Frontal white matter tracts sustaining speech production in primary progressive aphasia

Maria Luisa Mandelli, Eduardo Caverzasi, Richard J. Binney, Maya L. Henry, Iryna Lobach, Nikolas Block, Bagrat Amirbekian, Nina Dronkers, Bruce L. Miller, Roland G. Henry, Maria Luisa Gorno-Tempini

Research output: Contribution to journalArticle

59 Citations (Scopus)

Abstract

In primary progressive aphasia (PPA), speech and language difficulties are caused by neurodegeneration of specific brain networks. In the nonfluent/agrammatic variant (nfvPPA), motor speech and grammatical deficits are associated with atrophy in a left fronto-insular-striatal network previously implicated in speech production. In vivo dissection of the crossing white matter (WM) tracts within this "speech production network" is complex and has rarely been performed in health or in PPA.Wehypothesized that damage to these tracts would be specific to nfvPPA and would correlate with differential aspects of the patients' fluency abilities. We prospectively studied 25 PPA and 21 healthy individuals who underwent extensive cognitive testing and 3 T MRI. Using residual bootstrap Q-ball probabilistic tractography on high angular resolution diffusion-weighted imaging (HARDI), we reconstructed pathways connecting posterior inferior frontal, inferior premotor, insula, supplementary motor area (SMA) complex, striatum, and standard ventral and dorsal language pathways. We extracted tract-specific diffusion tensor imaging (DTI) metrics to assess changes across PPA variants and perform brain-behavioral correlations. SignificantWMchanges in the left intrafrontal and frontostriatal pathways were found in nfvPPA, but not in the semantic or logopenic variants. Correlations between tract-specific DTI metrics with cognitive scores confirmed the specific involvement of this anterior- dorsal network in fluency and suggested a preferential role of a posterior premotor-SMA pathway in motor speech. This study shows that left WM pathways connecting the speech production network are selectively damaged in nfvPPA and suggests that different tracts within this system are involved in subcomponents of fluency. These findings emphasize the emerging role of diffusion imaging in the differential diagnosis of neurodegenerative diseases.

Original languageEnglish (US)
Pages (from-to)9754-9767
Number of pages14
JournalJournal of Neuroscience
Volume34
Issue number29
DOIs
StatePublished - 2014
Externally publishedYes

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Primary Progressive Aphasia
Diffusion Tensor Imaging
Motor Cortex
Language
Efferent Pathways
Corpus Striatum
Aptitude
Brain
Semantics
Neurodegenerative Diseases
Atrophy
White Matter
Dissection
Differential Diagnosis
Health

Keywords

  • Diffusion tensor imaging
  • Frontal tracts
  • Primary progressive aphasia
  • Speech production
  • Tractography
  • White matter

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Mandelli, M. L., Caverzasi, E., Binney, R. J., Henry, M. L., Lobach, I., Block, N., ... Gorno-Tempini, M. L. (2014). Frontal white matter tracts sustaining speech production in primary progressive aphasia. Journal of Neuroscience, 34(29), 9754-9767. https://doi.org/10.1523/JNEUROSCI.3464-13.2014

Frontal white matter tracts sustaining speech production in primary progressive aphasia. / Mandelli, Maria Luisa; Caverzasi, Eduardo; Binney, Richard J.; Henry, Maya L.; Lobach, Iryna; Block, Nikolas; Amirbekian, Bagrat; Dronkers, Nina; Miller, Bruce L.; Henry, Roland G.; Gorno-Tempini, Maria Luisa.

In: Journal of Neuroscience, Vol. 34, No. 29, 2014, p. 9754-9767.

Research output: Contribution to journalArticle

Mandelli, ML, Caverzasi, E, Binney, RJ, Henry, ML, Lobach, I, Block, N, Amirbekian, B, Dronkers, N, Miller, BL, Henry, RG & Gorno-Tempini, ML 2014, 'Frontal white matter tracts sustaining speech production in primary progressive aphasia', Journal of Neuroscience, vol. 34, no. 29, pp. 9754-9767. https://doi.org/10.1523/JNEUROSCI.3464-13.2014
Mandelli, Maria Luisa ; Caverzasi, Eduardo ; Binney, Richard J. ; Henry, Maya L. ; Lobach, Iryna ; Block, Nikolas ; Amirbekian, Bagrat ; Dronkers, Nina ; Miller, Bruce L. ; Henry, Roland G. ; Gorno-Tempini, Maria Luisa. / Frontal white matter tracts sustaining speech production in primary progressive aphasia. In: Journal of Neuroscience. 2014 ; Vol. 34, No. 29. pp. 9754-9767.
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