Aerobic Exercise Induces Functional and Structural Reorganization of CNS Networks in Multiple Sclerosis: A Randomized Controlled Trial

Objectives: Evidence from animal studies suggests that aerobic exercise may promote neuroplasticity and could, therefore, provide therapeutic benefits for neurological diseases such as multiple sclerosis (MS). However, the effects of exercise in human CNS disorders on the topology of brain networks,...

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Main Authors: Jan-Patrick Stellmann, Adil Maarouf, Karl-Heinz Schulz, Lisa Baquet, Jana Pöttgen, Stefan Patra, Iris-Katharina Penner, Susanne Gellißen, Gesche Ketels, Pierre Besson, Jean-Philippe Ranjeva, Maxime Guye, Guido Nolte, Andreas K. Engel, Bertrand Audoin, Christoph Heesen, Stefan M. Gold
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-06-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnhum.2020.00255/full
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author Jan-Patrick Stellmann
Jan-Patrick Stellmann
Jan-Patrick Stellmann
Jan-Patrick Stellmann
Adil Maarouf
Adil Maarouf
Karl-Heinz Schulz
Karl-Heinz Schulz
Lisa Baquet
Lisa Baquet
Jana Pöttgen
Jana Pöttgen
Stefan Patra
Stefan Patra
Iris-Katharina Penner
Susanne Gellißen
Susanne Gellißen
Gesche Ketels
Pierre Besson
Pierre Besson
Jean-Philippe Ranjeva
Jean-Philippe Ranjeva
Maxime Guye
Maxime Guye
Guido Nolte
Andreas K. Engel
Bertrand Audoin
Bertrand Audoin
Christoph Heesen
Christoph Heesen
Stefan M. Gold
Stefan M. Gold
Stefan M. Gold
author_facet Jan-Patrick Stellmann
Jan-Patrick Stellmann
Jan-Patrick Stellmann
Jan-Patrick Stellmann
Adil Maarouf
Adil Maarouf
Karl-Heinz Schulz
Karl-Heinz Schulz
Lisa Baquet
Lisa Baquet
Jana Pöttgen
Jana Pöttgen
Stefan Patra
Stefan Patra
Iris-Katharina Penner
Susanne Gellißen
Susanne Gellißen
Gesche Ketels
Pierre Besson
Pierre Besson
Jean-Philippe Ranjeva
Jean-Philippe Ranjeva
Maxime Guye
Maxime Guye
Guido Nolte
Andreas K. Engel
Bertrand Audoin
Bertrand Audoin
Christoph Heesen
Christoph Heesen
Stefan M. Gold
Stefan M. Gold
Stefan M. Gold
author_sort Jan-Patrick Stellmann
collection DOAJ
description Objectives: Evidence from animal studies suggests that aerobic exercise may promote neuroplasticity and could, therefore, provide therapeutic benefits for neurological diseases such as multiple sclerosis (MS). However, the effects of exercise in human CNS disorders on the topology of brain networks, which might serve as an outcome at the interface between biology and clinical performance, remain poorly understood.Methods: We investigated functional and structural networks in patients with relapsing-remitting MS in a clinical trial of standardized aerobic exercise. Fifty-seven patients were randomly assigned to moderate-intensity exercise for 3 months or a non-exercise control group. We reconstructed functional networks based on resting-state functional magnetic resonance imaging (MRI) and used probabilistic tractography on diffusion-weighted imaging data for structural networks.Results: At baseline, compared to 30 healthy controls, patients exhibited decreased structural connectivity that was most pronounced in hub regions of the brain. Vice versa, functional connectivity was increased in hubs. After 3 months, we observed hub independent increased functional connectivity in the exercise group while the control group presented a loss of functional hub connectivity. On a structural level, the control group remained unchanged, while the exercise group had also increased connectivity. Increased clustering of hubs indicates a better structural integration and internal connectivity at the top of the network hierarchy.Conclusion: Increased functional connectivity of hubs contrasts a loss of structural connectivity in relapsing-remitting MS. Under an exercise condition, a further hub independent increase of functional connectivity seems to translate in higher structural connectivity of the whole brain.
