Motor symptoms in Parkinson’s disease are related to the interplay between cortical curvature and thickness

Introduction: Brain atrophy in Parkinson’s disease occurs to varying degrees in different brain regions, even at the early stage of the disease. While cortical morphological features are often considered independently in structural brain imaging studies, research on the co-progression of different c...

Full description

Bibliographic Details
Main Authors: Hannes Almgren, Alexandru Hanganu, Milton Camacho, Mekale Kibreab, Richard Camicioli, Zahinoor Ismail, Nils D. Forkert, Oury Monchi
Format: Article
Language:English
Published: Elsevier 2023-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158222003655
_version_ 1797869769670524928
author Hannes Almgren
Alexandru Hanganu
Milton Camacho
Mekale Kibreab
Richard Camicioli
Zahinoor Ismail
Nils D. Forkert
Oury Monchi
author_facet Hannes Almgren
Alexandru Hanganu
Milton Camacho
Mekale Kibreab
Richard Camicioli
Zahinoor Ismail
Nils D. Forkert
Oury Monchi
author_sort Hannes Almgren
collection DOAJ
description Introduction: Brain atrophy in Parkinson’s disease occurs to varying degrees in different brain regions, even at the early stage of the disease. While cortical morphological features are often considered independently in structural brain imaging studies, research on the co-progression of different cortical morphological measurements could provide new insights regarding the progression of PD. This study’s aim was to examine the interplay between cortical curvature and thickness as a function of PD diagnosis, motor symptoms, and cognitive performance. Methods: A total of 359 de novo PD patients and 159 healthy controls (HC) from the Parkinson’s Progression Markers Initiative (PPMI) database were included in this study. Additionally, an independent cohort from four databases (182 PD, 132 HC) with longer disease durations was included to assess the effects of PD diagnosis in more advanced cases. Pearson correlation was used to determine subject-specific associations between cortical curvature and thickness estimated from T1-weighted MRI images. General linear modeling (GLM) was then used to assess the effect of PD diagnosis, motor symptoms, and cognitive performance on the curvature-thickness association. Next, longitudinal changes in the curvature-thickness correlation as well as the predictive effect of the cortical curvature-thickness association on changes in motor symptoms and cognitive performance across four years were investigated. Finally, Akaike information criterion (AIC) was used to build a GLM to model PD motor symptom severity cross-sectionally. Results: A significant interaction effect between PD motor symptoms and age on the curvature-thickness correlation was found (βstandardized = 0.11; t(350) = 2.12; p = 0.03). This interaction effect showed that motor symptoms in older patients were related to an attenuated curvature-thickness association. No significant effect of PD diagnosis was observed for the PPMI database (β = 0.03; t(510) = 0.35; p = 0.72). However, in patients with a longer disease duration, a significant effect of diagnosis on the curvature-thickness association was found (βstandardized = 0.31; t(306.7) = 3.49; p = 0.0006). Moreover, rigidity, but not tremor, in PD was significantly related to the curvature-thickness correlation (βstandardized = 0.11, t(350) = 2.24, p = 0.03; βstandardized = -0.03, t(350) = -0.58, p = 0.56, respectively). The curvature-thickness association was attenuated over time in both PD and HC, but the two groups did not show a significantly different effect (βstandardized = 0.03, t(184.7) = 0.78, p = 0.44). No predictive effects of the CC-CT correlation on longitudinal changes in cognitive performance or motor symptoms were observed (all p-values > 0.05). The best cross-sectional model for PD motor symptoms included the curvature-thickness correlation, cognitive performance, and putamen dopamine transporter (DAT) binding, which together explained 14 % of variance. Conclusion: The association between cortical curvature and thickness is related to PD motor symptoms and age. This research shows the potential of modeling the curvature-thickness interplay in PD.
