Identification of a metabolic brain network characterizing essential tremor

Abstract The neuronal correlate of tremor genesis and cognitive function in essential tremor (ET) and its modulation by deep brain stimulation (DBS) are poorly understood. To explore the underlying metabolic topography of motor and cognitive symptoms, sixteen ET patients (age 63.6 ± 49.1 years) and...

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Main Authors: Solange Volnov, Hamzah Baagil, Oliver Winz, Hans-Juergen Kaiser, Sanne Katherina Meles, Joerg Bernhard Schulz, Kathrin Reetz, Felix Manuel Mottaghy, Florian Holtbernd
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-024-82069-4
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author Solange Volnov
Hamzah Baagil
Oliver Winz
Hans-Juergen Kaiser
Sanne Katherina Meles
Joerg Bernhard Schulz
Kathrin Reetz
Felix Manuel Mottaghy
Florian Holtbernd
author_facet Solange Volnov
Hamzah Baagil
Oliver Winz
Hans-Juergen Kaiser
Sanne Katherina Meles
Joerg Bernhard Schulz
Kathrin Reetz
Felix Manuel Mottaghy
Florian Holtbernd
author_sort Solange Volnov
collection DOAJ
description Abstract The neuronal correlate of tremor genesis and cognitive function in essential tremor (ET) and its modulation by deep brain stimulation (DBS) are poorly understood. To explore the underlying metabolic topography of motor and cognitive symptoms, sixteen ET patients (age 63.6 ± 49.1 years) and 18 healthy controls (HC) (61.1 ± 6.3 years) underwent tremor and cognitive assessments and18F-fluorodeoxyglucose PET of the brain. Multivariate spatial covariance analysis was applied for identifying ET related metabolic brain networks. For network validation and to explore DBS effects, 8 additional ET patients (68.1 ± 8.2 years) treated with DBS were assessed in both the ON and OFF state, respectively. The ET related metabolic spatial covariance pattern (ETRP) was characterized by relatively increased metabolism in the cerebellum, brainstem, and temporo-occipital cortices, accompanied by relative metabolic decreases mainly in fronto-temporal and motor cortices. Network expression showed inverse correlations with tremor severity and disease duration and positive correlations with cognitive dysfunction. DBS substantially alleviated tremor, but had only marginal effects on cognitive performance. There were no significant DBS effects on ETRP expression at the group level, but all but one subject showed higher scores in the ON state. Our findings suggest ET is characterized by an abnormal brain network associated with disease phenotype.
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spelling doaj-art-c5bd58bb9cbe469ab2edc2c25dc2fdd32025-01-19T12:19:16ZengNature PortfolioScientific Reports2045-23222025-01-0115111210.1038/s41598-024-82069-4Identification of a metabolic brain network characterizing essential tremorSolange Volnov0Hamzah Baagil1Oliver Winz2Hans-Juergen Kaiser3Sanne Katherina Meles4Joerg Bernhard Schulz5Kathrin Reetz6Felix Manuel Mottaghy7Florian Holtbernd8Department of Neurology, University Hospital RWTH AachenDepartment of Neurology, University Hospital RWTH AachenDepartment of Nuclear Medicine, University Hospital RWTH AachenDepartment of Nuclear Medicine, University Hospital RWTH AachenDepartment of Neurology, University Medical Centre Groningen, University of GroningenDepartment of Neurology, University Hospital RWTH AachenDepartment of Neurology, University Hospital RWTH AachenDepartment of Nuclear Medicine, University Hospital RWTH AachenDepartment of Neurology, University Hospital RWTH AachenAbstract The neuronal correlate of tremor genesis and cognitive function in essential tremor (ET) and its modulation by deep brain stimulation (DBS) are poorly understood. To explore the underlying metabolic topography of motor and cognitive symptoms, sixteen ET patients (age 63.6 ± 49.1 years) and 18 healthy controls (HC) (61.1 ± 6.3 years) underwent tremor and cognitive assessments and18F-fluorodeoxyglucose PET of the brain. Multivariate spatial covariance analysis was applied for identifying ET related metabolic brain networks. For network validation and to explore DBS effects, 8 additional ET patients (68.1 ± 8.2 years) treated with DBS were assessed in both the ON and OFF state, respectively. The ET related metabolic spatial covariance pattern (ETRP) was characterized by relatively increased metabolism in the cerebellum, brainstem, and temporo-occipital cortices, accompanied by relative metabolic decreases mainly in fronto-temporal and motor cortices. Network expression showed inverse correlations with tremor severity and disease duration and positive correlations with cognitive dysfunction. DBS substantially alleviated tremor, but had only marginal effects on cognitive performance. There were no significant DBS effects on ETRP expression at the group level, but all but one subject showed higher scores in the ON state. Our findings suggest ET is characterized by an abnormal brain network associated with disease phenotype.https://doi.org/10.1038/s41598-024-82069-4Deep brain stimulationEssential tremorFDG PETBrain metabolismSpatial covariance analysis
spellingShingle Solange Volnov
Hamzah Baagil
Oliver Winz
Hans-Juergen Kaiser
Sanne Katherina Meles
Joerg Bernhard Schulz
Kathrin Reetz
Felix Manuel Mottaghy
Florian Holtbernd
Identification of a metabolic brain network characterizing essential tremor
Scientific Reports
Deep brain stimulation
Essential tremor
FDG PET
Brain metabolism
Spatial covariance analysis
title Identification of a metabolic brain network characterizing essential tremor
title_full Identification of a metabolic brain network characterizing essential tremor
title_fullStr Identification of a metabolic brain network characterizing essential tremor
title_full_unstemmed Identification of a metabolic brain network characterizing essential tremor
title_short Identification of a metabolic brain network characterizing essential tremor
title_sort identification of a metabolic brain network characterizing essential tremor
topic Deep brain stimulation
Essential tremor
FDG PET
Brain metabolism
Spatial covariance analysis
url https://doi.org/10.1038/s41598-024-82069-4
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