Structural and functional brain connectivity in presymptomatic familial frontotemporal dementia

Dopper, Elise G.P.; Rombouts, Serge A.R.B.; Jiskoot, Lize C.; den Heijer, Tom; de Graaf, J. Roos A.; de Koning, Inge; Hammerschlag, Anke R.; Seelaar, Harro; Seeley, William W.; Veer, Ilya M.; van Buchem, Mark A.; Rizzu, Patrizia; van Swieten, John C.

doi:10.1212/wnl.0000000000000583

Cited by 152Dementia and Cognitive Impairment ResearchFunctional Brain Connectivity StudiesAmyotrophic Lateral Sclerosis Research

Structural and functional brain connectivity in presymptomatic familial frontotemporal dementia

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Dopper, Elise G.P., Rombouts, Serge A.R.B., Jiskoot, Lize C., den Heijer, Tom, de Graaf, J. Roos A., de Koning, Inge, Hammerschlag, Anke R., Seelaar, Harro +5 more·2014·Neurology

DOI 10.1212/wnl.0000000000000583

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Abstract

Objective: We aimed to investigate whether cognitive deficits and structural and functional connectivity changes can be detected before symptom onset in a large cohort of carriers of MAPT (microtubule-associated protein tau) or GRN (progranulin) mutations. Methods: In this case-control study, 75 healthy individuals (aged 20–70 years) with 50% risk of frontotemporal dementia (FTD) underwent DNA screening, neuropsychological assessment, structural MRI, and fMRI. We used voxel-based morphometry and tract-based spatial statistics for voxel-wise analyses of gray matter volume and diffusion tensor imaging measures. Using resting-state fMRI scans, we assessed whole-brain functional connectivity to frontoinsular, anterior midcingulate, and posterior cingulate cortices. Results: Carriers (n = 39) and noncarriers (n = 36) had similar neuropsychological performance, except for lower Letter Digit Substitution Test scores in carriers. Worse performance on Stroop III, Rivermead Behavioral Memory Test, and Happé Cartoons correlated with higher age in carriers, but not controls. Reduced fractional anisotropy in the right uncinate fasciculus was found in carriers compared with controls. Reductions in functional connectivity between anterior midcingulate cortex and frontoinsula and several other brain regions were found in carriers compared with controls and correlated with higher age in carriers, but not controls. We found no significant differences or age correlations in posterior cingulate cortex connectivity. No differences in regional gray matter volume were found, except for a small cluster of higher volume in the precentral gyrus in carriers. Conclusions: This study demonstrates that alterations in structural and functional connectivity develop before the first symptoms of FTD arise. These findings suggest that diffusion tensor imaging and resting-state fMRI may have the potential to become sensitive biomarkers for early FTD in future clinical trials.

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Functional ROI-to-ROI models showed alterations in fronto-temporal, intrafrontal, and precuneus-insula connectivity.
“In line with previous studies, the functional ROI-to-ROI models showed alterations in fronto-temporal (Jastorff et al., 2016; Meijboom et al., 2017), intrafrontal (Dopper et al., 2014; Whitwell, 2019), and precuneus-insula (Whitwell et al., 2011b) connectivity.”
From Multiclass characterization of frontotemporal dementia variants via multimodal brain network computational inference (2023) · cites this paper as Dopper et al., 2014
Brain connectivity alterations may be present at early stages.
“while brain connectivity alterations may be present at early stages (Dopper et al., 2014; Meeter et al., 2017).”
From Multiclass characterization of frontotemporal dementia variants via multimodal brain network computational inference (2023) · cites this paper as Dopper et al., 2014

