MRI signatures of the frontotemporal lobar degeneration continuum

Federica Agosta, Sebastiano Galantucci, Giuseppe Magnani, Alessandra Marcone, Daniele Martinelli, Maria Antonietta Volontè, Nilo Riva, Sandro Iannaccone, Pilar M. Ferraro, Francesca Caso, Adriano Chiò, Giancarlo Comi, Andrea Falini, Massimo Filippi

Research output: Contribution to journalArticle

18 Citations (Scopus)

Abstract

Objective. To identify overlapping and unique grey (GM) and white matter (WM) signatures within the frontotemporal lobar degeneration (FTLD) continuum, and discriminate likely FTLD-TAU and FTLD-TDP patients using structural and diffusion tensor (DT) magnetic resonance imaging (MRI). Methods. T1-weighted and DT MRI were collected from 121 subjects: 35 motor neuron disease (MND), 14 behavioral variant of frontotemporal dementia, 12 semantic and 11 nonfluent primary progressive aphasia, 21 progressive supranuclear palsy syndrome patients, and 28 healthy controls. Patterns of GM atrophy were established using voxel-based morphometry. Tract-based spatial statistics was used to perform a WM voxelwise analysis of mean diffusivity and fractional anisotropy. Results. In all clinical FTLD phenotypes, the pattern of WM damage was more distributed than that of GM atrophy. All patient groups, with the exception of MND cases with a pure motor syndrome, shared a focal GM atrophy centered around the dorsolateral and medial frontal cortex and a largely overlapping pattern of WM damage involving the genu and body of the corpus callosum and ventral frontotemporal and dorsal frontoparietal WM pathways. Surrounding this common area, phenotype (symptom)-specific GM and WM regions of damage were found in each group. Conclusions. In the FTLD spectrum, WM disruption is more severe than GM damage. Frontal cortex and WM pathways represent the common target of neurodegeneration in these conditions. The topographic pattern of damage supports a "prion-like" protein propagation through WM connections as underlying mechanism of the stereotyped progression of FTLD.

Original languageEnglish
Pages (from-to)2602-2614
Number of pages13
JournalHuman Brain Mapping
Volume36
Issue number7
DOIs
Publication statusPublished - Jul 1 2015

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Frontotemporal Lobar Degeneration
Magnetic Resonance Imaging
Atrophy
Motor Neuron Disease
Diffusion Magnetic Resonance Imaging
Frontal Lobe
Primary Progressive Nonfluent Aphasia
Progressive Supranuclear Palsy
Phenotype
White Matter
Frontotemporal Dementia
Corpus Callosum
Anisotropy
Semantics

Keywords

  • Amyotrophic lateral sclerosis
  • Diffusion tensor MRI
  • Frontotemporal dementia
  • Frontotemporal lobar degeneration
  • Motor neuron disease
  • Primary progressive aphasia
  • Progressive supranuclear palsy
  • White matter

ASJC Scopus subject areas

  • Clinical Neurology
  • Anatomy
  • Neurology
  • Radiology Nuclear Medicine and imaging
  • Radiological and Ultrasound Technology

Cite this

MRI signatures of the frontotemporal lobar degeneration continuum. / Agosta, Federica; Galantucci, Sebastiano; Magnani, Giuseppe; Marcone, Alessandra; Martinelli, Daniele; Antonietta Volontè, Maria; Riva, Nilo; Iannaccone, Sandro; Ferraro, Pilar M.; Caso, Francesca; Chiò, Adriano; Comi, Giancarlo; Falini, Andrea; Filippi, Massimo.

In: Human Brain Mapping, Vol. 36, No. 7, 01.07.2015, p. 2602-2614.

