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@ARTICLE{Ruppert:874734,
author = {Ruppert, Marina C and Greuel, Andrea and Tahmasian, Masoud
and Schwartz, Frank and Stürmer, Sophie and Maier,
Franziska and Hammes, Jochen and Tittgemeyer, Marc and
Timmermann, Lars and van Eimeren, Thilo and Drzezga,
Alexander and Eggers, Carsten},
title = {{N}etwork degeneration in {P}arkinson’s disease:
multimodal imaging of nigro-striato-cortical dysfunction},
journal = {Brain},
volume = {143},
number = {3},
issn = {1460-2156},
address = {Oxford},
publisher = {Oxford Univ. Press},
reportid = {FZJ-2020-01643},
pages = {944 - 959},
year = {2020},
abstract = {The spreading hypothesis of neurodegeneration assumes an
expansion of neural pathologies along existing neural
pathways. Multimodal neuroimaging studies have demonstrated
distinct topographic patterns of cerebral pathologies in
neurodegeneration. For Parkinson’s disease the hypothesis
so far rests largely on histopathological evidence of
α-synuclein spreading in a characteristic pattern and
progressive nigrostriatal dopamine depletion. Functional
consequences of nigrostriatal dysfunction on cortical
activity remain to be elucidated. Our goal was to
investigate multimodal imaging correlates of degenerative
processes in Parkinson’s disease by assessing dopamine
depletion and its potential effect on striatocortical
connectivity networks and cortical metabolism in relation to
parkinsonian symptoms. We combined 18F-DOPA-PET,
18F-fluorodeoxyglucose (FDG)-PET and resting state
functional MRI to multimodally characterize network
alterations in Parkinson’s disease. Forty-two patients
with mild-to-moderate stage Parkinson’s disease and 14
age-matched healthy control subjects underwent a multimodal
imaging protocol and comprehensive clinical examination. A
voxel-wise group comparison of 18F-DOPA uptake identified
the exact location and extent of putaminal dopamine
depletion in patients. Resulting clusters were defined as
seeds for a seed-to-voxel functional connectivity analysis.
18F-FDG metabolism was compared between groups at a
whole-brain level and uptake values were extracted from
regions with reduced putaminal connectivity. To unravel
associations between dopaminergic activity, striatocortical
connectivity, glucose metabolism and symptom severity,
correlations between normalized uptake values,
seed-to-cluster β-values and clinical parameters were
tested while controlling for age and dopaminergic
medication. Aside from cortical hypometabolism, 18F-FDG-PET
data for the first time revealed a hypometabolic midbrain
cluster in patients with Parkinson’s disease that
comprised caudal parts of the bilateral substantia nigra
pars compacta. Putaminal dopamine synthesis capacity was
significantly reduced in the bilateral posterior putamen and
correlated with ipsilateral nigral 18F-FDG uptake. Resting
state functional MRI data indicated significantly reduced
functional connectivity between the dopamine depleted
putaminal seed and cortical areas primarily belonging to the
sensorimotor network in patients with Parkinson’s disease.
In the inferior parietal cortex, hypoconnectivity in
patients was significantly correlated with lower metabolism
(left P = 0.021, right P = 0.018). Of note, unilateral
network alterations quantified with different modalities
corresponded with contralateral motor impairments. In
conclusion, our results support the hypothesis that
degeneration of nigrostriatal fibres functionally impairs
distinct striatocortical connections, disturbing the
efficient interplay between motor processing areas and
impairing motor control in patients with Parkinson’s
disease. The present study is the first to reveal trimodal
evidence for network-dependent degeneration in Parkinson’s
disease by outlining the impact of functional nigrostriatal
pathway impairment on striatocortical functional
connectivity networks and cortical metabolism.},
cin = {INM-3 / INM-2},
ddc = {610},
cid = {I:(DE-Juel1)INM-3-20090406 / I:(DE-Juel1)INM-2-20090406},
pnm = {572 - (Dys-)function and Plasticity (POF3-572)},
pid = {G:(DE-HGF)POF3-572},
typ = {PUB:(DE-HGF)16},
pubmed = {pmid:32057084},
UT = {WOS:000522641900028},
doi = {10.1093/brain/awaa019},
url = {https://juser.fz-juelich.de/record/874734},
}