Longitudinal changes in movement-related functional MRI activity in Parkinson's disease patients

Naomi Hannaway; Nicholas P. Lao-Kaim; Antonio Martín-Bastida; Andreas Antonios Roussakis; Jonathan Howard; Matthew B. Wall; Clare Loane; Roger A. Barker; Paola Piccini

doi:10.1016/j.parkreldis.2021.04.025

Longitudinal changes in movement-related functional MRI activity in Parkinson's disease patients

Naomi Hannaway, Nicholas P. Lao-Kaim, Antonio Martín-Bastida, Andreas Antonios Roussakis, Jonathan Howard, Matthew B. Wall, Clare Loane, Roger A. Barker, Paola Piccini^*

^*Corresponding author for this work

Neuroimaging

Research output: Contribution to journal › Article › peer-review

4 Citations (Scopus)

Abstract

Introduction: Functional brain imaging has shown alterations in the basal ganglia, cortex and cerebellum in Parkinson's disease patients. However, few functional imaging studies have tested how these changes evolve over time. Our study aimed to test the longitudinal progression of movement-related functional activity in Parkinson's disease patients. Methods: At baseline, 48 Parkinson's disease patients and 16 healthy controls underwent structural and functional magnetic resonance imaging during a joystick motor task. Patients had repeated imaging after 18-months (n = 42) and 36-months (n = 32). T-tests compared functional responses between Parkinson's disease patients and controls, and linear mixed effects models examined longitudinal differences within Parkinson's disease. Correlations of motor-activity with bradykinesia, rigidity and tremor were undertaken. All contrasts used whole-brain analyses, thresholded at Z > 3.1 with a cluster-wise P < 0.05. Results: Baseline activation was significantly greater in patients than controls across contralateral parietal and occipital regions, ipsilateral precentral gyrus and thalamus. Longitudinally, patients showed significant increases in cerebellar activity at successive visits following baseline. Task-related activity also increased in the contralateral motor, parietal and temporal areas at 36 months compared to baseline, however this was reduced when controlling for motor task performance. Conclusion: We have shown that there are changes over time in the blood-activation level dependent response of patients with Parkinson's disease undertaking a simple motor task. These changes are observed primarily in the ipsilateral cerebellum and may be compensatory in nature.

Original language	English
Pages (from-to)	61-69
Number of pages	9
Journal	Parkinsonism and Related Disorders
Volume	87
DOIs	https://doi.org/10.1016/j.parkreldis.2021.04.025
Publication status	Published - Jun 2021

Keywords

fMRI
Movement disorders
Parkinson's disease

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10.1016/j.parkreldis.2021.04.025

Cite this

@article{7eeffb1cc74b4fe59e7f859662195b19,

title = "Longitudinal changes in movement-related functional MRI activity in Parkinson's disease patients",

abstract = "Introduction: Functional brain imaging has shown alterations in the basal ganglia, cortex and cerebellum in Parkinson's disease patients. However, few functional imaging studies have tested how these changes evolve over time. Our study aimed to test the longitudinal progression of movement-related functional activity in Parkinson's disease patients. Methods: At baseline, 48 Parkinson's disease patients and 16 healthy controls underwent structural and functional magnetic resonance imaging during a joystick motor task. Patients had repeated imaging after 18-months (n = 42) and 36-months (n = 32). T-tests compared functional responses between Parkinson's disease patients and controls, and linear mixed effects models examined longitudinal differences within Parkinson's disease. Correlations of motor-activity with bradykinesia, rigidity and tremor were undertaken. All contrasts used whole-brain analyses, thresholded at Z > 3.1 with a cluster-wise P < 0.05. Results: Baseline activation was significantly greater in patients than controls across contralateral parietal and occipital regions, ipsilateral precentral gyrus and thalamus. Longitudinally, patients showed significant increases in cerebellar activity at successive visits following baseline. Task-related activity also increased in the contralateral motor, parietal and temporal areas at 36 months compared to baseline, however this was reduced when controlling for motor task performance. Conclusion: We have shown that there are changes over time in the blood-activation level dependent response of patients with Parkinson's disease undertaking a simple motor task. These changes are observed primarily in the ipsilateral cerebellum and may be compensatory in nature.",

keywords = "fMRI, Movement disorders, Parkinson's disease",

author = "Naomi Hannaway and Lao-Kaim, {Nicholas P.} and Antonio Mart{\'i}n-Bastida and Roussakis, {Andreas Antonios} and Jonathan Howard and Wall, {Matthew B.} and Clare Loane and Barker, {Roger A.} and Paola Piccini",