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spelling doaj.art-3600203a7d6846749ed8789cf341d2ea2022-12-22T02:51:19ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612020-06-011410.3389/fnhum.2020.00255530459Aerobic Exercise Induces Functional and Structural Reorganization of CNS Networks in Multiple Sclerosis: A Randomized Controlled TrialJan-Patrick Stellmann0Jan-Patrick Stellmann1Jan-Patrick Stellmann2Jan-Patrick Stellmann3Adil Maarouf4Adil Maarouf5Karl-Heinz Schulz6Karl-Heinz Schulz7Lisa Baquet8Lisa Baquet9Jana Pöttgen10Jana Pöttgen11Stefan Patra12Stefan Patra13Iris-Katharina Penner14Susanne Gellißen15Susanne Gellißen16Gesche Ketels17Pierre Besson18Pierre Besson19Jean-Philippe Ranjeva20Jean-Philippe Ranjeva21Maxime Guye22Maxime Guye23Guido Nolte24Andreas K. Engel25Bertrand Audoin26Bertrand Audoin27Christoph Heesen28Christoph Heesen29Stefan M. Gold30Stefan M. Gold31Stefan M. Gold32Institut für Neuroimmunologie und Multiple Sklerose, Universitätsklinikum Hamburg-Eppendorf, Hamburg, GermanyKlinik und Poliklinik für Neurologie, Universitätsklinikum Hamburg-Eppendorf, Hamburg, GermanyAPHM, Hopital de la Timone, CEMEREM, Marseille, FranceAix Marseille Univ, CNRS, CRMBM, UMR 7339, Marseille, FranceAPHM, Hopital de la Timone, CEMEREM, Marseille, FranceAix Marseille Univ, CNRS, CRMBM, UMR 7339, Marseille, FranceInstitut und Poliklinik für Medizinische Psychologie, Universitätsklinikum Hamburg-Eppendorf, Hamburg, GermanyUniversitäres Kompetenzzentrum für Sport—und Bewegungsmedizin (Athleticum), Universitätsklinikum Hamburg-Eppendorf, Hamburg, GermanyInstitut für Neuroimmunologie und Multiple Sklerose, Universitätsklinikum Hamburg-Eppendorf, Hamburg, GermanyKlinik und Poliklinik für Neurologie, Universitätsklinikum Hamburg-Eppendorf, Hamburg, GermanyInstitut für Neuroimmunologie und Multiple Sklerose, Universitätsklinikum Hamburg-Eppendorf, Hamburg, GermanyKlinik und Poliklinik für Neurologie, Universitätsklinikum Hamburg-Eppendorf, Hamburg, GermanyInstitut und Poliklinik für Medizinische Psychologie, Universitätsklinikum Hamburg-Eppendorf, Hamburg, GermanyUniversitäres Kompetenzzentrum für Sport—und Bewegungsmedizin (Athleticum), Universitätsklinikum Hamburg-Eppendorf, Hamburg, GermanyDepartment of Neurology, Medical Faculty, Heinrich-Heine University Düsseldorf, Düsseldorf, GermanyInstitut für Neuroimmunologie und Multiple Sklerose, Universitätsklinikum Hamburg-Eppendorf, Hamburg, GermanyDepartment of Diagnostic and Interventional Neuroradiology, University Medical Center Hamburg Eppendorf, Hamburg, GermanyDepartment of Physiotherapy, University Medical Center Hamburg Eppendorf, Hamburg, GermanyAPHM, Hopital de la Timone, CEMEREM, Marseille, FranceAix Marseille Univ, CNRS, CRMBM, UMR 7339, Marseille, FranceAPHM, Hopital de la Timone, CEMEREM, Marseille, FranceAix Marseille Univ, CNRS, CRMBM, UMR 7339, Marseille, FranceAPHM, Hopital de la Timone, CEMEREM, Marseille, FranceAix Marseille Univ, CNRS, CRMBM, UMR 7339, Marseille, France0Department of Neurophysiology and Pathophysiology, Universitätsklinikum Hamburg-Eppendorf, Hamburg, Germany0Department of Neurophysiology and Pathophysiology, Universitätsklinikum Hamburg-Eppendorf, Hamburg, GermanyAPHM, Hopital de la Timone, CEMEREM, Marseille, FranceAix Marseille Univ, CNRS, CRMBM, UMR 7339, Marseille, FranceInstitut für Neuroimmunologie und Multiple Sklerose, Universitätsklinikum Hamburg-Eppendorf, Hamburg, GermanyKlinik und Poliklinik für Neurologie, Universitätsklinikum Hamburg-Eppendorf, Hamburg, GermanyInstitut für Neuroimmunologie und Multiple Sklerose, Universitätsklinikum Hamburg-Eppendorf, Hamburg, Germany1Charité—Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt Universität zu Berlin, and Berlin Institute of Health (BIH), Klinik für Psychiatrie und Psychotherapie, Campus Benjamin Franklin (CBF), Berlin, Germany2Charité—Universitätsmedizin Berlin, Freie Universität Berlin, Humboldt Universität zu Berlin, and Berlin Institute