Motor Cortical Network Plasticity in Patients With Recurrent Brain Tumors.

Lucia Bulubas,Srikantan S Nagarajan,Anne Findlay,Susanne M Honma,Mitchel S Berger,Sandro M Krieg,Danielle Mizuiri,Phiroz E Tarapore,Tavish Traut,Nina Sardesh

doi:10.3389/fnhum.2020.00118

Abstract

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.

Highlights

The human brain contains eloquent regions of particular significance to specific neurological functions
From a population of patients that presented at our Department for tumor resection surgery, we identified the cohort who had recurrent tumors and underwent tumor resection and MEG-based motor mapping as part of preoperative assessment at two or more time points
We demonstrate that both contralateral and ipsilateral motor cortices are capable of functional reorganization in patients with primary brain tumors, and that greater time between scans and presence of a motor deficit are associated with greater cortical reorganization

Summary

Introduction

The human brain contains eloquent regions of particular significance to specific neurological functions. Functional reorganization likely takes place via several mechanisms, many of which are still under investigation One such mechanism involves the recruitment of compensatory areas, the ipsilateral non-primary, or the contralateral primary and non-primary motor cortices (Weiller et al, 1993; Seitz et al, 1995; Duffau et al, 2002; Bulubas et al, 2016). Functional reorganization is important in patients with slow-growing brain tumors, in whom the competing pressures of tumor progression and cortical adaptation create an evolving spatial relationship between lesion and surrounding cortex. For such a patient, functional reorganization may dictate whether a lesion is operable and, if not, whether it may be so in the future, having profound implications on length and quality of life

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Conclusion