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Published in: Neurological Sciences 10/2022

15-07-2022 | Magnetic Resonance Imaging | Original Article

Functional brain changes in Parkinson’s disease: a whole brain ALE study

Authors: Lihua Gu, Hao Shu, Hui Xu, Yanjuan Wang

Published in: Neurological Sciences | Issue 10/2022

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Abstract

Background

Resting-state functional magnetic resonance imaging (rs-fMRI) was widely used as an effective tool in the diagnosis of neurodegenerative diseases. However, prior rs-fMRI studies reported inconsistent results for comparison between Parkinson’s disease (PD) and healthy controls (HC).

Methods

We searched studies published before December 2021 in databases (PubMed, Web of Science, and Google Scholar). An activation likelihood estimation (ALE) meta-analysis was made for functional changes in PD.

Results

The study finally included 25 studies (including 973 PD patients and 766 HC). PD patients showed reduced amplitude of low frequency fluctuations (ALFF) in the left superior temporal gyrus (STG), the left superior frontal gyrus (SFG), the left medial frontal gyrus (MFG), the left precuneus (PCUN), and the right lentiform nucleus, compared to HC. PD patients showed increased ALFF in the right SFG, the left superior parietal lobule (SPL), the left STG, the right fusiform gyrus, the left inferior temporal gyrus (ITG), and the right parahippocampal gyrus (PHG), compared to HC. PD patients showed reduced regional homogeneity (ReHo) in the right declive, the right MFG, the left culmen, and the left thalamus, compared to HC. PD patients showed increased ReHo in the right SFG, compared to HC. Additionally, PD patients showed reduced functional connectivity (FC) in the right posterior cingulate (PCG), compared to HC.

