Motor Cortical Network Plasticity in Patients With Recurrent Brain Tumors

Objective: The adult brain’s potential for plastic reorganization is an important mechanism for the preservation and restoration of function in patients with primary glial neoplasm. Patients with recurrent brain tumors requiring multiple interventions over time present an opportunity to examine brai...

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Main Authors: Lucia Bulubas, Nina Sardesh, Tavish Traut, Anne Findlay, Danielle Mizuiri, Susanne M. Honma, Sandro M. Krieg, Mitchel S. Berger, Srikantan S. Nagarajan, Phiroz E. Tarapore
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-04-01
Series:Frontiers in Human Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnhum.2020.00118/full
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author Lucia Bulubas
Lucia Bulubas
Lucia Bulubas
Lucia Bulubas
Lucia Bulubas
Nina Sardesh
Nina Sardesh
Tavish Traut
Tavish Traut
Anne Findlay
Anne Findlay
Danielle Mizuiri
Danielle Mizuiri
Susanne M. Honma
Susanne M. Honma
Sandro M. Krieg
Mitchel S. Berger
Mitchel S. Berger
Srikantan S. Nagarajan
Srikantan S. Nagarajan
Phiroz E. Tarapore
Phiroz E. Tarapore
spellingShingle Lucia Bulubas
Lucia Bulubas
Lucia Bulubas
Lucia Bulubas
Lucia Bulubas
Nina Sardesh
Nina Sardesh
Tavish Traut
Tavish Traut
Anne Findlay
Anne Findlay
Danielle Mizuiri
Danielle Mizuiri
Susanne M. Honma
Susanne M. Honma
Sandro M. Krieg
Mitchel S. Berger
Mitchel S. Berger
Srikantan S. Nagarajan
Srikantan S. Nagarajan
Phiroz E. Tarapore
Phiroz E. Tarapore
Motor Cortical Network Plasticity in Patients With Recurrent Brain Tumors
Frontiers in Human Neuroscience
brain tumor
magnetoencephalography
motor cortex
neurological surgery
preoperative motor mapping
plasticity
author_facet Lucia Bulubas
Lucia Bulubas
Lucia Bulubas
Lucia Bulubas
Lucia Bulubas
Nina Sardesh
Nina Sardesh
Tavish Traut
Tavish Traut
Anne Findlay
Anne Findlay
Danielle Mizuiri
Danielle Mizuiri
Susanne M. Honma
Susanne M. Honma
Sandro M. Krieg
Mitchel S. Berger
Mitchel S. Berger
Srikantan S. Nagarajan
Srikantan S. Nagarajan
Phiroz E. Tarapore
Phiroz E. Tarapore
author_sort Lucia Bulubas
title Motor Cortical Network Plasticity in Patients With Recurrent Brain Tumors
title_short Motor Cortical Network Plasticity in Patients With Recurrent Brain Tumors
title_full Motor Cortical Network Plasticity in Patients With Recurrent Brain Tumors
title_fullStr Motor Cortical Network Plasticity in Patients With Recurrent Brain Tumors
title_full_unstemmed Motor Cortical Network Plasticity in Patients With Recurrent Brain Tumors
title_sort motor cortical network plasticity in patients with recurrent brain tumors
publisher Frontiers Media S.A.
series Frontiers in Human Neuroscience
issn 1662-5161
publishDate 2020-04-01
description Objective: The adult brain’s potential for plastic reorganization is an important mechanism for the preservation and restoration of function in patients with primary glial neoplasm. Patients with recurrent brain tumors requiring multiple interventions over time present an opportunity to examine brain reorganization. Magnetoencephalography (MEG) is a noninvasive imaging modality that can be used for motor cortical network mapping which, when performed at regular intervals, offers insight into this process of reorganization. Utilizing MEG-based motor mapping, we sought to characterize the reorganization of motor cortical networks over time in a cohort of 78 patients with recurrent glioma.Methods: MEG-based motor cortical maps were obtained by measuring event-related desynchronization (ERD) in ß-band frequency during unilateral index finger flexion. Each patient presented at our Department at least on two occasions for tumor resection due to tumor recurrence, and MEG-based motor mapping was performed as part of preoperative assessment before each surgical resection. Whole-brain activation patterns from first to second MEG scan (obtained before first and second surgery) were compared. Additionally, we calculated distances of activation peaks, which represent the location of the primary motor cortex (MC), to determine the magnitude of movement in motor eloquent areas between the first and second MEG scan. We also explored which demographic, anatomic, and pathological factors influence these shifts.Results: The whole-brain activation motor maps showed a subtle movement of the primary MC from first to second timepoint, as was confirmed by the determination of motor activation peaks. The shift of ipsilesional MC was directly correlated with a frontal-parietal tumor location (p < 0.001), presence of motor deficits (p = 0.021), and with a longer period between MEG scans (p = 0.048). Also, a disengagement of wide areas in the contralesional (ipsilateral to finger movement) hemisphere at the second time point was observed.Conclusions: MEG imaging is a sensitive method for depicting the plasticity of the motor cortical network. Although the location of the primary MC undergoes only subtle changes, appreciable shifts can occur in the setting of a stronger and longer impairment of the tumor on the MC. The ipsilateral hemisphere may serve as a reservoir for functional recovery.
