Diffusion tractography of superior cerebellar peduncle and dentatorubrothalamic tracts in two autopsy confirmed progressive supranuclear palsy variants: Richardson syndrome and the speech-language variant

Background: Progressive supranuclear palsy (PSP) is a 4-repeat tauopathy with neurodegeneration typically observed in the superior cerebellar peduncle (SCP) and dentatorubrothalamic tracts (DRTT). However, it is unclear how these tracts are differentially affected in different clinical variants of P...

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Main Authors: Rodolfo G. Gatto, Peter R. Martin, Farwa Ali, Heather M. Clark, Joseph R. Duffy, Rene L. Utianski, Hugo Botha, Mary M. Machulda, Dennis W. Dickson, Keith A. Josephs, Jennifer L. Whitwell
Format: Article
Language:English
Published: Elsevier 2022-01-01
Series:NeuroImage: Clinical
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Online Access:http://www.sciencedirect.com/science/article/pii/S221315822200095X
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author Rodolfo G. Gatto
Peter R. Martin
Farwa Ali
Heather M. Clark
Joseph R. Duffy
Rene L. Utianski
Hugo Botha
Mary M. Machulda
Dennis W. Dickson
Keith A. Josephs
Jennifer L. Whitwell
author_facet Rodolfo G. Gatto
Peter R. Martin
Farwa Ali
Heather M. Clark
Joseph R. Duffy
Rene L. Utianski
Hugo Botha
Mary M. Machulda
Dennis W. Dickson
Keith A. Josephs
Jennifer L. Whitwell
author_sort Rodolfo G. Gatto
collection DOAJ
description Background: Progressive supranuclear palsy (PSP) is a 4-repeat tauopathy with neurodegeneration typically observed in the superior cerebellar peduncle (SCP) and dentatorubrothalamic tracts (DRTT). However, it is unclear how these tracts are differentially affected in different clinical variants of PSP. Objectives: To determine whether diffusion tractography of the SCP and DRTT can differentiate autopsy-confirmed PSP with Richardson’s syndrome (PSP-RS) and PSP with predominant speech/language disorder (PSP-SL). Methods: We studied 22 autopsy-confirmed PSP patients that included 12 with PSP-RS and 10 with PSP-SL. We compared these two groups to 11 patients with autopsy-confirmed Alzheimer’s disease with SL problems, i.e., logopenic progressive aphasia (AD-LPA) (disease controls) and 10 healthy controls. Whole brain tractography was performed to identify the SCP and DRTT, as well as the frontal aslant tract and superior longitudinal fasciculus. We assessed fractional anisotropy and mean diffusivity for each tract. Hierarchical linear modeling was used for statistical comparisons, and correlations were assessed with clinical disease severity, ocular motor impairment, and parkinsonism. DRTT connectomics matrix analysis was also performed across groups. Results: The SCP showed decreased fractional anisotropy for PSP-RS and PSP-SL and increased mean diffusivity in PSP-RS, compared to controls and AD-LPA. Right DRTT fibers showed lower fractional anisotropy in PSP-RS and PSP-SL compared to controls and AD-LPA, with PSP-RS also showing lower values compared to PSP-SL. Reductions in connectivity were observed in infratentorial DRTT regions in PSP-RS vs cortical regions in PSP-SL. PSP-SL showed greater abnormalities in the frontal aslant tract and superior longitudinal fasciculus compared to controls, PSP-RS, and AD-LPA. Significant correlations were observed between ocular motor impairment and SCP in PSP-RS (p = 0.042), and DRTT in PSP-SL (p = 0.022). In PSP-SL, the PSP Rating Scale correlated with the SCP (p = 0.045) and DRTT (p = 0.008), and the Unified Parkinson’s Disease Rating Scale correlated with the DRTT (p = 0.014). Conclusions: Degeneration of the SCP and DRTT are diagnostic features of both PSP-RS and PSP-SL and associations with clinical metrics validate the role of these tracts in PSP-related clinical features, particularly in PSP-SL.