Conclusions

The present ALE analysis has confirmed functional deficits in motor-, emotion-, and cognition-related regions in PD. Deficits in these regions in rs-fMRI studies could play a role in early diagnosis of PD.
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Literature
1.
go back to reference Kalia LV, Lang AE (2015) Parkinson’s disease. Lancet (London, England) 386(9996):896–912CrossRef Kalia LV, Lang AE (2015) Parkinson’s disease. Lancet (London, England) 386(9996):896–912CrossRef
2.
go back to reference Global, regional, and national burden of Parkinson’s disease, (1990–20160) (2018) a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol 17(11):939–53CrossRef Global, regional, and national burden of Parkinson’s disease, (1990–20160) (2018) a systematic analysis for the Global Burden of Disease Study 2016. Lancet Neurol 17(11):939–53CrossRef
3.
go back to reference Gu L, Zhang Z (2019) Exploring structural and functional brain changes in mild cognitive impairment: a whole brain ALE meta-analysis for multimodal MRI. ACS Chem Neurosci 10(6):2823–9PubMedCrossRef Gu L, Zhang Z (2019) Exploring structural and functional brain changes in mild cognitive impairment: a whole brain ALE meta-analysis for multimodal MRI. ACS Chem Neurosci 10(6):2823–9PubMedCrossRef
4.
go back to reference Li Y, Liang P, Jia X et al (2016) Abnormal regional homogeneity in Parkinson’s disease: a resting state fMRI study. Clin Radiol 71(1):e28-34PubMedCrossRef Li Y, Liang P, Jia X et al (2016) Abnormal regional homogeneity in Parkinson’s disease: a resting state fMRI study. Clin Radiol 71(1):e28-34PubMedCrossRef
5.
go back to reference Choe IH, Yeo S, Chung KC et al (2013) Decreased and increased cerebral regional homogeneity in early Parkinson’s disease. Brain Res 1527:230–7PubMedCrossRef Choe IH, Yeo S, Chung KC et al (2013) Decreased and increased cerebral regional homogeneity in early Parkinson’s disease. Brain Res 1527:230–7PubMedCrossRef
6.
go back to reference Yang H, Zhou XJ, Zhang MM et al (2013) Changes in spontaneous brain activity in early Parkinson’s disease. Neurosci Lett 549:24–8PubMedCrossRef Yang H, Zhou XJ, Zhang MM et al (2013) Changes in spontaneous brain activity in early Parkinson’s disease. Neurosci Lett 549:24–8PubMedCrossRef
7.
go back to reference Moher D, Liberati A, Tetzlaff J et al (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Annal Internal Med 151(4):264–9 w64CrossRef Moher D, Liberati A, Tetzlaff J et al (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Annal Internal Med 151(4):264–9 w64CrossRef
8.
go back to reference Laird AR, Robinson JL, McMillan KM et al (2010) Comparison of the disparity between Talairach and MNI coordinates in functional neuroimaging data: validation of the Lancaster transform. Neuroimage 51(2):677–683PubMedCrossRef Laird AR, Robinson JL, McMillan KM et al (2010) Comparison of the disparity between Talairach and MNI coordinates in functional neuroimaging data: validation of the Lancaster transform. Neuroimage 51(2):677–683PubMedCrossRef
9.
go back to reference Lancaster JL, Tordesillas-Gutierrez D, Martinez M et al (2007) Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum Brain Mapp 28(11):1194–1205PubMedPubMedCentralCrossRef Lancaster JL, Tordesillas-Gutierrez D, Martinez M et al (2007) Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum Brain Mapp 28(11):1194–1205PubMedPubMedCentralCrossRef
10.
go back to reference Turkeltaub PE, Eickhoff SB, Laird AR et al (2012) Minimizing within-experiment and within-group effects in Activation Likelihood Estimation meta-analyses. Hum Brain Mapp 33(1):1–13PubMedCrossRef Turkeltaub PE, Eickhoff SB, Laird AR et al (2012) Minimizing within-experiment and within-group effects in Activation Likelihood Estimation meta-analyses. Hum Brain Mapp 33(1):1–13PubMedCrossRef
11.
go back to reference Wu T, Long X, Zang Y et al (2009) Regional homogeneity changes in patients with Parkinson’s disease. Hum Brain Mapp 30(5):1502–1510PubMedCrossRef Wu T, Long X, Zang Y et al (2009) Regional homogeneity changes in patients with Parkinson’s disease. Hum Brain Mapp 30(5):1502–1510PubMedCrossRef
12.
go back to reference Kwak Y, Peltier SJ, Bohnen NI et al (2012) L-DOPA changes spontaneous low-frequency BOLD signal oscillations in Parkinson’s disease: a resting state fMRI study. Front Syst Neurosci 6:52PubMedPubMedCentralCrossRef Kwak Y, Peltier SJ, Bohnen NI et al (2012) L-DOPA changes spontaneous low-frequency BOLD signal oscillations in Parkinson’s disease: a resting state fMRI study. Front Syst Neurosci 6:52PubMedPubMedCentralCrossRef