note = "Funding Information: At baseline, 48 patients with idiopathic PD were recruited from a larger observational cohort [7] Of these, 42 had repeated imaging 20.16 ? 3.52 months later and 32 returned for a third visit, 38.18 ? 4.15 months after baseline. All PD patients satisfied Queen Square Brain Bank criteria for the diagnosis of idiopathic PD, and were on no- or standard- PD medication at baseline [8]. The diagnosis of PD remained the same throughout the study, with no participants showing symptoms consistent with atypical parkinsonism. No participants reported significant motor fluctuations. 16 HC were scanned at baseline only. All volunteers were right-handed, free from significant cognitive impairment (Mini-Mental State Examination >26) and other ongoing neurological or psychiatric disorders. For more detailed information about the inclusion/exclusion criteria see Barker et al. (2019) [7]. Data were collected under funding from the FP7 EC Transeuro research project. All participants gave informed consent and research was carried out in accordance with the declaration of Helsinki. Appropriate approvals were obtained by the local National Research Ethics Service Committee and the Joint Research Compliance Office of Imperial College London.This research received funding from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007?2013) [FP7?242003]. Infrastructure support for this research was provided by the NIHR Imperial Biomedical Research Centre and the NIHR Imperial CRF, Imperial College Healthcare NHS Trust. The views expressed are those of the authors and not necessarily those of the funder, the NHS, the NIHR, or the department of Health. The authors thank Gang Chen for his assistance with implementing 3dLME. We would also like to thank all the patients and volunteers who took part in this study. Funding Information: At baseline, 48 patients with idiopathic PD were recruited from a larger observational cohort [ 7 ] Of these, 42 had repeated imaging 20.16 ± 3.52 months later and 32 returned for a third visit, 38.18 ± 4.15 months after baseline. All PD patients satisfied Queen Square Brain Bank criteria for the diagnosis of idiopathic PD, and were on no- or standard- PD medication at baseline [ 8 ]. The diagnosis of PD remained the same throughout the study, with no participants showing symptoms consistent with atypical parkinsonism. No participants reported significant motor fluctuations. 16 HC were scanned at baseline only. All volunteers were right-handed, free from significant cognitive impairment (Mini-Mental State Examination >26) and other ongoing neurological or psychiatric disorders. For more detailed information about the inclusion/exclusion criteria see Barker et al. (2019) [ 7 ]. Data were collected under funding from the FP7 EC Transeuro research project. All participants gave informed consent and research was carried out in accordance with the declaration of Helsinki. Appropriate approvals were obtained by the local National Research Ethics Service Committee and the Joint Research Compliance Office of Imperial College London. Funding Information: This research received funding from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007–2013) [ FP7–242003 ]. Infrastructure support for this research was provided by the NIHR Imperial Biomedical Research Centre and the NIHR Imperial CRF , Imperial College Healthcare NHS Trust . The views expressed are those of the authors and not necessarily those of the funder, the NHS, the NIHR, or the department of Health. The authors thank Gang Chen for his assistance with implementing 3dLME. We would also like to thank all the patients and volunteers who took part in this study. Publisher Copyright: {\textcopyright} 2021 Elsevier Ltd Copyright: Copyright 2021 Elsevier B.V., All rights reserved.",

year = "2021",

month = jun,

doi = "10.1016/j.parkreldis.2021.04.025",

language = "English",

volume = "87",

pages = "61--69",

journal = "Parkinsonism and Related Disorders",

issn = "1353-8020",

publisher = "Elsevier",

}

TY - JOUR

T1 - Longitudinal changes in movement-related functional MRI activity in Parkinson's disease patients

AU - Hannaway, Naomi

AU - Lao-Kaim, Nicholas P.

AU - Martín-Bastida, Antonio

AU - Roussakis, Andreas Antonios

AU - Howard, Jonathan

AU - Wall, Matthew B.

AU - Loane, Clare

AU - Barker, Roger A.

