Language Neuroplasticity in Brain Tumor Patients Revealed by Magnetoencephalography

Abstract

<jats:p> Little is known about language impairment in brain tumor patients, especially in the presurgical phase. Impairment in this population may be missed because standardized tests fail to capture mild deficits. Additionally, neuroplasticity may also contribute to minimizing language impairments. We examined 14 presurgical patients with brain tumors in the language-dominant hemisphere using magnetoencephalography (MEG) while they performed a demanding picture–word interference task, that is, participants name pictures while ignoring distractor words. Brain tumor patients had behavioral picture-naming effects typically observed in healthy controls. The MEG responses also showed the expected pattern in its timing and amplitude modulation typical of controls, but with an altered spatial distribution of right hemisphere sources, in contrast to the classic left hemisphere source found in healthy individuals. This finding supports tumor-induced neural reorganization of language before surgery. Crucially, the use of electrophysiology allowed us to show the “same” neuronal response in terms of its timing and amplitude modulation in the right hemisphere, supporting the hypothesis that the processes performed by the right hemisphere following reorganization are similar in nature to those (previously) performed by the left hemisphere. We also identified one participant with a fast-growing tumor affecting large parts of critical language areas and underlying ventral and dorsal white matter tracts who showed a deviant pattern in behavior and in the MEG event-related responses. In conclusion, our results attest to the validity of using a demanding picture-naming task in presurgical patients and provide evidence for neuroplasticity, with the right hemisphere performing similar computations as the left hemisphere typically performs. </jats:p>

Oscillatory and structural signatures of language plasticity in brain tumor patients: A longitudinal study

“…Indeed, recent studies (Duffau, 2008; Vassal et al, 2010) using direct electrical stimulation have revealed a right mirror organization of language networks, pointing to the existence of functional redundancies that can undertake functions previously supported by damaged areas. Furthermore, this finding also aligns well with neurophysiological evidence from brain tumor (Piai et al, 2020; Traut et al, 2019) and stroke patients (Kielar et al, 2016; Piai et al, 2017) showing compensatory recruitment of the right hemisphere during language processing. Of note, one of these studies (Piai et al, 2017) showed that contralesional recruitment in the alpha‐beta band was associated with the integrity of the posterior bundles of the corpus callosum.…”

“…Furthermore, this finding also aligns well with neurophysiological evidence from brain tumor (Piai et al, 2020;Traut et al, 2019) and stroke patients (Kielar et al, 2016;Piai et al, 2017) showing compensatory recruitment of the right hemisphere during language processing. Of note, one of these studies (Piai et al, 2017) showed that contralesional recruitment in the alpha-beta band was associated with the integrity of the posterior bundles of the corpus callosum.…”

Understanding Language Reorganization With Neuroimaging: How Language Adapts to Different Focal Lesions and Insights Into Clinical Applications

“…Patients with brain tumors in the language-dominant hemisphere showed a neuronal response in the right hemisphere similar to that of left-sided language eloquent areas on MEG, including timing and amplitude modulation. This evidence seems to support the hypothesis that right-hemispheric reorganization is similar in nature to normal processes performed by the left hemisphere (Piai et al, 2020). Language functional reorganization in the setting of brain tumors includes perilesional rearrangement (Figure 4; Duffau et al, 2003b;Desmurget et al, 2007), as well as recruitment of contralateral language area homologues (Figure 5; Holodny et al, 2002;Petrovich et al, 2004;Rosenberg et al, 2008;Wang et al, 2013;Ge ¸bska-Kośla et al, 2017;Li et al, 2019).…”

Neural Regulation of Cancer: Cancer‐Induced Remodeling of the Central Nervous System

“…Invasive and noninvasive imaging modalities have empowered the study of glioma-induced cortical neuron reorganization using direct electrocortical stimulation (DES), PET, magnetoencephalography (MEG), fMRI, electrocorticography (ECoG), and transcranial magnetic stimulation (TMS) (Figure 1). [27,29,30]…”