White matter damage in primary progressive aphasias: A diffusion tensor tractography study

Sebastiano Galantucci, Maria Carmela Tartaglia, Stephen M Wilson, Maya L. Henry, Massimo Filippi, Federica Agosta, Nina F. Dronkers, Roland G. Henry, Jennifer M. Ogar, Bruce L. Miller, Maria Luisa Gorno-Tempini

Research output: Contribution to journalArticle

187 Citations (Scopus)

Abstract

Primary progressive aphasia is a clinical syndrome that encompasses three major phenotypes: non-fluent/agrammatic, semantic and logopenic. These clinical entities have been associated with characteristic patterns of focal grey matter atrophy in left posterior frontoinsular, anterior temporal and left temporoparietal regions, respectively. Recently, network-level dysfunction has been hypothesized but research to date has focused largely on studying grey matter damage. The aim of this study was to assess the integrity of white matter tracts in the different primary progressive aphasia subtypes. We used diffusion tensor imaging in 48 individuals: nine non-fluent, nine semantic, nine logopenic and 21 age-matched controls. Probabilistic tractography was used to identify bilateral inferior longitudinal (anterior, middle, posterior) and uncinate fasciculi (referred to as the ventral pathway); and the superior longitudinal fasciculus segmented into its frontosupramarginal, frontoangular, frontotemporal and temporoparietal components, (referred to as the dorsal pathway). We compared the tracts' mean fractional anisotropy, axial, radial and mean diffusivities for each tract in the different diagnostic categories. The most prominent white matter changes were found in the dorsal pathways in non-fluent patients, in the two ventral pathways and the temporal components of the dorsal pathways in semantic variant, and in the temporoparietal component of the dorsal bundles in logopenic patients. Each of the primary progressive aphasia variants showed different patterns of diffusion tensor metrics alterations: non-fluent patients showed the greatest changes in fractional anisotropy and radial and mean diffusivities; semantic variant patients had severe changes in all metrics; and logopenic patients had the least white matter damage, mainly involving diffusivity, with fractional anisotropy altered only in the temporoparietal component of the dorsal pathway. This study demonstrates that both careful dissection of the main language tracts and consideration of all diffusion tensor metrics are necessary to characterize the white matter changes that occur in the variants of primary progressive aphasia. These results highlight the potential value of diffusion tensor imaging as a new tool in the multimodal diagnostic evaluation of primary progressive aphasia.

Original languageEnglish (US)
Pages (from-to)3011-3029
Number of pages19
JournalBrain
Volume134
Issue number10
DOIs
StatePublished - Oct 2011

Fingerprint

Primary Progressive Aphasia
Diffusion Tensor Imaging
Semantics
Anisotropy
Atrophy
Dissection
Language
White Matter
Pathway
Damage
Phenotype
Research

Keywords

  • diffusion tensor imaging
  • logopenic progressive aphasia
  • primary progressive aphasia
  • progressive non-fluent aphasia
  • semantic dementia

ASJC Scopus subject areas

  • Clinical Neurology
  • Arts and Humanities (miscellaneous)

Cite this

Galantucci, S., Tartaglia, M. C., Wilson, S. M., Henry, M. L., Filippi, M., Agosta, F., ... Gorno-Tempini, M. L. (2011). White matter damage in primary progressive aphasias: A diffusion tensor tractography study. Brain, 134(10), 3011-3029. https://doi.org/10.1093/brain/awr099

White matter damage in primary progressive aphasias : A diffusion tensor tractography study. / Galantucci, Sebastiano; Tartaglia, Maria Carmela; Wilson, Stephen M; Henry, Maya L.; Filippi, Massimo; Agosta, Federica; Dronkers, Nina F.; Henry, Roland G.; Ogar, Jennifer M.; Miller, Bruce L.; Gorno-Tempini, Maria Luisa.

In: Brain, Vol. 134, No. 10, 10.2011, p. 3011-3029.