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spelling doaj.art-1116345c829049db8a6f035fb194df942022-12-22T02:20:56ZengElsevierNeuroImage: Clinical2213-15822022-01-0135103030Diffusion tractography of superior cerebellar peduncle and dentatorubrothalamic tracts in two autopsy confirmed progressive supranuclear palsy variants: Richardson syndrome and the speech-language variantRodolfo G. Gatto0Peter R. Martin1Farwa Ali2Heather M. Clark3Joseph R. Duffy4Rene L. Utianski5Hugo Botha6Mary M. Machulda7Dennis W. Dickson8Keith A. Josephs9Jennifer L. Whitwell10Department of Neurology, Mayo Clinic, Rochester, MN, USADepartment of Quantitative Health Sciences, Mayo Clinic, Rochester, MN, USADepartment of Neurology, Mayo Clinic, Rochester, MN, USADepartment of Neurology, Mayo Clinic, Rochester, MN, USADepartment of Neurology, Mayo Clinic, Rochester, MN, USADepartment of Neurology, Mayo Clinic, Rochester, MN, USADepartment of Neurology, Mayo Clinic, Rochester, MN, USADepartment of Psychiatry and Psychology, Mayo Clinic, Rochester, MN, USADepartment of Neuroscience, Mayo Clinic, Jacksonville, FL, USADepartment of Neurology, Mayo Clinic, Rochester, MN, USADepartment of Radiology, Mayo Clinic, Rochester, MN, USA; Corresponding author at: Department of Radiology, Mayo Clinic, 200 1st St SW, Rochester MN 55905, USA.Background: Progressive supranuclear palsy (PSP) is a 4-repeat tauopathy with neurodegeneration typically observed in the superior cerebellar peduncle (SCP) and dentatorubrothalamic tracts (DRTT). However, it is unclear how these tracts are differentially affected in different clinical variants of PSP. Objectives: To determine whether diffusion tractography of the SCP and DRTT can differentiate autopsy-confirmed PSP with Richardson’s syndrome (PSP-RS) and PSP with predominant speech/language disorder (PSP-SL). Methods: We studied 22 autopsy-confirmed PSP patients that included 12 with PSP-RS and 10 with PSP-SL. We compared these two groups to 11 patients with autopsy-confirmed Alzheimer’s disease with SL problems, i.e., logopenic progressive aphasia (AD-LPA) (disease controls) and 10 healthy controls. Whole brain tractography was performed to identify the SCP and DRTT, as well as the frontal aslant tract and superior longitudinal fasciculus. We assessed fractional anisotropy and mean diffusivity for each tract. Hierarchical linear modeling was used for statistical comparisons, and correlations were assessed with clinical disease severity, ocular motor impairment, and parkinsonism. DRTT connectomics matrix analysis was also performed across groups. Results: The SCP showed decreased fractional anisotropy for PSP-RS and PSP-SL and increased mean diffusivity in PSP-RS, compared to controls and AD-LPA. Right DRTT fibers showed lower fractional anisotropy in PSP-RS and PSP-SL compared to controls and AD-LPA, with PSP-RS also showing lower values compared to PSP-SL. Reductions in connectivity were observed in infratentorial DRTT regions in PSP-RS vs cortical regions in PSP-SL. PSP-SL showed greater abnormalities in the frontal aslant tract and superior longitudinal fasciculus compared to controls, PSP-RS, and AD-LPA. Significant correlations were observed between ocular motor impairment and SCP in PSP-RS (p = 0.042), and DRTT in PSP-SL (p = 0.022). In PSP-SL, the PSP Rating Scale correlated with the SCP (p = 0.045) and DRTT (p = 0.008), and the Unified Parkinson’s Disease Rating Scale correlated with the DRTT (p = 0.014). Conclusions: Degeneration of the SCP and DRTT are diagnostic features of both PSP-RS and PSP-SL and associations with clinical metrics validate the role of these tracts in PSP-related clinical features, particularly in PSP-SL.http://www.sciencedirect.com/science/article/pii/S221315822200095XProgressive supranuclear palsyMRIDiffusion tensor imagingTractographySuperior cerebellar peduncleDentato-rubro-thalamic tract
spellingShingle Rodolfo G. Gatto
Peter R. Martin
Farwa Ali
Heather M. Clark
Joseph R. Duffy
Rene L. Utianski
Hugo Botha
Mary M. Machulda
Dennis W. Dickson
Keith A. Josephs
Jennifer L. Whitwell
Diffusion tractography of superior cerebellar peduncle and dentatorubrothalamic tracts in two autopsy confirmed progressive supranuclear palsy variants: Richardson syndrome and the speech-language variant
NeuroImage: Clinical
Progressive supranuclear palsy
MRI
Diffusion tensor imaging
Tractography
Superior cerebellar peduncle
Dentato-rubro-thalamic tract
title Diffusion tractography of superior cerebellar peduncle and dentatorubrothalamic tracts in two autopsy confirmed progressive supranuclear palsy variants: Richardson syndrome and the speech-language variant
title_full Diffusion tractography of superior cerebellar peduncle and dentatorubrothalamic tracts in two autopsy confirmed progressive supranuclear palsy variants: Richardson syndrome and the speech-language variant
title_fullStr Diffusion tractography of superior cerebellar peduncle and dentatorubrothalamic tracts in two autopsy confirmed progressive supranuclear palsy variants: Richardson syndrome and the speech-language variant
title_full_unstemmed Diffusion tractography of superior cerebellar peduncle and dentatorubrothalamic tracts in two autopsy confirmed progressive supranuclear palsy variants: Richardson syndrome and the speech-language variant
title_short Diffusion tractography of superior cerebellar peduncle and dentatorubrothalamic tracts in two autopsy confirmed progressive supranuclear palsy variants: Richardson syndrome and the speech-language variant
title_sort diffusion tractography of superior cerebellar peduncle and dentatorubrothalamic tracts in two autopsy confirmed progressive supranuclear palsy variants richardson syndrome and the speech language variant
topic Progressive supranuclear palsy
MRI
Diffusion tensor imaging
Tractography
Superior cerebellar peduncle
Dentato-rubro-thalamic tract
url http://www.sciencedirect.com/science/article/pii/S221315822200095X
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