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Aberrant functional connectivity within the basal ganglia of patients with Parkinson's disease
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The presymptomatic phase of amyotrophic lateral sclerosis: are we merely scratching the surface?
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Alteration of the Intra- and Cross- Hemisphere Posterior Default Mode Network in Frontal Lobe Glioma Patients
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Altered Sense of Humor in Dementia
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Clinical and volumetric changes with increasing functional impairment in familial frontotemporal lobar degeneration
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Bias Introduced by Multiple Head Coils in MRI Research: An 8 Channel and 32 Channel Coil Comparison
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Humour processing in frontotemporal lobar degeneration: A behavioural and neuroanatomical analysis
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Applications of Resting-State Functional Connectivity to Neurodegenerative Disease
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The inner fluctuations of the brain in presymptomatic Frontotemporal Dementia: The chronnectome fingerprint
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Emotion recognition of morphed facial expressions in presymptomatic and symptomatic frontotemporal dementia, and Alzheimer’s dementia
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Widespread temporo-occipital lobe dysfunction in amyotrophic lateral sclerosis
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Lateral Temporal Lobe: An Early Imaging Marker of the Presymptomatic GRN Disease?
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[ 18 F]Flortaucipir PET Across Various MAPT Mutations in Presymptomatic and Symptomatic Carriers
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Resting-state brain connectivity in healthy young and middle-aged adults at risk of progressive Alzheimer’s disease
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Biological, Neuroimaging, and Neurophysiological Markers in Frontotemporal Dementia: Three Faces of the Same Coin
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The Use of Biomarkers and Genetic Screening to Diagnose Frontotemporal Dementia: Evidence and Clinical Implications
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Biomarkers for Amyotrophic Lateral Sclerosis and Frontotemporal Dementia Associated With Hexanucleotide Expansion Mutations in C9orf72
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ACR Appropriateness Criteria® Dementia
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Plasma neurofilament light protein correlates with diffusion tensor imaging metrics in frontotemporal dementia
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Longitudinal Cognitive Changes in Genetic Frontotemporal Dementia Within the GENFI Cohort
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Precision Medicine for Frontotemporal Dementia
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Multimodality imaging of neurodegenerative disorders with a focus on multiparametric magnetic resonance and molecular imaging
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Clinical Value of Longitudinal Serum Neurofilament Light Chain in Prodromal Genetic Frontotemporal Dementia
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Weighted Symbolic Dependence Metric (wSDM) for fMRI resting-state connectivity: A multicentric validation for frontotemporal dementia
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Neuroanatomical Correlates of Transcranial Magnetic Stimulation in Presymptomatic Granulin Mutation Carriers
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Imaging Biomarkers for Neurodegeneration in Presymptomatic Familial Frontotemporal Lobar Degeneration
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Biomarkers in frontotemporal dementia: Current landscape and future directions
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Lower functional connectivity of default mode network in cognitively normal young adults with mutation of APP, presenilins and APOE ε4
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Longitudinal Brain Atrophy Rates in Presymptomatic Carriers of Genetic Frontotemporal Dementia
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A multimodal MRI-based classification signature emerges just prior to symptom onset in frontotemporal dementia mutation carriers
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Preclinical Interventions in Mouse Models of Frontotemporal Dementia Due to Progranulin Mutations
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Early anterior cingulate involvement is seen in presymptomatic MAPT P301L mutation carriers
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ACR Appropriateness Criteria® Dementia: 2024 Update
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CSF placental growth factor – a novel candidate biomarker of frontotemporal dementia
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Frontotemporal dementia. How to deal with its diagnostic complexity?
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Impaired Knowledge of Social Norms in Dementia and Psychiatric Disorders: Validation of the Social Norms Questionnaire–Dutch Version (SNQ-NL)
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Trajectory of lobar atrophy in asymptomatic and symptomatic GRN mutation carriers: a longitudinal MRI study