Research output: Contribution to journalArticle

Galantucci, S, Tartaglia, MC, Wilson, SM, Henry, ML, Filippi, M, Agosta, F, Dronkers, NF, Henry, RG, Ogar, JM, Miller, BL & Gorno-Tempini, ML 2011, 'White matter damage in primary progressive aphasias: A diffusion tensor tractography study', Brain, vol. 134, no. 10, pp. 3011-3029. https://doi.org/10.1093/brain/awr099
Galantucci S, Tartaglia MC, Wilson SM, Henry ML, Filippi M, Agosta F et al. White matter damage in primary progressive aphasias: A diffusion tensor tractography study. Brain. 2011 Oct;134(10):3011-3029. https://doi.org/10.1093/brain/awr099
Galantucci, Sebastiano ; Tartaglia, Maria Carmela ; Wilson, Stephen M ; Henry, Maya L. ; Filippi, Massimo ; Agosta, Federica ; Dronkers, Nina F. ; Henry, Roland G. ; Ogar, Jennifer M. ; Miller, Bruce L. ; Gorno-Tempini, Maria Luisa. / White matter damage in primary progressive aphasias : A diffusion tensor tractography study. In: Brain. 2011 ; Vol. 134, No. 10. pp. 3011-3029.
@article{99cf87c9fe904767b733cddbb1b908e4,
title = "White matter damage in primary progressive aphasias: A diffusion tensor tractography study",
abstract = "Primary progressive aphasia is a clinical syndrome that encompasses three major phenotypes: non-fluent/agrammatic, semantic and logopenic. These clinical entities have been associated with characteristic patterns of focal grey matter atrophy in left posterior frontoinsular, anterior temporal and left temporoparietal regions, respectively. Recently, network-level dysfunction has been hypothesized but research to date has focused largely on studying grey matter damage. The aim of this study was to assess the integrity of white matter tracts in the different primary progressive aphasia subtypes. We used diffusion tensor imaging in 48 individuals: nine non-fluent, nine semantic, nine logopenic and 21 age-matched controls. Probabilistic tractography was used to identify bilateral inferior longitudinal (anterior, middle, posterior) and uncinate fasciculi (referred to as the ventral pathway); and the superior longitudinal fasciculus segmented into its frontosupramarginal, frontoangular, frontotemporal and temporoparietal components, (referred to as the dorsal pathway). We compared the tracts' mean fractional anisotropy, axial, radial and mean diffusivities for each tract in the different diagnostic categories. The most prominent white matter changes were found in the dorsal pathways in non-fluent patients, in the two ventral pathways and the temporal components of the dorsal pathways in semantic variant, and in the temporoparietal component of the dorsal bundles in logopenic patients. Each of the primary progressive aphasia variants showed different patterns of diffusion tensor metrics alterations: non-fluent patients showed the greatest changes in fractional anisotropy and radial and mean diffusivities; semantic variant patients had severe changes in all metrics; and logopenic patients had the least white matter damage, mainly involving diffusivity, with fractional anisotropy altered only in the temporoparietal component of the dorsal pathway. This study demonstrates that both careful dissection of the main language tracts and consideration of all diffusion tensor metrics are necessary to characterize the white matter changes that occur in the variants of primary progressive aphasia. These results highlight the potential value of diffusion tensor imaging as a new tool in the multimodal diagnostic evaluation of primary progressive aphasia.",
keywords = "diffusion tensor imaging, logopenic progressive aphasia, primary progressive aphasia, progressive non-fluent aphasia, semantic dementia",
author = "Sebastiano Galantucci and Tartaglia, {Maria Carmela} and Wilson, {Stephen M} and Henry, {Maya L.} and Massimo Filippi and Federica Agosta and Dronkers, {Nina F.} and Henry, {Roland G.} and Ogar, {Jennifer M.} and Miller, {Bruce L.} and Gorno-Tempini, {Maria Luisa}",
year = "2011",
month = "10",
doi = "10.1093/brain/awr099",
language = "English (US)",
volume = "134",
pages = "3011--3029",
journal = "Brain",
issn = "0006-8950",
publisher = "Oxford University Press",
number = "10",

}

TY - JOUR

T1 - White matter damage in primary progressive aphasias

T2 - A diffusion tensor tractography study

AU - Galantucci, Sebastiano

AU - Tartaglia, Maria Carmela

AU - Wilson, Stephen M

AU - Henry, Maya L.

AU - Filippi, Massimo

AU - Agosta, Federica

AU - Dronkers, Nina F.

AU - Henry, Roland G.

AU - Ogar, Jennifer M.

AU - Miller, Bruce L.