topic brain tumor
magnetoencephalography
motor cortex
neurological surgery
preoperative motor mapping
plasticity
url https://www.frontiersin.org/article/10.3389/fnhum.2020.00118/full
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spelling doaj-a1594e51d6864e7586c60c2830c770e62020-11-25T02:11:50ZengFrontiers Media S.A.Frontiers in Human Neuroscience1662-51612020-04-011410.3389/fnhum.2020.00118510298Motor Cortical Network Plasticity in Patients With Recurrent Brain TumorsLucia Bulubas0Lucia Bulubas1Lucia Bulubas2Lucia Bulubas3Lucia Bulubas4Nina Sardesh5Nina Sardesh6Tavish Traut7Tavish Traut8Anne Findlay9Anne Findlay10Danielle Mizuiri11Danielle Mizuiri12Susanne M. Honma13Susanne M. Honma14Sandro M. Krieg15Mitchel S. Berger16Mitchel S. Berger17Srikantan S. Nagarajan18Srikantan S. Nagarajan19Phiroz E. Tarapore20Phiroz E. Tarapore21Biomagnetic Imaging Lab, Department of Radiology and Biomedical Imaging, University of California San Francisco (UCSF), San Francisco, CA, United StatesDepartment of Neurological Surgery, University of California San Francisco (UCSF), San Francisco, CA, United StatesDepartment of Neurosurgery and TUM-Neuroimaging Center, Klinikum Rechts der Isar, Technische Universität (TU), Munich, GermanyDepartment of Psychiatry and Psychotherapy, University Hospital, Ludwig-Maximilians Universität (LMU), Munich, GermanyInternational Max Planck Research School for Translational Psychiatry (IMPRS-TP), Munich, GermanyBiomagnetic Imaging Lab, Department of Radiology and Biomedical Imaging, University of California San Francisco (UCSF), San Francisco, CA, United StatesDepartment of Neurological Surgery, University of California San Francisco (UCSF), San Francisco, CA, United StatesBiomagnetic Imaging Lab, Department of Radiology and Biomedical Imaging, University of California San Francisco (UCSF), San Francisco, CA, United StatesDepartment of Neurological Surgery, University of California San Francisco (UCSF), San Francisco, CA, United StatesBiomagnetic Imaging Lab, Department of Radiology and Biomedical Imaging, University of California San Francisco (UCSF), San Francisco, CA, United StatesDepartment of Neurological Surgery, University of California San Francisco (UCSF), San Francisco, CA, United StatesBiomagnetic Imaging Lab, Department of Radiology and Biomedical Imaging, University of California San Francisco (UCSF), San Francisco, CA, United StatesDepartment of Neurological Surgery, University of California San Francisco (UCSF), San Francisco, CA, United StatesBiomagnetic Imaging Lab, Department of Radiology and Biomedical Imaging, University of California San Francisco (UCSF), San Francisco, CA, United StatesDepartment of Neurological Surgery, University of California San Francisco (UCSF), San Francisco, CA, United StatesDepartment of Neurosurgery and TUM-Neuroimaging Center, Klinikum Rechts der Isar, Technische Universität (TU), Munich, GermanyBiomagnetic Imaging Lab, Department of Radiology and Biomedical Imaging, University of California San Francisco (UCSF), San Francisco, CA, United StatesDepartment of Neurological Surgery, University of California San Francisco (UCSF), San Francisco, CA, United StatesBiomagnetic Imaging Lab, Department of Radiology and Biomedical Imaging, University of California San Francisco (UCSF), San Francisco, CA, United StatesDepartment of Neurological Surgery, University of California San Francisco (UCSF), San Francisco, CA, United StatesBiomagnetic Imaging Lab, Department of Radiology and Biomedical Imaging, University of California San Francisco (UCSF), San Francisco, CA, United StatesDepartment of Neurological Surgery, University of California San Francisco (UCSF), San Francisco, CA, United StatesObjective: The adult brain’s potential for plastic reorganization is an important mechanism for the preservation and restoration of function in patients with primary glial neoplasm. Patients with recurrent brain tumors requiring multiple interventions over time present an opportunity to examine brain reorganization. Magnetoencephalography (MEG) is a noninvasive imaging modality that can be used for motor cortical network mapping which, when performed at regular intervals, offers insight into this process of reorganization. Utilizing MEG-based motor mapping, we sought to characterize the reorganization of motor cortical networks over time in a cohort of 78 patients with recurrent glioma.Methods: MEG-based motor cortical maps were obtained by measuring event-related desynchronization (ERD) in ß-band frequency during unilateral index finger flexion. Each patient presented at our Department at least on two occasions for tumor resection due to tumor recurrence, and MEG-based motor mapping was performed as part of preoperative assessment before each surgical resection. Whole-brain activation patterns from first to second MEG scan (obtained before first and second surgery) were compared. Additionally, we calculated distances of activation peaks, which represent the location of the primary motor cortex (MC), to determine the magnitude of movement in motor eloquent areas between the first and second MEG scan. We also explored which demographic, anatomic, and pathological factors influence these shifts.Results: The whole-brain activation motor maps showed a subtle movement of the primary MC from first to second timepoint, as was confirmed by the determination of motor activation peaks. The shift of ipsilesional MC was directly correlated with a frontal-parietal tumor location (p < 0.001), presence of motor deficits (p = 0.021), and with a longer period between MEG scans (p = 0.048). Also, a disengagement of wide areas in the contralesional (ipsilateral to finger movement) hemisphere at the second time point was observed.Conclusions: MEG imaging is a sensitive method for depicting the plasticity of the motor cortical network. Although the location of the primary MC undergoes only subtle changes, appreciable shifts can occur in the setting of a stronger and longer impairment of the tumor on the MC. The ipsilateral hemisphere may serve as a reservoir for functional recovery.https://www.frontiersin.org/article/10.3389/fnhum.2020.00118/fullbrain tumormagnetoencephalographymotor cortexneurological surgerypreoperative motor mappingplasticity