first_indexed 2024-04-10T00:18:04Z
format Article
id doaj.art-9c9a7e0dbf6b408c8d9d7803070713b9
institution Directory Open Access Journal
issn 2213-1582
language English
last_indexed 2024-04-10T00:18:04Z
publishDate 2023-01-01
publisher Elsevier
record_format Article
series NeuroImage: Clinical
spelling doaj.art-9c9a7e0dbf6b408c8d9d7803070713b92023-03-16T05:03:58ZengElsevierNeuroImage: Clinical2213-15822023-01-0137103300Motor symptoms in Parkinson’s disease are related to the interplay between cortical curvature and thicknessHannes Almgren0Alexandru Hanganu1Milton Camacho2Mekale Kibreab3Richard Camicioli4Zahinoor Ismail5Nils D. Forkert6Oury Monchi7Department of Clinical Neurosciences, University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, Canada; Hotchkiss Brain Institute, Cumming School of Medicine, University of Calgary, Calgary, 3330 Hospital Dr NW, Calgary, AB T2N 1N4, Canada; Corresponding author at: 2500 University Drive NW, Calgary, AB T2N 1N4, CanadaDépartement de Psychologie, Université de Montréal, Pavillon Marie-Victorin, 90 Vincent d'Indy Ave, Montréal, QC H2V 2S9, Canada; Centre de recherche de l’Institut universitaire de gériatrie de Montréal, 4565 Chemin Queen Mary, Montréal, QC H3W 1W5, CanadaHotchkiss Brain Institute, Cumming School of Medicine, University of Calgary, Calgary, 3330 Hospital Dr NW, Calgary, AB T2N 1N4, Canada; Department of Radiology, University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, CanadaDepartment of Clinical Neurosciences, University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, Canada; Hotchkiss Brain Institute, Cumming School of Medicine, University of Calgary, Calgary, 3330 Hospital Dr NW, Calgary, AB T2N 1N4, CanadaDivision of Neurology, Department of Medicine, and Neuroscience and Mental Health Institute, University of Alberta, 7-112 Clinical Sciences Building 11350 83rd Avenue, Edmonton, Alberta, AB T6G 2G3, CanadaDepartment of Clinical Neurosciences, University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, Canada; Hotchkiss Brain Institute, Cumming School of Medicine, University of Calgary, Calgary, 3330 Hospital Dr NW, Calgary, AB T2N 1N4, Canada; Department of Psychiatry, University of Calgary, 3280 Hospital Dr NW, Calgary, AB T2N 4Z6, CanadaDepartment of Clinical Neurosciences, University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, Canada; Hotchkiss Brain Institute, Cumming School of Medicine, University of Calgary, Calgary, 3330 Hospital Dr NW, Calgary, AB T2N 1N4, Canada; Department of Radiology, University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, Canada; Alberta Children’s Hospital Research Institute, University of Calgary, Heritage Medical Research Building, 3330 Hospital Dr. NW, Calgary, AB T2N 4N1, CanadaDepartment of Clinical Neurosciences, University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, Canada; Hotchkiss Brain Institute, Cumming School of Medicine, University of Calgary, Calgary, 3330 Hospital Dr NW, Calgary, AB T2N 1N4, Canada; Centre de recherche de l’Institut universitaire de gériatrie de Montréal, 4565 Chemin Queen Mary, Montréal, QC H3W 1W5, Canada; Department of Radiology, University of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, Canada; Département de radiologie, radio-oncologie et médecine nucléaire, Faculté de médecine, Université de Montréal, Pavillon Roger-Gaudry, 2900 boulevard, Édouard-Montpetit, Montréal, QC H3T 1A4, CanadaIntroduction: Brain atrophy in Parkinson’s disease occurs to varying degrees in different brain regions, even at the early stage of the disease. While cortical morphological features are often considered independently in structural brain imaging studies, research on the co-progression of different cortical morphological measurements could provide new insights regarding the progression of PD. This study’s aim was to examine the interplay between cortical curvature and thickness as a function of PD diagnosis, motor symptoms, and cognitive performance. Methods: A total of 359 de novo PD patients and 159 healthy controls (HC) from the Parkinson’s Progression Markers Initiative (PPMI) database were included in this study. Additionally, an independent cohort from four databases (182 PD, 132 HC) with longer disease durations was included to assess the effects of PD diagnosis in more advanced cases. Pearson correlation was used to determine subject-specific associations between cortical curvature and thickness