14.
go back to reference Skidmore FM, Yang M, Baxter L et al (2013) Reliability analysis of the resting state can sensitively and specifically identify the presence of Parkinson disease. NeuroImage 75:249–61PubMedCrossRef Skidmore FM, Yang M, Baxter L et al (2013) Reliability analysis of the resting state can sensitively and specifically identify the presence of Parkinson disease. NeuroImage 75:249–61PubMedCrossRef
15.
go back to reference Wen X, Wu X, Liu J et al (2013) Abnormal baseline brain activity in non-depressed Parkinson’s disease and depressed Parkinson’s disease: a resting-state functional magnetic resonance imaging study. PLoS ONE 8(5):e63691PubMedPubMedCentralCrossRef Wen X, Wu X, Liu J et al (2013) Abnormal baseline brain activity in non-depressed Parkinson’s disease and depressed Parkinson’s disease: a resting-state functional magnetic resonance imaging study. PLoS ONE 8(5):e63691PubMedPubMedCentralCrossRef
16.
go back to reference Zhang J, Wei L, Hu X et al (2013) Specific frequency band of amplitude low-frequency fl uctuation predicts Parkinson’s disease. Behav Brain Res 252:18–23PubMedCrossRef Zhang J, Wei L, Hu X et al (2013) Specific frequency band of amplitude low-frequency fl uctuation predicts Parkinson’s disease. Behav Brain Res 252:18–23PubMedCrossRef
18.
go back to reference Luo C, Chen Q, Song W et al (2014) Resting-state fMRI study on drug-naive patients with Parkinson’s disease and with depression. J Neurol Neurosurg Psychiatr 85(6):675–683CrossRef Luo C, Chen Q, Song W et al (2014) Resting-state fMRI study on drug-naive patients with Parkinson’s disease and with depression. J Neurol Neurosurg Psychiatr 85(6):675–683CrossRef
19.
go back to reference Sheng K, Fang W, Su M et al (2014) Altered spontaneous brain activity in patients with Parkinson’s disease accompanied by depressive symptoms, as revealed by regional homogeneity and functional connectivity in the prefrontal-limbic system. PLoS ONE 9(1):e84705PubMedPubMedCentralCrossRef Sheng K, Fang W, Su M et al (2014) Altered spontaneous brain activity in patients with Parkinson’s disease accompanied by depressive symptoms, as revealed by regional homogeneity and functional connectivity in the prefrontal-limbic system. PLoS ONE 9(1):e84705PubMedPubMedCentralCrossRef
20.
go back to reference Wei L, Zhang J, Long Z et al (2014) Reduced topological efficiency in cortical-basal ganglia motor network of Parkinson’s disease: a resting state fMRI study. PLoS ONE 9(10):e108124PubMedPubMedCentralCrossRef Wei L, Zhang J, Long Z et al (2014) Reduced topological efficiency in cortical-basal ganglia motor network of Parkinson’s disease: a resting state fMRI study. PLoS ONE 9(10):e108124PubMedPubMedCentralCrossRef
21.
go back to reference Borroni B, Premi E, Formenti A et al (2015) Structural and functional imaging study in dementia with Lewy bodies and Parkinson’s disease dementia. Parkinsonism Relat Disord 21(9):1049–1055PubMedCrossRef Borroni B, Premi E, Formenti A et al (2015) Structural and functional imaging study in dementia with Lewy bodies and Parkinson’s disease dementia. Parkinsonism Relat Disord 21(9):1049–1055PubMedCrossRef
22.
go back to reference Chen HM, Wang ZJ, Fang JP et al (2015) Different patterns of spontaneous brain activity between tremor-dominant and postural instability/gait difficulty subtypes of Parkinson’s disease: a resting-state fMRI study. CNS Neurosci Ther 21(10):855–866PubMedPubMedCentralCrossRef Chen HM, Wang ZJ, Fang JP et al (2015) Different patterns of spontaneous brain activity between tremor-dominant and postural instability/gait difficulty subtypes of Parkinson’s disease: a resting-state fMRI study. CNS Neurosci Ther 21(10):855–866PubMedPubMedCentralCrossRef
23.
go back to reference Hu XF, Zhang JQ, Jiang XM et al (2015) Amplitude of low-frequency oscillations in Parkinson’s disease: a 2-year longitudinal resting-state functional magnetic resonance imaging study. Chin Med J 128(5):593–601PubMedPubMedCentralCrossRef Hu XF, Zhang JQ, Jiang XM et al (2015) Amplitude of low-frequency oscillations in Parkinson’s disease: a 2-year longitudinal resting-state functional magnetic resonance imaging study. Chin Med J 128(5):593–601PubMedPubMedCentralCrossRef
24.
