Transcranial magnetic stimulation and environmental enrichment enhances cortical excitability and functional outcomes after traumatic brain injury

Background: Therapeutic strategies for traumatic brain injury (TBI) in the last three decades have failed to show significant benefit in large scale studies. Given the multitude of pathological mechanisms involved in TBI, strategies focusing on multimodality regimen have gained interest as promising...

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Main Authors: Samuel S. Shin, Vijai Krishnan, William Stokes, Courtney Robertson, Pablo Celnik, Yanrong Chen, Xiaolei Song, Hanzhang Lu, Peiying Liu, Galit Pelled
Format: Article
Language:English
Published: Elsevier 2018-11-01
Series:Brain Stimulation
Subjects:
TBI
TMS
Online Access:http://www.sciencedirect.com/science/article/pii/S1935861X18302547
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language English
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author Samuel S. Shin
Vijai Krishnan
William Stokes
Courtney Robertson
Pablo Celnik
Yanrong Chen
Xiaolei Song
Hanzhang Lu
Peiying Liu
Galit Pelled
spellingShingle Samuel S. Shin
Vijai Krishnan
William Stokes
Courtney Robertson
Pablo Celnik
Yanrong Chen
Xiaolei Song
Hanzhang Lu
Peiying Liu
Galit Pelled
Transcranial magnetic stimulation and environmental enrichment enhances cortical excitability and functional outcomes after traumatic brain injury
Brain Stimulation
Traumatic brain injury
TBI
Transcranial magnetic stimulation
TMS
Environmental enrichment
author_facet Samuel S. Shin
Vijai Krishnan
William Stokes
Courtney Robertson
Pablo Celnik
Yanrong Chen
Xiaolei Song
Hanzhang Lu
Peiying Liu
Galit Pelled
author_sort Samuel S. Shin
title Transcranial magnetic stimulation and environmental enrichment enhances cortical excitability and functional outcomes after traumatic brain injury
title_short Transcranial magnetic stimulation and environmental enrichment enhances cortical excitability and functional outcomes after traumatic brain injury
title_full Transcranial magnetic stimulation and environmental enrichment enhances cortical excitability and functional outcomes after traumatic brain injury
title_fullStr Transcranial magnetic stimulation and environmental enrichment enhances cortical excitability and functional outcomes after traumatic brain injury
title_full_unstemmed Transcranial magnetic stimulation and environmental enrichment enhances cortical excitability and functional outcomes after traumatic brain injury
title_sort transcranial magnetic stimulation and environmental enrichment enhances cortical excitability and functional outcomes after traumatic brain injury
publisher Elsevier
series Brain Stimulation
issn 1935-861X
publishDate 2018-11-01
description Background: Therapeutic strategies for traumatic brain injury (TBI) in the last three decades have failed to show significant benefit in large scale studies. Given the multitude of pathological mechanisms involved in TBI, strategies focusing on multimodality regimen have gained interest as promising future interventions. Hypothesis: We hypothesized that combining noninvasive transcranial magnetic stimulation (TMS) with rehabilitative training in an environmental enrichment (EE) can facilitate post-TBI recovery in rats via cortical excitability and reorganization. Methods: We subjected rats to controlled cortical impact, and then assigned them to one of four groups: 1. No treatments (TBI), 2. EE after injury (TBI + EE), 3. TMS for one week (TBI + TMS), and 4. TMS for one week combined with EE (TBI + TMS/EE). For TMS, a 10 Hz repetitive TMS protocol was used. Results: At 7 days, TBI + TMS and TBI + TMS/EE groups had significantly increased primary somatosensory cortex local field potential (LFP) compared to TBI and TBI + EE groups (P < 0.05). Also, TBI + TMS/EE group had significantly improved performance on beam walk test compared to TBI group (P < 0.005). At 6 weeks, there was significantly higher response in TBI + TMS/EE group compared to TBI + TMS for somatosensory cortex LFP (P < 0.05), bicep motor evoked potentials (MEP) (P < 0.05), challenge ladder test performance (P < 0.01), and fMRI responses to tactile forepaw stimulation. Conclusions: We demonstrate here for the first time the mechanism by which combined therapy using TMS and EE after TBI leads to functional improvement, possibly via cortical excitability and reorganization.
