impacts on interindividual variability in resting-state cerebral metabolism in normal aging. Neuroimage 63, 713-722.
Franzmeier N, Gottler J, Grimmer T, Drzezga A, Araque-Caballero MA, Simon-Vermot L, Taylor ANW, Bürger K, Catak C, Janowitz D, Müller C, Duering M, Sorg C, Ewers M(2017) Resting-state connectivity of the left frontal cortex to the default mode and dorsal attention network supports reserve in mild cognitive impairment. Front Aging Neurosci 9, 264.
Franzmeier N, Düzel E, Jessen F, Buerger K, Levin J, Duering M, Dichgans M, Haass C, Suárez-Calvet M, Fagan AM, Paumier K, Benzinger T, Masters CL, Morris JC, Perneczky R, Janowitz D, Catak C, Wolfsgruber S, Wagner M, Teipel S, Kilimann I, Ramirez A, Rossor M, Jucker M, Chhatwal J, Spottke A, Boecker H, Brosseron F, Falkai P, Fliessbach K, Heneka MT, Laske C, Nestor P, Peters O, Fuentes M, Menne F, Priller J, Spruth EJ, Franke C, Schneider A, Kofler B,Westerteicher C, Speck O,Wiltfang J, Bartels C, Araque Caballero MA, Metzger C, Bittner D, Weiner M, Lee J-H, Salloway S, Danek A, Goate A, Schofield PR, Bateman RJ, Ewers M (2018) Left frontal hub connectivity delays cognitive impairment in autosomaldominant and sporadic Alzheimer's disease. Brain 141, 1186-1200.
Neitzel J, Franzmeier N, Rubinski A, Ewers M, Alzheimer's Disease Neuroimaging Initiative (ADNI) (2019) Left frontal connectivity attenuates the adverse effect of entorhinal tau pathology on memory. Neurology 93, e347-e357.
Calhoun VD, Eichele T, Adali T, Allen EA (2012) Decomposing the brain: Components and modes, networks and nodes. Trends Cogn Sci 16, 255-256.
Jack CR Jr, Bennett DA, Blennow K, Carrillo MC, Dunn B, Haeberlein SB, Holtzman DM, JagustW, Jessen F, Karlawish J, Liu E, Molinuevo JL, Montine T, Phelps C, Rankin KP, Rowe CC, Scheltens P, Siemers E, Snyder HM, Sperling R, Contributors (2018)NIA-AAResearch Framework:Toward a biological definition of Alzheimer's disease. Alzheimers Dement 14, 535-562.
Palmqvist S, Schöll M, Strandberg O, Mattsson N, Stomrud E, Zetterberg H, Blennow K, Landau S, Jagust W, Hansson O (2017) Earliest accumulation of-amyloid occurs within the default-mode network and concurrently affects brain connectivity. Nat Commun 8, 1214.
Bocancea DI, van Loenhoud AC, Groot C, Barkhof F, van der Flier WM, Ossenkoppele R (2021) Measuring resilience and resistance in aging and Alzheimer disease using residual methods:Asystematic reviewand meta-analysis. Neurology 97, 474-488.
Jessen F, Spottke A, Boecker H, Brosseron F, Buerger K, Catak C, Fliessbach K, Franke C, Fuentes M, Heneka MT, Janowitz D, Kilimann I, Laske C, Menne F, Nestor P, Peters O, Priller J, Pross V, Ramirez A, Schneider A, Speck O, Spruth EJ, Teipel S, Vukovich R,Westerteicher C,Wiltfang J, Wolfsgruber S, Wagner M, Düzel E (2018) Design and first baseline data of the DZNE multicenter observational study on predementia Alzheimer's disease (DELCODE). Alzheimers Res Ther 10, 15.
Jack CR Jr, Bennett DA, Blennow K, Carrillo MC, Feldman HH, Frisoni GB, Hampel H, Jagust WJ, Johnson KA, Knopman DS, Petersen RC, Scheltens P, Sperling RA, Dubois B (2016) A/T/N: An unbiased descriptive classification scheme for Alzheimer disease biomarkers. Neurology 87, 539-547.