estimated from T1-weighted MRI images. General linear modeling (GLM) was then used to assess the effect of PD diagnosis, motor symptoms, and cognitive performance on the curvature-thickness association. Next, longitudinal changes in the curvature-thickness correlation as well as the predictive effect of the cortical curvature-thickness association on changes in motor symptoms and cognitive performance across four years were investigated. Finally, Akaike information criterion (AIC) was used to build a GLM to model PD motor symptom severity cross-sectionally. Results: A significant interaction effect between PD motor symptoms and age on the curvature-thickness correlation was found (βstandardized = 0.11; t(350) = 2.12; p = 0.03). This interaction effect showed that motor symptoms in older patients were related to an attenuated curvature-thickness association. No significant effect of PD diagnosis was observed for the PPMI database (β = 0.03; t(510) = 0.35; p = 0.72). However, in patients with a longer disease duration, a significant effect of diagnosis on the curvature-thickness association was found (βstandardized = 0.31; t(306.7) = 3.49; p = 0.0006). Moreover, rigidity, but not tremor, in PD was significantly related to the curvature-thickness correlation (βstandardized = 0.11, t(350) = 2.24, p = 0.03; βstandardized = -0.03, t(350) = -0.58, p = 0.56, respectively). The curvature-thickness association was attenuated over time in both PD and HC, but the two groups did not show a significantly different effect (βstandardized = 0.03, t(184.7) = 0.78, p = 0.44). No predictive effects of the CC-CT correlation on longitudinal changes in cognitive performance or motor symptoms were observed (all p-values > 0.05). The best cross-sectional model for PD motor symptoms included the curvature-thickness correlation, cognitive performance, and putamen dopamine transporter (DAT) binding, which together explained 14 % of variance. Conclusion: The association between cortical curvature and thickness is related to PD motor symptoms and age. This research shows the potential of modeling the curvature-thickness interplay in PD.http://www.sciencedirect.com/science/article/pii/S2213158222003655Cortical brain morphologyStructural MRIParkinson’s diseaseMotor symptomsCognitive performance
spellingShingle Hannes Almgren
Alexandru Hanganu
Milton Camacho
Mekale Kibreab
Richard Camicioli
Zahinoor Ismail
Nils D. Forkert
Oury Monchi
Motor symptoms in Parkinson’s disease are related to the interplay between cortical curvature and thickness
NeuroImage: Clinical
Cortical brain morphology
Structural MRI
Parkinson’s disease
Motor symptoms
Cognitive performance
title Motor symptoms in Parkinson’s disease are related to the interplay between cortical curvature and thickness
title_full Motor symptoms in Parkinson’s disease are related to the interplay between cortical curvature and thickness
title_fullStr Motor symptoms in Parkinson’s disease are related to the interplay between cortical curvature and thickness
title_full_unstemmed Motor symptoms in Parkinson’s disease are related to the interplay between cortical curvature and thickness
title_short Motor symptoms in Parkinson’s disease are related to the interplay between cortical curvature and thickness
title_sort motor symptoms in parkinson s disease are related to the interplay between cortical curvature and thickness
topic Cortical brain morphology
Structural MRI
Parkinson’s disease
Motor symptoms
Cognitive performance
url http://www.sciencedirect.com/science/article/pii/S2213158222003655
work_keys_str_mv AT hannesalmgren motorsymptomsinparkinsonsdiseasearerelatedtotheinterplaybetweencorticalcurvatureandthickness
AT alexandruhanganu motorsymptomsinparkinsonsdiseasearerelatedtotheinterplaybetweencorticalcurvatureandthickness
AT miltoncamacho motorsymptomsinparkinsonsdiseasearerelatedtotheinterplaybetweencorticalcurvatureandthickness
AT mekalekibreab motorsymptomsinparkinsonsdiseasearerelatedtotheinterplaybetweencorticalcurvatureandthickness
AT richardcamicioli motorsymptomsinparkinsonsdiseasearerelatedtotheinterplaybetweencorticalcurvatureandthickness
AT zahinoorismail motorsymptomsinparkinsonsdiseasearerelatedtotheinterplaybetweencorticalcurvatureandthickness
AT nilsdforkert motorsymptomsinparkinsonsdiseasearerelatedtotheinterplaybetweencorticalcurvatureandthickness
AT ourymonchi motorsymptomsinparkinsonsdiseasearerelatedtotheinterplaybetweencorticalcurvatureandthickness