Characterizing upper extremity fine motor function in the presence of white matter hyperintensities: A 7 T MRI cross-sectional study in older adults

Background: White matter hyperintensities (WMH) are a prevalent radiographic finding in the aging brain studies. Research on WMH association with motor impairment is mostly focused on the lower-extremity function and further investigation on the upper-extremity is needed. How different degrees of WM...

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Main Authors: Riccardo Iandolo, Esin Avci, Giulia Bommarito, Ioanna Sandvig, Gitta Rohweder, Axel Sandvig
Format: Article
Language:English
Published: Elsevier 2024-01-01
Series:NeuroImage: Clinical
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213158224000081
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author Riccardo Iandolo
Esin Avci
Giulia Bommarito
Ioanna Sandvig
Gitta Rohweder
Axel Sandvig
author_facet Riccardo Iandolo
Esin Avci
Giulia Bommarito
Ioanna Sandvig
Gitta Rohweder
Axel Sandvig
author_sort Riccardo Iandolo
collection DOAJ
description Background: White matter hyperintensities (WMH) are a prevalent radiographic finding in the aging brain studies. Research on WMH association with motor impairment is mostly focused on the lower-extremity function and further investigation on the upper-extremity is needed. How different degrees of WMH burden impact the network of activation recruited during upper limb motor performance could provide further insight on the complex mechanisms of WMH pathophysiology and its interaction with aging and neurological disease processes. Methods: 40 healthy elderly subjects without a neurological/psychiatric diagnosis were included in the study (16F, mean age 69.3 years). All subjects underwent ultra-high field 7 T MRI including structural and finger tapping task-fMRI. First, we quantified the WMH lesion load and its spatial distribution. Secondly, we performed a data-driven stratification of the subjects according to their periventricular and deep WMH burdens. Thirdly, we investigated the distribution of neural recruitment and the corresponding activity assessed through BOLD signal changes among different brain regions for groups of subjects. We clustered the degree of WMH based on location, numbers, and volume into three categories; ranging from mild, moderate, and severe. Finally, we explored how the spatial distribution of WMH, and activity elicited during task-fMRI relate to motor function, measured with the 9-Hole Peg Test. Results: Within our population, we found three subgroups of subjects, partitioned according to their periventricular and deep WMH lesion load. We found decreased activity in several frontal and cingulate cortex areas in subjects with a severe WMH burden. No statistically significant associations were found when performing the brain-behavior statistical analysis for structural or functional data. Conclusion: WMH burden has an effect on brain activity during fine motor control and the activity changes are associated with varying degrees of the total burden and distributions of WMH lesions. Collectively, our results shed new light on the potential impact of WMH on motor function in the context of aging and neurodegeneration.
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spelling doaj.art-e90b76d695fb486daea7affdc8c9e0e82024-03-13T04:45:37ZengElsevierNeuroImage: Clinical2213-15822024-01-0141103569Characterizing upper extremity fine motor function in the presence of white matter hyperintensities: A 7 T MRI cross-sectional study in older adultsRiccardo Iandolo0Esin Avci1Giulia Bommarito2Ioanna Sandvig3Gitta Rohweder4Axel Sandvig5Department of Neuromedicine and Movement Science, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology (NTNU), Trondheim, Norway; Corresponding authors at: Department of Neuromedicine and Movement Science, Edvard Griegs gate 8, 7030 Trondheim, Norway.Department of Neuromedicine and Movement Science, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology (NTNU), Trondheim, Norway; Corresponding authors at: Department of Neuromedicine and Movement Science, Edvard Griegs gate 8, 7030 Trondheim, Norway.Department of Clinical Neurosciences, Lausanne University Hospital and University of Lausanne, Lausanne, SwitzerlandDepartment of Neuromedicine and Movement Science, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology (NTNU), Trondheim, NorwayDepartment of Neuromedicine and Movement Science, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology (NTNU), Trondheim, Norway; Stroke Unit, Department of Medicine, St Olav’s University Hospital, Trondheim, NorwayDepartment of Neuromedicine and Movement Science, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology (NTNU), Trondheim, Norway; Department of Neurology and Clinical Neurophysiology, St. Olav’s University Hospital, Trondheim, Norway; Department of Clinical Neurosciences, Division of Neuro, Head and Neck, Umeå University Hospital, Umeå, Sweden; Department of Community Medicine and Rehabilitation, Umeå University Hospital, Umeå, Sweden; Corresponding authors at: Department of Neuromedicine and Movement Science, Edvard Griegs gate 8, 7030 Trondheim, Norway.Background: White matter hyperintensities (WMH) are a prevalent radiographic finding in the aging brain studies. Research on WMH association with motor impairment is mostly focused on the lower-extremity function and further investigation on the upper-extremity is needed. How different degrees of WMH burden impact the network of activation recruited during upper limb motor performance could provide further insight on the complex mechanisms of WMH pathophysiology and its interaction with aging and neurological disease processes. Methods: 40 healthy elderly subjects without a neurological/psychiatric diagnosis were included in the study (16F, mean age 69.3 years). All subjects underwent ultra-high field 7 T MRI including structural and finger tapping task-fMRI. First, we quantified the WMH lesion load and its spatial distribution. Secondly, we performed a data-driven stratification of the subjects according to their periventricular and deep WMH burdens. Thirdly, we investigated the distribution of neural recruitment and the corresponding activity assessed through BOLD signal changes among different brain regions for groups of subjects. We clustered the degree of WMH based on location, numbers, and volume into three categories; ranging from mild, moderate, and severe. Finally, we explored how the spatial distribution of WMH, and activity elicited during task-fMRI relate to motor function, measured with the 9-Hole Peg Test. Results: Within our population, we found three subgroups of subjects, partitioned according to their periventricular and deep WMH lesion load. We found decreased activity in several frontal and cingulate cortex areas in subjects with a severe WMH burden. No statistically significant associations were found when performing the brain-behavior statistical analysis for structural or functional data. Conclusion: WMH burden has an effect on brain activity during fine motor control and the activity changes are associated with varying degrees of the total burden and distributions of WMH lesions. Collectively, our results shed new light on the potential impact of WMH on motor function in the context of aging and neurodegeneration.http://www.sciencedirect.com/science/article/pii/S2213158224000081AgingNeurodegenerationMotor impairmentHigh-resolution MRILeukoaraiosis
spellingShingle Riccardo Iandolo
Esin Avci
Giulia Bommarito
Ioanna Sandvig
Gitta Rohweder
Axel Sandvig
Characterizing upper extremity fine motor function in the presence of white matter hyperintensities: A 7 T MRI cross-sectional study in older adults
NeuroImage: Clinical
Aging
Neurodegeneration
Motor impairment
High-resolution MRI
Leukoaraiosis
title Characterizing upper extremity fine motor function in the presence of white matter hyperintensities: A 7 T MRI cross-sectional study in older adults
title_full Characterizing upper extremity fine motor function in the presence of white matter hyperintensities: A 7 T MRI cross-sectional study in older adults
title_fullStr Characterizing upper extremity fine motor function in the presence of white matter hyperintensities: A 7 T MRI cross-sectional study in older adults
title_full_unstemmed Characterizing upper extremity fine motor function in the presence of white matter hyperintensities: A 7 T MRI cross-sectional study in older adults
title_short Characterizing upper extremity fine motor function in the presence of white matter hyperintensities: A 7 T MRI cross-sectional study in older adults
title_sort characterizing upper extremity fine motor function in the presence of white matter hyperintensities a 7 t mri cross sectional study in older adults
topic Aging
Neurodegeneration
Motor impairment
High-resolution MRI
Leukoaraiosis
url http://www.sciencedirect.com/science/article/pii/S2213158224000081
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