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Mindfulness-Based Stress Reduction in Pre-symptomatic Genetic Frontotemporal Dementia: A Pilot Study
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The Effect of Predictive Testing in Adult‐Onset Neurodegenerative Diseases on Social and Personal Life
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Brain MR Spectroscopy Changes Precede Frontotemporal Lobar Degeneration Phenoconversion in Mapt Mutation Carriers
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Cortical iron accumulation in MAPT ‐ and C9orf 72‐associated frontotemporal lobar degeneration
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Cognitive control inhibition networks in adulthood are impaired by early iron deficiency in infancy
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Longitudinal cerebral perfusion in presymptomatic genetic frontotemporal dementia: GENFI results
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Multiclass characterization of frontotemporal dementia variants via multimodal brain network computational inference
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Functional Imaging for Neurodegenerative Diseases
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IC‐P‐138: Longitudinal structural and functional brain connectivity assessment in presymptomatic familial frontotemporal dementia
Dopper, E. G. P., Rombouts, S. A. R. B., Jiskoot, L. C., den Heijer, T., de Graaf, J., de Koning, I., Hammerschlag, A. R., Seelaar, H., Seeley, W. W., Veer, I. M., et al. (2013) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2013.05.135
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O5–03–06: Longitudinal structural and functional brain connectivity assessment in presymptomatic familial frontotemporal dementia
Dopper, E. G. P., Rombouts, S. A. R. B., Jiskoot, L. C., den Heijer, T., de Graaf, J., de Koning, I., Hammerschlag, A. R., Seelaar, H., Seeley, W. W., Veer, I. M., et al. (2013) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2013.04.486
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O2‐01‐02: Longitudinal, structural and functional connectivity in presymptomatic familial frontotemporal dementia
Jiskoot, L. C., Dopper, E. G. P., den Heijer, T., Hafkemeijer, A., de Koning, I., Seelaar, H., Veer, I. M., van Buchem, M. A., van Minkelen, R., Rombouts, S. A. R. B., et al. (2015) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2015.07.131
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Structural and functional connectivity in tau mutation carriers: from presymptomatic to symptomatic frontotemporal dementia
Bouzigues, A., Du, V. L., Joulot, M., Peysson, N., Houot, M., Béranger, B., Russell, L. L., Foster, P. H., Ferry‐Bolder, E., Swieten, J. C. V., et al. (2025) · Alzheimer s & Dementia · doi:10.1002/alz.70367 · Cited by 10 · see citing works
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Cellular signatures of functional resilience in presymptomatic frontotemporal dementiaPreprint
Tsvetanov, K. A., Malpetti, M., Jones, P. S., Rittman, T., Whiteside, D. J., Murley, A. G., Bethlehem, R. A. I., Paquola, C., Premi, E., Bouzigues, A., et al. (2025) · medRxiv · doi:10.1101/2025.02.24.25322778 · Cited by 1 · see citing works
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Authors: Dopper, E. G. P., Rombouts, S. A. R. B., Jiskoot, L. C., den Heijer, T., de Graaf, J. R. A., de Koning, I., Hammerschlag, A. R., Seelaar, H., Seeley, W. W., Veer, I. M., van Buchem, M. A., Rizzu, P., & van Swieten, J. C.
Affiliations: Leiden University (NL)
From the Departments of Neurology (E.G.P.D., L.C.J., T.d.H., H.S., J.C.v.S.), Epidemiology (T.d.H.), and Neuropsychology (J.R.A.d.G., I.d.K.), Erasmus Medical Center, Rotterdam; Department of Radiology (E.G.P.D., S.A.R.B.R., I.M.V., M.A.v.B.), Leiden University Medical Center; Departments of Neurology (E.G.P.D.) and Clinical Genetics (A.R.H., P.R., J.C.v.S.), VU Medical Center, Amsterdam; Leiden Institute for Brain and Cognition (S.A.R.B.R., I.M.V., M.A.v.B.) and Institute of Psychology (S.A.R.B.R.,...
ORCID: Dopper, Elise G.P.
Rombouts, Serge A.R.B.
Jiskoot, Lize C.
Hammerschlag, Anke R.
Seelaar, Harro
Seeley, William W.
Veer, Ilya M.
Rizzu, Patrizia
Venue: Neurology
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2014-07-08
Volume: 83
Issue: 2
ISSN: 0028-3878 (ISSN-L)
1526-632X
DOI: 10.1212/wnl.0000000000000583
OpenAlex: W4251162813
Cited by: 152
References: 35
Citations by year: 2026: 11 · 2025: 13 · 2024: 5 · 2023: 13 · 2022: 12 · 2021: 11 · 2020: 13 · 2019: 19 · 2018: 12 · 2017: 11 · 2016: 14 · 2015: 11 · 2014: 6 · 2013: 1
FWCI: 10.69
Type: journal article
Language: en
Open access: green
hdl.handle.net
Licence: other-oa
Locations: Neurology (publishedVersion)
RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Health Sciences › Medicine › Neurology › Amyotrophic Lateral Sclerosis Research
Keywords: frontotemporal dementia, presymptomatic carriers, MAPT mutations, GRN mutations, familial frontotemporal dementia, brain connectivity, functional connectivity, structural connectivity, uncinate fasciculus, fractional anisotropy, anterior midcingulate cortex, frontoinsular cortex, posterior cingulate cortex, gray matter volume, cognitive impairment, early biomarkers, diffusion tensor imaging, resting-state fMRI

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Structural and functional brain connectivity in presymptomatic familial frontotemporal dementia

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