The diminishing dominance of the dominant hemisphere: Language fMRI in focal epilepsy

Abstract

“Which is the dominant hemisphere?” is a question that arises frequently in patients considered for neurosurgery. The concept of the dominant hemisphere implies uniformity of language lateralisation throughout the brain. It is increasingly recognised that this is not the case in the healthy control brain, and it is especially not so in neurological diseases such as epilepsy.In the present work we adapt our published objective lateralisation method (based on the construction of laterality curves) for use with sub-lobar cortical, subcortical and cerebellar regions of interest (ROIs). We apply this method to investigate regional lateralisation of language activation in 12 healthy controls and 18 focal epilepsy patients, using three different block design language fMRI paradigms, each tapping different aspects of language processing. We compared lateralisation within each ROI across tasks, and investigated how the quantity of data collected affected the ability to robustly estimate laterality across ROIs.In controls, lateralisation was stronger, and the variance across individuals smaller, in cortical ROIs, particularly in the Inferior Frontal (Broca) region. Lateralisation within temporal ROIs was dependent on the nature of the language task employed. One of the healthy controls was left lateralised anteriorly and right lateralised posteriorly. Consistent with previous work, departures from normality occurred in ~ 15–50% of focal epilepsy patients across the different ROIs, with atypicality most common in the Lateral Temporal (Wernicke) region. Across tasks and ROIs the absolute magnitude of the laterality estimate increased and its across participant variance decreased as more cycles of task and rest were included, stabilising at ~ 4 cycles (~ 4 min of data collection).Our data highlight the importance of considering language as a complex task where lateralisation varies at the subhemispheric scale. This is especially important for presurgical planning for focal resections where the concept of ‘hemispheric dominance’ may be misleading. This is a precision medicine approach that enables objective evaluation of language dominance within specific brain regions and can reveal surprising and unexpected anomalies that may be clinically important for individual cases.

Language network measures at rest indicate individual differences in naming decline after anterior temporal lobe resection

“…In their large multisite study, Tomasi and Volkow (2012) characterized the resting-state language network using a seed-to-voxel approach from Broca's and Wernike's areas, and found that both seeds demonstrated robust connectivity to language regions that were much more bilateral than typically reported in studies of task activation. Furthermore, it has since been proposed that the concept of language "dominance," at least as assessed using fMRI, may actually be inappropriate when considering regional effects rather than at the level of the entire hemisphere (Tailby, Abbott, & Jackson, 2017). They suggested that bilateral activity captured with resting-state reflects "prepotent" language regions of which specific areas are recruited depending on task demands.…”

Measurement of language laterality using functional transcranial Doppler ultrasound: a comparison of different tasks

“…Although other tasks have been shown to be sensitive and reliable at assessing cerebral lateralisation, we still know relatively little about the key characteristics of tasks that give reliable left lateralisation. Indeed, it has been proposed that language laterality is multifactorial, and may dissociate within an individual from one task to another ( Gaillard et al , 2004; Stroobant et al , 2009; Tailby et al , 2017). …”

fMRI prediction of naming change after adult temporal lobe epilepsy surgery: Activation matters

“…[39][40][41] Decreased left lateralization in patients with left TLE was associated with better postoperative naming. 22,43,44 Operating on the "dominant" hemisphere, however identified, creates a risk of postoperative language impairment, and thus, in this sense, fMRI determination of language dominance is associated with the risk of language decline. 42 The degree of language laterality as well as the extent of WA resected predicted outcome, agreeing with previous reports.…”

“…Several studies support the concept that language dominance is not hemispheric but varies on regional and individual bases. 22,43,44 Operating on the "dominant" hemisphere, however identified, creates a risk of postoperative language impairment, and thus, in this sense, fMRI determination of language dominance is associated with the risk of language decline. 45 Using fMRI, language dominance usually is determined by LI in both IFG and WA.…”