of Health (BIH), Med. Klinik m.S. Psychosomatik, Campus Benjamin Franklin (CBF), Berlin, GermanyObjectives: Evidence from animal studies suggests that aerobic exercise may promote neuroplasticity and could, therefore, provide therapeutic benefits for neurological diseases such as multiple sclerosis (MS). However, the effects of exercise in human CNS disorders on the topology of brain networks, which might serve as an outcome at the interface between biology and clinical performance, remain poorly understood.Methods: We investigated functional and structural networks in patients with relapsing-remitting MS in a clinical trial of standardized aerobic exercise. Fifty-seven patients were randomly assigned to moderate-intensity exercise for 3 months or a non-exercise control group. We reconstructed functional networks based on resting-state functional magnetic resonance imaging (MRI) and used probabilistic tractography on diffusion-weighted imaging data for structural networks.Results: At baseline, compared to 30 healthy controls, patients exhibited decreased structural connectivity that was most pronounced in hub regions of the brain. Vice versa, functional connectivity was increased in hubs. After 3 months, we observed hub independent increased functional connectivity in the exercise group while the control group presented a loss of functional hub connectivity. On a structural level, the control group remained unchanged, while the exercise group had also increased connectivity. Increased clustering of hubs indicates a better structural integration and internal connectivity at the top of the network hierarchy.Conclusion: Increased functional connectivity of hubs contrasts a loss of structural connectivity in relapsing-remitting MS. Under an exercise condition, a further hub independent increase of functional connectivity seems to translate in higher structural connectivity of the whole brain.https://www.frontiersin.org/article/10.3389/fnhum.2020.00255/fullCNS networksneuroplasticityexercisemultiple sclerosisrandomized controlled trial
spellingShingle Jan-Patrick Stellmann
Jan-Patrick Stellmann
Jan-Patrick Stellmann
Jan-Patrick Stellmann
Adil Maarouf
Adil Maarouf
Karl-Heinz Schulz
Karl-Heinz Schulz
Lisa Baquet
Lisa Baquet
Jana Pöttgen
Jana Pöttgen
Stefan Patra
Stefan Patra
Iris-Katharina Penner
Susanne Gellißen
Susanne Gellißen
Gesche Ketels
Pierre Besson
Pierre Besson
Jean-Philippe Ranjeva
Jean-Philippe Ranjeva
Maxime Guye
Maxime Guye
Guido Nolte
Andreas K. Engel
Bertrand Audoin
Bertrand Audoin
Christoph Heesen
Christoph Heesen
Stefan M. Gold
Stefan M. Gold
Stefan M. Gold
Aerobic Exercise Induces Functional and Structural Reorganization of CNS Networks in Multiple Sclerosis: A Randomized Controlled Trial
Frontiers in Human Neuroscience
CNS networks
neuroplasticity
exercise
multiple sclerosis
randomized controlled trial
title Aerobic Exercise Induces Functional and Structural Reorganization of CNS Networks in Multiple Sclerosis: A Randomized Controlled Trial
title_full Aerobic Exercise Induces Functional and Structural Reorganization of CNS Networks in Multiple Sclerosis: A Randomized Controlled Trial
title_fullStr Aerobic Exercise Induces Functional and Structural Reorganization of CNS Networks in Multiple Sclerosis: A Randomized Controlled Trial
title_full_unstemmed Aerobic Exercise Induces Functional and Structural Reorganization of CNS Networks in Multiple Sclerosis: A Randomized Controlled Trial
title_short Aerobic Exercise Induces Functional and Structural Reorganization of CNS Networks in Multiple Sclerosis: A Randomized Controlled Trial
title_sort aerobic exercise induces functional and structural reorganization of cns networks in multiple sclerosis a randomized controlled trial
topic CNS networks
neuroplasticity
exercise
multiple sclerosis
randomized controlled trial
url https://www.frontiersin.org/article/10.3389/fnhum.2020.00255/full
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