go back to reference Luo C, Guo X, Song W et al (2015) Decreased resting-state interhemispheric functional connectivity in Parkinson’s disease. BioMed Res Int 2015:692684PubMedPubMedCentral Luo C, Guo X, Song W et al (2015) Decreased resting-state interhemispheric functional connectivity in Parkinson’s disease. BioMed Res Int 2015:692684PubMedPubMedCentral
25.
go back to reference Wu T, Ma Y, Zheng Z et al (2015) Parkinson’s disease-related spatial covariance pattern identified with resting-state functional MRI. J Cereb Blood Flow Metab 35(11):1764–1770PubMedPubMedCentralCrossRef Wu T, Ma Y, Zheng Z et al (2015) Parkinson’s disease-related spatial covariance pattern identified with resting-state functional MRI. J Cereb Blood Flow Metab 35(11):1764–1770PubMedPubMedCentralCrossRef
26.
go back to reference Zhang J, Wei L, Hu X et al (2015) Akinetic-rigid and tremor-dominant Parkinson’s disease patients show different patterns of intrinsic brain activity. Parkinsonism Relat Disord 21(1):23–30PubMedCrossRef Zhang J, Wei L, Hu X et al (2015) Akinetic-rigid and tremor-dominant Parkinson’s disease patients show different patterns of intrinsic brain activity. Parkinsonism Relat Disord 21(1):23–30PubMedCrossRef
27.
go back to reference Tinaz S, Lauro P, Hallett M et al (2016) Deficits in task-set maintenance and execution networks in Parkinson’s disease. Brain Struct Funct 221(3):1413–1425PubMedCrossRef Tinaz S, Lauro P, Hallett M et al (2016) Deficits in task-set maintenance and execution networks in Parkinson’s disease. Brain Struct Funct 221(3):1413–1425PubMedCrossRef
28.
go back to reference Zhang JJ, Ding J, Li JY et al (2017) Abnormal resting-state neural activity and connectivity of fatigue in Parkinson’s disease. CNS Neurosci Ther 23(3):241–247PubMedPubMedCentralCrossRef Zhang JJ, Ding J, Li JY et al (2017) Abnormal resting-state neural activity and connectivity of fatigue in Parkinson’s disease. CNS Neurosci Ther 23(3):241–247PubMedPubMedCentralCrossRef
29.
go back to reference Zhou C, Zhong X, Yang Y et al (2018) Alterations of regional homogeneity in freezing of gait in Parkinson’s disease. J Neurol Sci 387:54 9CrossRef Zhou C, Zhong X, Yang Y et al (2018) Alterations of regional homogeneity in freezing of gait in Parkinson’s disease. J Neurol Sci 387:54 9CrossRef
30.
go back to reference Hu J, Xiao C, Gong D et al (2019) Regional homogeneity analysis of major Parkinson’s disease subtypes based on functional magnetic resonance imaging. Neurosci lett 706:81–7PubMedCrossRef Hu J, Xiao C, Gong D et al (2019) Regional homogeneity analysis of major Parkinson’s disease subtypes based on functional magnetic resonance imaging. Neurosci lett 706:81–7PubMedCrossRef
31.
go back to reference Li MG, Liu TF, Zhang TH et al (2020) Alterations of regional homogeneity in Parkinson’s disease with mild cognitive impairment: a preliminary resting-state fMRI study. Neuroradiology 62(3):327–34PubMedCrossRef Li MG, Liu TF, Zhang TH et al (2020) Alterations of regional homogeneity in Parkinson’s disease with mild cognitive impairment: a preliminary resting-state fMRI study. Neuroradiology 62(3):327–34PubMedCrossRef
32.
go back to reference Guo W, Jin W, Li N et al (2021) Brain activity alterations in patients with Parkinson’s disease with cognitive impairment based on resting-state functional MRI. Neurosci Lett 747:135672PubMedCrossRef Guo W, Jin W, Li N et al (2021) Brain activity alterations in patients with Parkinson’s disease with cognitive impairment based on resting-state functional MRI. Neurosci Lett 747:135672PubMedCrossRef
33.
go back to reference Li M-G, Liu T-F, Zhang T-H et al (2020) Alterations of regional homogeneity in Parkinson’s disease with mild cognitive impairment: a preliminary resting-state fMRI study. Neuroradiology 62(3):327–34PubMedCrossRef Li M-G, Liu T-F, Zhang T-H et al (2020) Alterations of regional homogeneity in Parkinson’s disease with mild cognitive impairment: a preliminary resting-state fMRI study. Neuroradiology 62(3):327–34PubMedCrossRef
34.
go back to reference Wang N, Edmiston EK, Luo X et al (2017) Comparing abnormalities of amplitude of low-frequency fluctuations in multiple system atrophy and idiopathic Parkinson’s disease measured with resting-state fMRI. Psychiatr Res Neuroimaging 269:73–81CrossRef Wang N, Edmiston EK, Luo X et al (2017) Comparing abnormalities of amplitude of low-frequency fluctuations in multiple system atrophy and idiopathic Parkinson’s disease measured with resting-state fMRI. Psychiatr Res Neuroimaging 269:73–81CrossRef
35.