Jessen F, Wolfsgruber S, Kleineindam L, Spottke A, Altenstein S, Bartels C, Berger M, Brosseron F, Daamen M, Dichgans M, Dobisch L, Ewers M, Fenski F, Fliessbach K, Freiesleben SD, Glanz W, Görß D, Gürsel S, Janowitz D, Kilimann I, Kobeleva X, Lohse A, Maier F, Metzger C, Munk M, Preis L, Sanzenbacher C, Spruth E, Rauchmann B, Vukovich R, Yakupov R, Weyrauch A-S, Ziegler G, Schmid M, Laske C, Perneczky R, Schneider A, Wiltfang J, Teipel S, Bürger K, Priller J, Peters O, Ramirez A, Boecker H, Heneka MT, Wagner M, Düzel E (2022) Subjective cognitive decline and stage 2 of Alzheimer disease in patients from memory centers. Alzheimers Dement. doi: 10.1002/alz.12674.
Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron 33, 341-355.
Pettigrew C, Soldan A (2019) Defining cognitive reserve and implications for cognitive aging. Curr Neurol Neurosci Rep 19, 1.
Behzadi Y, Restom K, Liau J, Liu TT (2007) A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage 37, 90-101.
Friston KJ,Williams S,Howard R, Frackowiak RS,TurnerR (1996)Movement-related effects in fMRI time-series.Magn Reson Med 35, 346-355.
Power JD, Mitra A, Laumann TO, Snyder AZ, Schlaggar BL, Petersen SE (2014) Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage 84, 320-341.
Chai XJ, Castanõn AN, Ongur D, Whitfield-Gabrieli S (2012) Anticorrelations in resting state networks without global signal regression. Neuroimage 59, 1420-1428.
Ciric R,Wolf DH, Power JD, Roalf DR, Baum GL, Ruparel K, Shinohara RT, Elliott MA, Eickhoff SB, Davatzikos C, Gur RC, Gur RE, Bassett DS, Satterthwaite TD (2017) Benchmarking of participant-level confound regression strategies for the control of motion artifact in studies of functional connectivity. Neuroimage 154, 174-187.
Wolfsgruber S, Kleineidam L, Guski J, Polcher A, Frommann I, Roeske S, Spruth EJ, Franke C, Priller J, Kilimann I, Teipel S, Buerger K, Janowitz D, Laske C, Buchmann M, Peters O, Menne F, Fuentes Casan M, Wiltfang J, Bartels C, Düzel E, Metzger C, Glanz W, Thelen M, Spottke A, Ramirez A, Kofler B, Fließbach K, Schneider A, Heneka MT, Brosseron F, Meiberth D, Jessen F, Wagner M, DELCODE Study Group (2020) Minor neuropsychological deficits in patients with subjective cognitive decline. Neurology 95, e1134-e1143.
Roeske S, Wolfsgruber S, Kleineidam L, Zulka L, Buerger K, Ewers M, LaskeC, Nestor P, Peters O, Priller J, Schneider A, Spottke A, Ramirez A, Heneka M, Teipel SJ, Wiltfang J, Okonkwo OC, Kalbe E, Düzel E, Jessen F, Wagner M, DELCODE Study Group (2018) P3-591:AGerman version of the lifetime of experiences questionnaire (leq) to measure cognitive reserve: Validation results from the delcode study. Alzheimers Dement 14, P1352-P1353.
Valenzuela MJ, Sachdev P (2007) Assessment of complex mental activity across the lifespan: Development of the Lifetime of Experiences Questionnaire (LEQ). Psychol Med 37, 1015-1025.
Nieto-Castanon A (2020) Handbook of functional connectivity Magnetic Resonance Imaging methods in CONN, Hilbert Press.
Calhoun VD, Adali T, Pearlson GD, Pekar JJ (2001) A method for making group inferences from functional MRI data using independent component analysis. Hum Brain Mapp 14, 140-151.
Mondragón JD, Maurits NM, De Deyn PP, Alzheimer's Disease Neuroimaging Initiative (2021) Functional connectivity differences in Alzheimer's disease and amnestic mild cognitive impairment associated with AT(N) classification and anosognosia. Neurobiol Aging 101, 22-39.
Erhardt EB, Rachakonda S, Bedrick EJ, Allen EA, Adali T, Calhoun VD (2011) Comparison of multi-subject ICA methods for analysis of fMRI data. Hum Brain Mapp 32, 2075-2095.
Amaefule CO, Dyrba M,Wolfsgruber S, Polcher A, Schneider A, Fliessbach K, Spottke A, Meiberth D, Preis L, Peters O, Incesoy EI, Spruth EJ, Priller J, Altenstein S, Bartels C, Wiltfang J, Janowitz D, Bürger K, Laske C, Munk M, Rudolph J, GlanzW, Dobisch L, Haynes JD, Dechent P, Ertl-Wagner B, Scheffler K, Kilimann I, Düzel E, Metzger CD, Wagner M, Jessen F, Teipel SJ (2021) Association between composite scores of domain-specific cognitive functions and regional patterns of atrophy and functional connectivity in the Alzheimer's disease spectrum. Neuroimage Clin 29, 102533.