AU - Piccini, Paola

N1 - Funding Information: At baseline, 48 patients with idiopathic PD were recruited from a larger observational cohort [7] Of these, 42 had repeated imaging 20.16 ? 3.52 months later and 32 returned for a third visit, 38.18 ? 4.15 months after baseline. All PD patients satisfied Queen Square Brain Bank criteria for the diagnosis of idiopathic PD, and were on no- or standard- PD medication at baseline [8]. The diagnosis of PD remained the same throughout the study, with no participants showing symptoms consistent with atypical parkinsonism. No participants reported significant motor fluctuations. 16 HC were scanned at baseline only. All volunteers were right-handed, free from significant cognitive impairment (Mini-Mental State Examination >26) and other ongoing neurological or psychiatric disorders. For more detailed information about the inclusion/exclusion criteria see Barker et al. (2019) [7]. Data were collected under funding from the FP7 EC Transeuro research project. All participants gave informed consent and research was carried out in accordance with the declaration of Helsinki. Appropriate approvals were obtained by the local National Research Ethics Service Committee and the Joint Research Compliance Office of Imperial College London.This research received funding from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007?2013) [FP7?242003]. Infrastructure support for this research was provided by the NIHR Imperial Biomedical Research Centre and the NIHR Imperial CRF, Imperial College Healthcare NHS Trust. The views expressed are those of the authors and not necessarily those of the funder, the NHS, the NIHR, or the department of Health. The authors thank Gang Chen for his assistance with implementing 3dLME. We would also like to thank all the patients and volunteers who took part in this study. Funding Information: At baseline, 48 patients with idiopathic PD were recruited from a larger observational cohort [ 7 ] Of these, 42 had repeated imaging 20.16 ± 3.52 months later and 32 returned for a third visit, 38.18 ± 4.15 months after baseline. All PD patients satisfied Queen Square Brain Bank criteria for the diagnosis of idiopathic PD, and were on no- or standard- PD medication at baseline [ 8 ]. The diagnosis of PD remained the same throughout the study, with no participants showing symptoms consistent with atypical parkinsonism. No participants reported significant motor fluctuations. 16 HC were scanned at baseline only. All volunteers were right-handed, free from significant cognitive impairment (Mini-Mental State Examination >26) and other ongoing neurological or psychiatric disorders. For more detailed information about the inclusion/exclusion criteria see Barker et al. (2019) [ 7 ]. Data were collected under funding from the FP7 EC Transeuro research project. All participants gave informed consent and research was carried out in accordance with the declaration of Helsinki. Appropriate approvals were obtained by the local National Research Ethics Service Committee and the Joint Research Compliance Office of Imperial College London. Funding Information: This research received funding from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007–2013) [ FP7–242003 ]. Infrastructure support for this research was provided by the NIHR Imperial Biomedical Research Centre and the NIHR Imperial CRF , Imperial College Healthcare NHS Trust . The views expressed are those of the authors and not necessarily those of the funder, the NHS, the NIHR, or the department of Health. The authors thank Gang Chen for his assistance with implementing 3dLME. We would also like to thank all the patients and volunteers who took part in this study. Publisher Copyright: © 2021 Elsevier Ltd Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

PY - 2021/6

Y1 - 2021/6

N2 - Introduction: Functional brain imaging has shown alterations in the basal ganglia, cortex and cerebellum in Parkinson's disease patients. However, few functional imaging studies have tested how these changes evolve over time. Our study aimed to test the longitudinal progression of movement-related functional activity in Parkinson's disease patients. Methods: At baseline, 48 Parkinson's disease patients and 16 healthy controls underwent structural and functional magnetic resonance imaging during a joystick motor task. Patients had repeated imaging after 18-months (n = 42) and 36-months (n = 32). T-tests compared functional responses between Parkinson's disease patients and controls, and linear mixed effects models examined longitudinal differences within Parkinson's disease. Correlations of motor-activity with bradykinesia, rigidity and tremor were undertaken. All contrasts used whole-brain analyses, thresholded at Z > 3.1 with a cluster-wise P < 0.05. Results: Baseline activation was significantly greater in patients than controls across contralateral parietal and occipital regions, ipsilateral precentral gyrus and thalamus. Longitudinally, patients showed significant increases in cerebellar activity at successive visits following baseline. Task-related activity also increased in the contralateral motor, parietal and temporal areas at 36 months compared to baseline, however this was reduced when controlling for motor task performance. Conclusion: We have shown that there are changes over time in the blood-activation level dependent response of patients with Parkinson's disease undertaking a simple motor task. These changes are observed primarily in the ipsilateral cerebellum and may be compensatory in nature.

AB - Introduction: Functional brain imaging has shown alterations in the basal ganglia, cortex and cerebellum in Parkinson's disease patients. However, few functional imaging studies have tested how these changes evolve over time. Our study aimed to test the longitudinal progression of movement-related functional activity in Parkinson's disease patients. Methods: At baseline, 48 Parkinson's disease patients and 16 healthy controls underwent structural and functional magnetic resonance imaging during a joystick motor task. Patients had repeated imaging after 18-months (n = 42) and 36-months (n = 32). T-tests compared functional responses between Parkinson's disease patients and controls, and linear mixed effects models examined longitudinal differences within Parkinson's disease. Correlations of motor-activity with bradykinesia, rigidity and tremor were undertaken. All contrasts used whole-brain analyses, thresholded at Z > 3.1 with a cluster-wise P < 0.05. Results: Baseline activation was significantly greater in patients than controls across contralateral parietal and occipital regions, ipsilateral precentral gyrus and thalamus. Longitudinally, patients showed significant increases in cerebellar activity at successive visits following baseline. Task-related activity also increased in the contralateral motor, parietal and temporal areas at 36 months compared to baseline, however this was reduced when controlling for motor task performance. Conclusion: We have shown that there are changes over time in the blood-activation level dependent response of patients with Parkinson's disease undertaking a simple motor task. These changes are observed primarily in the ipsilateral cerebellum and may be compensatory in nature.

KW - fMRI

KW - Movement disorders

KW - Parkinson's disease

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U2 - 10.1016/j.parkreldis.2021.04.025

DO - 10.1016/j.parkreldis.2021.04.025

M3 - Article

AN - SCOPUS:85105508519

SN - 1353-8020

VL - 87

SP - 61

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JO - Parkinsonism and Related Disorders

JF - Parkinsonism and Related Disorders

ER -

Longitudinal changes in movement-related functional MRI activity in Parkinson's disease patients

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Keywords

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