AU - Gorno-Tempini, Maria Luisa

PY - 2011/10

Y1 - 2011/10

N2 - Primary progressive aphasia is a clinical syndrome that encompasses three major phenotypes: non-fluent/agrammatic, semantic and logopenic. These clinical entities have been associated with characteristic patterns of focal grey matter atrophy in left posterior frontoinsular, anterior temporal and left temporoparietal regions, respectively. Recently, network-level dysfunction has been hypothesized but research to date has focused largely on studying grey matter damage. The aim of this study was to assess the integrity of white matter tracts in the different primary progressive aphasia subtypes. We used diffusion tensor imaging in 48 individuals: nine non-fluent, nine semantic, nine logopenic and 21 age-matched controls. Probabilistic tractography was used to identify bilateral inferior longitudinal (anterior, middle, posterior) and uncinate fasciculi (referred to as the ventral pathway); and the superior longitudinal fasciculus segmented into its frontosupramarginal, frontoangular, frontotemporal and temporoparietal components, (referred to as the dorsal pathway). We compared the tracts' mean fractional anisotropy, axial, radial and mean diffusivities for each tract in the different diagnostic categories. The most prominent white matter changes were found in the dorsal pathways in non-fluent patients, in the two ventral pathways and the temporal components of the dorsal pathways in semantic variant, and in the temporoparietal component of the dorsal bundles in logopenic patients. Each of the primary progressive aphasia variants showed different patterns of diffusion tensor metrics alterations: non-fluent patients showed the greatest changes in fractional anisotropy and radial and mean diffusivities; semantic variant patients had severe changes in all metrics; and logopenic patients had the least white matter damage, mainly involving diffusivity, with fractional anisotropy altered only in the temporoparietal component of the dorsal pathway. This study demonstrates that both careful dissection of the main language tracts and consideration of all diffusion tensor metrics are necessary to characterize the white matter changes that occur in the variants of primary progressive aphasia. These results highlight the potential value of diffusion tensor imaging as a new tool in the multimodal diagnostic evaluation of primary progressive aphasia.

AB - Primary progressive aphasia is a clinical syndrome that encompasses three major phenotypes: non-fluent/agrammatic, semantic and logopenic. These clinical entities have been associated with characteristic patterns of focal grey matter atrophy in left posterior frontoinsular, anterior temporal and left temporoparietal regions, respectively. Recently, network-level dysfunction has been hypothesized but research to date has focused largely on studying grey matter damage. The aim of this study was to assess the integrity of white matter tracts in the different primary progressive aphasia subtypes. We used diffusion tensor imaging in 48 individuals: nine non-fluent, nine semantic, nine logopenic and 21 age-matched controls. Probabilistic tractography was used to identify bilateral inferior longitudinal (anterior, middle, posterior) and uncinate fasciculi (referred to as the ventral pathway); and the superior longitudinal fasciculus segmented into its frontosupramarginal, frontoangular, frontotemporal and temporoparietal components, (referred to as the dorsal pathway). We compared the tracts' mean fractional anisotropy, axial, radial and mean diffusivities for each tract in the different diagnostic categories. The most prominent white matter changes were found in the dorsal pathways in non-fluent patients, in the two ventral pathways and the temporal components of the dorsal pathways in semantic variant, and in the temporoparietal component of the dorsal bundles in logopenic patients. Each of the primary progressive aphasia variants showed different patterns of diffusion tensor metrics alterations: non-fluent patients showed the greatest changes in fractional anisotropy and radial and mean diffusivities; semantic variant patients had severe changes in all metrics; and logopenic patients had the least white matter damage, mainly involving diffusivity, with fractional anisotropy altered only in the temporoparietal component of the dorsal pathway. This study demonstrates that both careful dissection of the main language tracts and consideration of all diffusion tensor metrics are necessary to characterize the white matter changes that occur in the variants of primary progressive aphasia. These results highlight the potential value of diffusion tensor imaging as a new tool in the multimodal diagnostic evaluation of primary progressive aphasia.

KW - diffusion tensor imaging

KW - logopenic progressive aphasia

KW - primary progressive aphasia

KW - progressive non-fluent aphasia

KW - semantic dementia

UR - http://www.scopus.com/inward/record.url?scp=80054080693&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=80054080693&partnerID=8YFLogxK

U2 - 10.1093/brain/awr099

DO - 10.1093/brain/awr099

M3 - Article

C2 - 21666264

AN - SCOPUS:80054080693

VL - 134

SP - 3011

EP - 3029

JO - Brain

JF - Brain

SN - 0006-8950

IS - 10

ER -