MEG Assessment of Expressive Language in Children Evaluated for Epilepsy Surgery

Abstract

Establishing language dominance is an important step in the presurgical evaluation of patients with refractory epilepsy. In the absence of a universally accepted gold-standard non-invasive method to determine language dominance in the preoperative assessment, a range of tools and methodologies have recently received attention. When applied to pediatric age, many of the proposed methods, such as functional magnetic resonance imaging (fMRI), may present some challenges due to the time-varying effects of epileptogenic lesions and of on-going seizures on maturational phenomena. Magnetoencephalography (MEG) has the advantage of being insensitive to the distortive effects of anatomical lesions on brain microvasculature and to differences in the metabolism or vascularization of the developing brain and also provides a less intimidating recording environment for younger children. In this study we investigated the reliability of lateralized synchronous cortical activation during a verb generation task in a group of 28 children (10 males and 18 females, mean age 12 years) with refractory epilepsy who were evaluated for epilepsy surgery. The verb generation task was associated with significant decreases in beta oscillatory power (13–30 Hz) in frontal and temporal lobes. The MEG data were compared with other available presurgical non-invasive data including cortical stimulation, neuropsychological and fMRI data on language lateralization where available. We found that the lateralization of MEG beta power reduction was concordant with language dominance determined by one or more different assessment methods (i.e. cortical stimulation mapping, neuropsychological, fMRI or post-operative data) in 89% of patients. Our data suggest that qualitative hemispheric differences in task-related changes of spectral power could offer a promising insight into the contribution of dominant and non-dominant hemispheres in language processing and may help to characterize the specialization and lateralization of language processes in children.

Localization of beta power decrease as measure for lateralization in pre-surgical language mapping with magnetoencephalography, compared with functional magnetic resonance imaging and validated by Wada test

“…In concordance with the literature, we observed a beta decrease after stimulus onset within the language-related regions within the dominant hemisphere (Hirata et al, 2004(Hirata et al, , 2010Fisher et al, 2008;Pang et al, 2011;Findlay et al, 2012;Foley et al, 2019;Youssofzadeh et al, 2020), and an increase within the non-dominant frontal and superior-parietal lobes (Sharma et al, 2021). The beta decrease was seen in controls between 300 and 800 ms and worked as the criterion to lateralize language in patients and controls.…”

“…Left: frontal ROI, middle: temporo-parietal ROI, right: other temporal areas. (Foley et al, 2019;Youssofzadeh et al, 2020), or applied clustercorrection to improve the sensitivity of statistics (Youssofzadeh et al, 2020).…”

“…While most studies analyzed broadband electromagnetic activity encompassing frequencies ranging from 1 to 50 Hz or higher (e.g., Tanaka et al, 2013;Kemp et al, 2018), frequencies within the beta band (13-30 Hz) were revealed to be of particular importance during language processing (Weiss and Mueller, 2012). In particular, a decrease in beta band activity, also referred to as event-related desynchronization, demonstrated high concordance with left language lateralization (Pang et al, 2011;Youssofzadeh et al, 2020) as well as fMRI (Foley et al, 2019) and Wada test results (Hirata et al, 2004(Hirata et al, , 2010Fisher et al, 2008;Findlay et al, 2012). Beta desynchronization during verb generation tasks was a very robust marker for assessing language lateralization, achieving a sensitivity of 100% in atypical Wada test patients (Fisher et al, 2008;Findlay et al, 2012).…”

Beta synchrony for expressive language lateralizes to right hemisphere in development

“…ERD has been found during phonetic processing in typically developing children and adolescents, but not in children with developmental language impairments such as aphasia and dyslexia 29 . Indeed, low-beta (13–23 Hz) ERD is considered an oscillatory signature for expressive language in both children and adults 30 . Studies have found this ERD at perisylvian language networks as early as 650 ms and as late as 1200 ms post-stimulus presentation, which is thought to be locked to response timing 31 – 33 .…”

Left hemispheric α band cerebral oscillatory changes correlate with verbal memory

“…Thus, it is conceivable that ERS/ERD in each frequency band may have differential language processing functions. Furthermore, it has been reported that lateralising variations in ERD in the β band or the low γ band can function as a non-invasive index for estimating the language-dominant hemisphere during language tasks in patients with epilepsy and brain tumour [18][19][20] . Thus, cerebral oscillatory variations in MEG signal may be related to language function when detected in the context of a language-related task.…”