topic Traumatic brain injury
TBI
Transcranial magnetic stimulation
TMS
Environmental enrichment
url http://www.sciencedirect.com/science/article/pii/S1935861X18302547
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spelling doaj-1263a79071844fddbd2e1f7d45ca18bd2021-03-19T07:12:36ZengElsevierBrain Stimulation1935-861X2018-11-0111613061313Transcranial magnetic stimulation and environmental enrichment enhances cortical excitability and functional outcomes after traumatic brain injurySamuel S. Shin0Vijai Krishnan1William Stokes2Courtney Robertson3Pablo Celnik4Yanrong Chen5Xiaolei Song6Hanzhang Lu7Peiying Liu8Galit Pelled9Department of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD, USA; F.M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD, USA; Russell H. Morgan Department of Radiology, The Johns Hopkins University School of Medicine, Baltimore, MD, USAF.M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD, USA; Russell H. Morgan Department of Radiology, The Johns Hopkins University School of Medicine, Baltimore, MD, USA; Department of Biomedical Engineering, Michigan State University, East Lansing, MI, USA; The Institute of Quantitative Health Science and Engineering, Michigan State University, East Lansing, MI, USAF.M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD, USA; Russell H. Morgan Department of Radiology, The Johns Hopkins University School of Medicine, Baltimore, MD, USADepartment of Anesthesiology/Critical Care Medicine and Pediatrics, The Johns Hopkins University School of Medicine, Baltimore, MD, USADepartment of Neurology, The Johns Hopkins University School of Medicine, Baltimore, MD, USA; Department of Physical Medicine and Rehabilitation, The Johns Hopkins University School of Medicine, Baltimore, MD, USAF.M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD, USA; Russell H. Morgan Department of Radiology, The Johns Hopkins University School of Medicine, Baltimore, MD, USAF.M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD, USA; Russell H. Morgan Department of Radiology, The Johns Hopkins University School of Medicine, Baltimore, MD, USAF.M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD, USA; Russell H. Morgan Department of Radiology, The Johns Hopkins University School of Medicine, Baltimore, MD, USAF.M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD, USA; Russell H. Morgan Department of Radiology, The Johns Hopkins University School of Medicine, Baltimore, MD, USAF.M. Kirby Research Center for Functional Brain Imaging, Kennedy Krieger Institute, Baltimore, MD, USA; Russell H. Morgan Department of Radiology, The Johns Hopkins University School of Medicine, Baltimore, MD, USA; Department of Biomedical Engineering, Michigan State University, East Lansing, MI, USA; The Institute of Quantitative Health Science and Engineering, Michigan State University, East Lansing, MI, USA; Department of Radiology, Michigan State University, East Lansing, MI, USA; Corresponding author. Biomedical Engineering, Radiology and Neuroscience, Division of Neuroengineering, Institute for Quantitative Health Science and Engineering, 775 Woodlot Drive, Room 2112, Michigan State University, East Lansing, MI 48824, USABackground: Therapeutic strategies for traumatic brain injury (TBI) in the last three decades have failed to show significant benefit in large scale studies. Given the multitude of pathological mechanisms involved in TBI, strategies focusing on multimodality regimen have gained interest as promising future interventions. Hypothesis: We hypothesized that combining noninvasive transcranial magnetic stimulation (TMS) with rehabilitative training in an environmental enrichment (EE) can facilitate post-TBI recovery in rats via cortical excitability and reorganization. Methods: We subjected rats to controlled cortical impact, and then assigned them to one of four groups: 1. No treatments (TBI), 2. EE after injury (TBI + EE), 3. TMS for one week (TBI + TMS), and 4. TMS for one week combined with EE (TBI + TMS/EE). For TMS, a 10 Hz repetitive TMS protocol was used. Results: At 7 days, TBI + TMS and TBI + TMS/EE groups had significantly increased primary somatosensory cortex local field potential (LFP) compared to TBI and TBI + EE groups (P < 0.05). Also, TBI + TMS/EE group had significantly improved performance on beam walk test compared to TBI group (P < 0.005). At 6 weeks, there was significantly higher response in TBI + TMS/EE group compared to TBI + TMS for somatosensory cortex LFP (P < 0.05), bicep motor evoked potentials (MEP) (P < 0.05), challenge ladder test performance (P < 0.01), and fMRI responses to tactile forepaw stimulation. Conclusions: We demonstrate here for the first time the mechanism by which combined therapy using TMS and EE after TBI leads to functional improvement, possibly via cortical excitability and reorganization.http://www.sciencedirect.com/science/article/pii/S1935861X18302547Traumatic brain injuryTBITranscranial magnetic stimulationTMSEnvironmental enrichment