Combined assessment of progressive apraxia of speech brain microstructure by diffusion tensor imaging tractography and multishell neurite orientation dispersion and density imaging

Abstract Background Progressive apraxia of speech (PAOS) is characterized by difficulties with motor speech programming and planning. PAOS targets gray matter (GM) and white matter (WM) microstructure that can be assessed using diffusion tensor imaging (DTI) and multishell applications, such as neur...

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Main Authors: Rodolfo G. Gatto, Gabriela Meade, Joseph R. Duffy, Heather M. Clark, Rene L. Utianski, Hugo Botha, Mary M. Machulda, Keith A. Josephs, Jennifer L. Whitwell
Format: Article
Language:English
Published: Wiley 2024-01-01
Series:Brain and Behavior
Subjects:
Online Access:https://doi.org/10.1002/brb3.3346
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author Rodolfo G. Gatto
Gabriela Meade
Joseph R. Duffy
Heather M. Clark
Rene L. Utianski
Hugo Botha
Mary M. Machulda
Keith A. Josephs
Jennifer L. Whitwell
author_facet Rodolfo G. Gatto
Gabriela Meade
Joseph R. Duffy
Heather M. Clark
Rene L. Utianski
Hugo Botha
Mary M. Machulda
Keith A. Josephs
Jennifer L. Whitwell
author_sort Rodolfo G. Gatto
collection DOAJ
description Abstract Background Progressive apraxia of speech (PAOS) is characterized by difficulties with motor speech programming and planning. PAOS targets gray matter (GM) and white matter (WM) microstructure that can be assessed using diffusion tensor imaging (DTI) and multishell applications, such as neurite orientation dispersion and density imaging (NODDI). In this study, we aimed to apply DTI and NODDI to add further insight into PAOS tissue microstructure. Methods Twenty‐two PAOS patients and 26 age‐ and sex‐matched controls, recruited by the Neurodegenerative Research Group (NRG) at Mayo Clinic, underwent diffusion MRI on 3T MRI. Brain maps of fractional anisotropy (FA) and mean diffusivity (MD) from DTI and intracellular volume fraction (ICVF) and isotropic volume fraction (IsoVF) from NODDI were generated. Global WM and GM, and specific WM tracts were identified using tractography and lobar GM regions. Results Global WM differences between PAOS and controls were greatest for ICVF, and global GM differences were greatest for MD and IsoVF. Abnormalities in key WM tracts involved in PAOS, including the body of the corpus callosum and frontal aslant tract, were identified with FA, MD, and ICVF, with excellent differentiation of PAOS from controls (area under the receiver operating characteristic curves >.90). MD and ICVF identified abnormalities in arcuate fasciculus, thalamic radiations, and corticostriatal tracts. Significant correlations were identified between an index of articulatory errors and DTI and NODDI metrics from the arcuate fasciculus, frontal aslant tract, and inferior longitudinal fasciculus. Conclusions DTI and NODDI represent different aspects of brain tissue microstructure, increasing the number of potential biomarkers for PAOS.
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spelling doaj.art-76e850b7928443e58ea7ca7b4898c7b12024-03-13T10:15:39ZengWileyBrain and Behavior2162-32792024-01-01141n/an/a10.1002/brb3.3346Combined assessment of progressive apraxia of speech brain microstructure by diffusion tensor imaging tractography and multishell neurite orientation dispersion and density imagingRodolfo G. Gatto0Gabriela Meade1Joseph R. Duffy2Heather M. Clark3Rene L. Utianski4Hugo Botha5Mary M. Machulda6Keith A. Josephs7Jennifer L. Whitwell8Department of Neurology Mayo Clinic Rochester Minnesota USADepartment of Neurology Mayo Clinic Rochester Minnesota USADepartment of Neurology Mayo Clinic Rochester Minnesota USADepartment of Neurology Mayo Clinic Rochester Minnesota USADepartment of Neurology Mayo Clinic Rochester Minnesota USADepartment of Neurology Mayo Clinic Rochester Minnesota USADepartment of Psychiatry and Psychology Mayo Clinic Rochester Minnesota USADepartment of Neurology Mayo Clinic Rochester Minnesota USADepartment of Radiology Mayo Clinic Rochester Minnesota USAAbstract Background Progressive apraxia of speech (PAOS) is characterized by difficulties with motor speech programming and planning. PAOS targets gray matter (GM) and white matter (WM) microstructure that can be assessed using diffusion tensor imaging (DTI) and multishell applications, such as neurite orientation dispersion and density imaging (NODDI). In this study, we aimed to apply DTI and NODDI to add further insight into PAOS tissue microstructure. Methods Twenty‐two PAOS patients and 26 age‐ and sex‐matched controls, recruited by the Neurodegenerative Research Group (NRG) at Mayo Clinic, underwent diffusion MRI on 3T MRI. Brain maps of fractional anisotropy (FA) and mean diffusivity (MD) from DTI and intracellular volume fraction (ICVF) and isotropic volume fraction (IsoVF) from NODDI were generated. Global WM and GM, and specific WM tracts were identified using tractography and lobar GM regions. Results Global WM differences between PAOS and controls were greatest for ICVF, and global GM differences were greatest for MD and IsoVF. Abnormalities in key WM tracts involved in PAOS, including the body of the corpus callosum and frontal aslant tract, were identified with FA, MD, and ICVF, with excellent differentiation of PAOS from controls (area under the receiver operating characteristic curves >.90). MD and ICVF identified abnormalities in arcuate fasciculus, thalamic radiations, and corticostriatal tracts. Significant correlations were identified between an index of articulatory errors and DTI and NODDI metrics from the arcuate fasciculus, frontal aslant tract, and inferior longitudinal fasciculus. Conclusions DTI and NODDI represent different aspects of brain tissue microstructure, increasing the number of potential biomarkers for PAOS.https://doi.org/10.1002/brb3.33464R tauopathiesdiffusion tensor imagingneurite orientation dispersion density imagingprogressive apraxia of speechtractography
spellingShingle Rodolfo G. Gatto
Gabriela Meade
Joseph R. Duffy
Heather M. Clark
Rene L. Utianski
Hugo Botha
Mary M. Machulda
Keith A. Josephs
Jennifer L. Whitwell
Combined assessment of progressive apraxia of speech brain microstructure by diffusion tensor imaging tractography and multishell neurite orientation dispersion and density imaging
Brain and Behavior
4R tauopathies
diffusion tensor imaging
neurite orientation dispersion density imaging
progressive apraxia of speech
tractography
title Combined assessment of progressive apraxia of speech brain microstructure by diffusion tensor imaging tractography and multishell neurite orientation dispersion and density imaging
title_full Combined assessment of progressive apraxia of speech brain microstructure by diffusion tensor imaging tractography and multishell neurite orientation dispersion and density imaging
title_fullStr Combined assessment of progressive apraxia of speech brain microstructure by diffusion tensor imaging tractography and multishell neurite orientation dispersion and density imaging
title_full_unstemmed Combined assessment of progressive apraxia of speech brain microstructure by diffusion tensor imaging tractography and multishell neurite orientation dispersion and density imaging
title_short Combined assessment of progressive apraxia of speech brain microstructure by diffusion tensor imaging tractography and multishell neurite orientation dispersion and density imaging
title_sort combined assessment of progressive apraxia of speech brain microstructure by diffusion tensor imaging tractography and multishell neurite orientation dispersion and density imaging
topic 4R tauopathies
diffusion tensor imaging
neurite orientation dispersion density imaging
progressive apraxia of speech
tractography
url https://doi.org/10.1002/brb3.3346
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