go back to reference Burciu RG, Ofori E, Shukla P et al (2015) Distinct patterns of brain activity in progressive supranuclear palsy and Parkinson’s disease. Mov Dis : Off J Mov Disord Soc 30(9):1248–1258CrossRef Burciu RG, Ofori E, Shukla P et al (2015) Distinct patterns of brain activity in progressive supranuclear palsy and Parkinson’s disease. Mov Dis : Off J Mov Disord Soc 30(9):1248–1258CrossRef
36.
go back to reference Puckett AM, Bollmann S, Poser BA et al (2018) Using multi-echo simultaneous multi-slice (SMS) EPI to improve functional MRI of the subcortical nuclei of the basal ganglia at ultra-high field (7T). Neuroimage 172:886PubMedCrossRef Puckett AM, Bollmann S, Poser BA et al (2018) Using multi-echo simultaneous multi-slice (SMS) EPI to improve functional MRI of the subcortical nuclei of the basal ganglia at ultra-high field (7T). Neuroimage 172:886PubMedCrossRef
37.
go back to reference Sperling W, Ller MH (2011) Nucleus lentiformis–a new model for psychiatry? Med hypotheses 76(5):720–2PubMedCrossRef Sperling W, Ller MH (2011) Nucleus lentiformis–a new model for psychiatry? Med hypotheses 76(5):720–2PubMedCrossRef
38.
go back to reference Petrella JR, Sheldon FC, Prince SE et al (2011) Default mode network connectivity in stable vs progressive mild cognitive impairment. Neurology 76(6):511–517PubMedPubMedCentralCrossRef Petrella JR, Sheldon FC, Prince SE et al (2011) Default mode network connectivity in stable vs progressive mild cognitive impairment. Neurology 76(6):511–517PubMedPubMedCentralCrossRef
39.
go back to reference Pihlajamki M, Jauhiainen AM, Soininen H (2009) Structural and functional MRI in mild cognitive impairment. Curr Alzheimer Res 6(2):179–85CrossRef Pihlajamki M, Jauhiainen AM, Soininen H (2009) Structural and functional MRI in mild cognitive impairment. Curr Alzheimer Res 6(2):179–85CrossRef
40.
go back to reference Yang Y, Raine A (2009) Prefrontal structural and functional brain imaging findings in antisocial, violent, and psychopathic individuals: a meta-analysis. Psychiatry Res 174(2):81–88PubMedPubMedCentralCrossRef Yang Y, Raine A (2009) Prefrontal structural and functional brain imaging findings in antisocial, violent, and psychopathic individuals: a meta-analysis. Psychiatry Res 174(2):81–88PubMedPubMedCentralCrossRef
41.
go back to reference Goodale MA, Milner AD, Jakobson LS et al (1991) A neurological dissociation between perceiving objects and grasping them. Nature 349(6305):154–156PubMedCrossRef Goodale MA, Milner AD, Jakobson LS et al (1991) A neurological dissociation between perceiving objects and grasping them. Nature 349(6305):154–156PubMedCrossRef
42.
go back to reference Grafton ST, Mazziotta JC, Presty S et al (1992) Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET. J Neurosci Off Neurosci 12(7):2542–2548CrossRef Grafton ST, Mazziotta JC, Presty S et al (1992) Functional anatomy of human procedural learning determined with regional cerebral blood flow and PET. J Neurosci Off Neurosci 12(7):2542–2548CrossRef
43.
go back to reference Camicioli R, Moore MM, Kinney A et al (2003) Parkinson’s disease is associated with hippocampal atrophy. Mov Disord 18(7):784–790PubMedCrossRef Camicioli R, Moore MM, Kinney A et al (2003) Parkinson’s disease is associated with hippocampal atrophy. Mov Disord 18(7):784–790PubMedCrossRef
44.
go back to reference George N, Dolan RJ, Fink GR et al (1999) Contrast polarity and face recognition in the human fusiform gyrus. Nat Neurosci 2(6):574–580PubMedCrossRef George N, Dolan RJ, Fink GR et al (1999) Contrast polarity and face recognition in the human fusiform gyrus. Nat Neurosci 2(6):574–580PubMedCrossRef
45.
go back to reference Sprengelmeyer R, Young AW, Mahn K et al (2003) Facial expression recognition in people with medicated and unmedicated Parkinson’s disease. Neuropsychologia 41(8):1047–1057PubMedCrossRef Sprengelmeyer R, Young AW, Mahn K et al (2003) Facial expression recognition in people with medicated and unmedicated Parkinson’s disease. Neuropsychologia 41(8):1047–1057PubMedCrossRef
Metadata
Title
Functional brain changes in Parkinson’s disease: a whole brain ALE study
Authors
Lihua Gu
Hao Shu
Hui Xu
Yanjuan Wang
Publication date
15-07-2022
Publisher
Springer International Publishing
Published in
Neurological Sciences / Issue 10/2022
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI
https://doi.org/10.1007/s10072-022-06272-9

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