Research output: Contribution to journalArticle

Agosta, F, Galantucci, S, Magnani, G, Marcone, A, Martinelli, D, Antonietta Volontè, M, Riva, N, Iannaccone, S, Ferraro, PM, Caso, F, Chiò, A, Comi, G, Falini, A & Filippi, M 2015, 'MRI signatures of the frontotemporal lobar degeneration continuum', Human Brain Mapping, vol. 36, no. 7, pp. 2602-2614. https://doi.org/10.1002/hbm.22794
Agosta F, Galantucci S, Magnani G, Marcone A, Martinelli D, Antonietta Volontè M et al. MRI signatures of the frontotemporal lobar degeneration continuum. Human Brain Mapping. 2015 Jul 1;36(7):2602-2614. https://doi.org/10.1002/hbm.22794
Agosta, Federica ; Galantucci, Sebastiano ; Magnani, Giuseppe ; Marcone, Alessandra ; Martinelli, Daniele ; Antonietta Volontè, Maria ; Riva, Nilo ; Iannaccone, Sandro ; Ferraro, Pilar M. ; Caso, Francesca ; Chiò, Adriano ; Comi, Giancarlo ; Falini, Andrea ; Filippi, Massimo. / MRI signatures of the frontotemporal lobar degeneration continuum. In: Human Brain Mapping. 2015 ; Vol. 36, No. 7. pp. 2602-2614.
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AU - Agosta, Federica

AU - Galantucci, Sebastiano

AU - Magnani, Giuseppe

AU - Marcone, Alessandra

AU - Martinelli, Daniele

AU - Antonietta Volontè, Maria

AU - Riva, Nilo

AU - Iannaccone, Sandro

AU - Ferraro, Pilar M.

AU - Caso, Francesca

AU - Chiò, Adriano

AU - Comi, Giancarlo

AU - Falini, Andrea

AU - Filippi, Massimo

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N2 - Objective. To identify overlapping and unique grey (GM) and white matter (WM) signatures within the frontotemporal lobar degeneration (FTLD) continuum, and discriminate likely FTLD-TAU and FTLD-TDP patients using structural and diffusion tensor (DT) magnetic resonance imaging (MRI). Methods. T1-weighted and DT MRI were collected from 121 subjects: 35 motor neuron disease (MND), 14 behavioral variant of frontotemporal dementia, 12 semantic and 11 nonfluent primary progressive aphasia, 21 progressive supranuclear palsy syndrome patients, and 28 healthy controls. Patterns of GM atrophy were established using voxel-based morphometry. Tract-based spatial statistics was used to perform a WM voxelwise analysis of mean diffusivity and fractional anisotropy. Results. In all clinical FTLD phenotypes, the pattern of WM damage was more distributed than that of GM atrophy. All patient groups, with the exception of MND cases with a pure motor syndrome, shared a focal GM atrophy centered around the dorsolateral and medial frontal cortex and a largely overlapping pattern of WM damage involving the genu and body of the corpus callosum and ventral frontotemporal and dorsal frontoparietal WM pathways. Surrounding this common area, phenotype (symptom)-specific GM and WM regions of damage were found in each group. Conclusions. In the FTLD spectrum, WM disruption is more severe than GM damage. Frontal cortex and WM pathways represent the common target of neurodegeneration in these conditions. The topographic pattern of damage supports a "prion-like" protein propagation through WM connections as underlying mechanism of the stereotyped progression of FTLD.

AB - Objective. To identify overlapping and unique grey (GM) and white matter (WM) signatures within the frontotemporal lobar degeneration (FTLD) continuum, and discriminate likely FTLD-TAU and FTLD-TDP patients using structural and diffusion tensor (DT) magnetic resonance imaging (MRI). Methods. T1-weighted and DT MRI were collected from 121 subjects: 35 motor neuron disease (MND), 14 behavioral variant of frontotemporal dementia, 12 semantic and 11 nonfluent primary progressive aphasia, 21 progressive supranuclear palsy syndrome patients, and 28 healthy controls. Patterns of GM atrophy were established using voxel-based morphometry. Tract-based spatial statistics was used to perform a WM voxelwise analysis of mean diffusivity and fractional anisotropy. Results. In all clinical FTLD phenotypes, the pattern of WM damage was more distributed than that of GM atrophy. All patient groups, with the exception of MND cases with a pure motor syndrome, shared a focal GM atrophy centered around the dorsolateral and medial frontal cortex and a largely overlapping pattern of WM damage involving the genu and body of the corpus callosum and ventral frontotemporal and dorsal frontoparietal WM pathways. Surrounding this common area, phenotype (symptom)-specific GM and WM regions of damage were found in each group. Conclusions. In the FTLD spectrum, WM disruption is more severe than GM damage. Frontal cortex and WM pathways represent the common target of neurodegeneration in these conditions. The topographic pattern of damage supports a "prion-like" protein propagation through WM connections as underlying mechanism of the stereotyped progression of FTLD.

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KW - White matter

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