Makris N, Goldstein JM, Kennedy D, Hodge SM, Caviness VS, Faraone SV, TsuangMT, Seidman LJ (2006) Decreased volume of left and total anterior insular lobule in schizophrenia. Schizophr Res 83, 155-171.
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc 57, 289-300.
Worsley KJ (1996) The geometry of random images. Chance (N Y) 9, 27-40.
Franzmeier N, Duering M, Weiner M, Dichgans M, Ewers M, Alzheimer's Disease Neuroimaging Initiative (ADNI) (2017) Left frontal cortex connectivity underlies cognitive reserve in prodromal Alzheimer disease. Neurology 88, 1054-1061.
Dennis EL, Thompson PM (2014) Functional brain connectivity using fMRI in aging and Alzheimer's disease. Neuropsychol Rev 24, 49-62.
Weiler M, Casseb RF, de Campos BM, de Ligo Teixeira CV, Carletti-CassaniAFMK,Vicentini JE, Magalhães TNC, de Almeira DQ, Talib LL, Forlenza OV, Balthazar MLF, Castellano G (2018) Cognitive reserve relates to functional network efficiency in Alzheimer's disease.Front Aging Neurosci 10, 255.
Serra L, Mancini M, Cercignani M, Di Domenico C, Spano B, Giulietti G, Koch G, Marra C, Bozzali M (2017) Network-based substrate of cognitive reserve in Alzheimer's disease. J Alzheimers Dis 55, 421-430.
Byun J-I, Kim H-W, Kang H, Cha KS, Sunwoo J-S, Shin JW, Moon J, Lee S-T, Jung K-H, Chu K, Kim M, Shin WC, Lee DS, Schenck CH, Lee SK, Jung K-Y (2020) Altered resting-state thalamo-occipital functional connectivity is associated with cognition in isolated rapid eye movement sleep behavior disorder. Sleep Med 69, 198-203.
Ersoezlue E, Rauchmann B-S, Schneider-Axmann T, Wagner M, Ballarini T, Tato M, Utecht J, Kurz C, Papazov B, Guersel S, Burow L, Koller G, Stöcklein S, Keeser D, Bartels C, Brosseron F, Buerger K, Cetindag AC, Dechent P, Dobisch L, Ewers M, Fliessbach K, Frommann I, Haynes JD, Heneka MT, Janowitz D, Kilimann I, Kleinedam L, Laske C, Maier F, Metzger CD, Munk MH, Peters O, Preis L, Priller J, Ramirez A, Roeske S, Roy N, Scheffler K, Schneider A, Spottke A, Spruth EJ, Teipel S, Wiltfang J, Wolfsgruber S, Yakupov R, Duezel E, Jessen F, Perneczky R (2023) Lifelong experiences as a proxy of cognitive reserve moderate the association between connectivity and cognition in Alzheimer's disease. Neurobiol Aging 122, 33-44.
Ruan J, Bludau S, Palomero-Gallagher N, Caspers S, Mohlberg H, Eickhoff SB, Seitz RJ, Amunts K (2018) Cytoarchitecture, probability maps, and functions of the human supplementary and pre-supplementary motor areas. Brain Struct Funct 223, 4169-4186.
Krienen FM, Tu P-C, Buckner RL (2010) Clan mentality: Evidence that the medial prefrontal cortex responds to close others. J Neurosci 30, 13906-13915.
Lin F, Heffner KL, Ren P, Tivarus ME, Brasch J, Chen D-G, Mapstone M, Porsteinsson AP, Tadin D (2016) Cognitive and neural effects of vision-based speed-of-processing training in older adults with amnestic mild cognitive impairment: A pilot study. J Am Geriatr Soc 64, 1293-1298.
Fox MD, Buckner RL, Liu H, Chakravarty MM, Lozano AM, Pascual-Leone A (2014) Resting-state networks link invasive and noninvasive brain stimulation across diverse psychiatric and neurological diseases. Proc Natl Acad Sci U S A 111, E4367-E4375.
Beisteiner R, Matt E, Fan C, Baldysiak H, Schönfeld M, Philippi Novak T, Amini A, Aslan T, Reinecke R, Lehrner J, Weber A, Reime U, Goldenstedt C, Marlinghaus E, Hallett M, Lohse-Busch H (2020) Transcranial pulse stimulation with ultrasound in Alzheimer's disease-A new navigated focal brain therapy. Adv Sci 7, 1902583.
