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,...
Main Authors: | , , , , , , , , , , , , , , , , |
---|---|
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 |
_version_ | 1811310343227441152 |
---|---|
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. |
first_indexed | 2024-04-13T09:57:22Z |
format | Article |
id | doaj.art-3600203a7d6846749ed8789cf341d2ea |
institution | Directory Open Access Journal |
issn | 1662-5161 |
language | English |
last_indexed | 2024-04-13T09:57:22Z |
publishDate | 2020-06-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Human Neuroscience |
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 |
work_keys_str_mv | AT janpatrickstellmann aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT janpatrickstellmann aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT janpatrickstellmann aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT janpatrickstellmann aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT adilmaarouf aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT adilmaarouf aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT karlheinzschulz aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT karlheinzschulz aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT lisabaquet aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT lisabaquet aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT janapottgen aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT janapottgen aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT stefanpatra aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT stefanpatra aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT iriskatharinapenner aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT susannegellißen aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT susannegellißen aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT gescheketels aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT pierrebesson aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT pierrebesson aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT jeanphilipperanjeva aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT jeanphilipperanjeva aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT maximeguye aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT maximeguye aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT guidonolte aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT andreaskengel aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT bertrandaudoin aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT bertrandaudoin aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT christophheesen aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT christophheesen aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT stefanmgold aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT stefanmgold aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial AT stefanmgold aerobicexerciseinducesfunctionalandstructuralreorganizationofcnsnetworksinmultiplesclerosisarandomizedcontrolledtrial |