The neuronal reserve in glioma surgery: functional reorganization of the motor network examined by navigated transcranial magnetic stimulation and diffusion tensor imaging tractography.

Abstract

Patients suffering from rolandic gliomas are differently affected by motor deficits due to the lesion growth and edema as well as the surgical intervention. One reason for the different dynamics of disease progression and surgical outcome might be an individual potential for compensation and adaptation of the motor network. The aim of the present study was therefore to investigate the reorganization capacity of the motor cortex in patients with glioma by using navigated transcranial magnetic stimulation and diffusion tensor imaging tractography. The cortical motor representation area of the first dorsal interosseous muscle was mapped preoperatively on both hemispheres in 27 patients suffering from glioma (WHO grade ≥ II) in the primary or secondary motor cortex and in 17 follow-up patients (median 7 [IQR 6.5, 8.5] months after surgery). Twenty-eight healthy volunteers served as the control group. Motor function was evaluated based on the British Medical Research Council scale. Corticospinal excitability was determined by the resting motor threshold (RMT) and recruitment curve, and the cortical representation by mapping of the motor area with 105% RMT. Intracortical inhibition was reflected by the cortical silent period. The corticospinal tract integrity was determined by diffusion tensor imaging tractography including fractional anisotropy and apparent diffusion coefficient. A motor paresis was preoperatively seen in 47% of the patients, which diminished to 23% at follow-up. The preoperatively observed RMT difference between the hemispheres diminished after 7 months (p < 0.05). An increased cortical excitability at follow-up was also indicated by less cortical inhibition (p < 0.05). A preoperatively small motor area size, excitability, and volume increased the risk for postoperative motor deficit (p < 0.05). Corticospinal tract disintegrity was associated with motor impairment (p < 0.05). Motor area reshaping expressed by a hotspot and center of gravity relocation could be observed in patients recovering from a motor deficit (p < 0.0001). This study confirmed prior findings on glioma-induced reorganization of primary motor areas. The association between functional recovery and reorganization, especially resizing and excitability changes, suggests an individual neuronal reserve explaining differences in disease progression. The authors support the extended consideration of navigated transcranial magnetic stimulation data for preoperative risk stratification and patient-tailored treatment strategies.