Overt speech critically changes lateralization index and did not allow determination of hemispheric dominance for language: an fMRI study

Abstract

Background Pre-surgical mapping of language using functional MRI aimed principally to determine the dominant hemisphere. This mapping is currently performed using covert linguistic task in way to avoid motion artefacts potentially biasing the results. However, overt task is closer to natural speaking, allows a control on the performance of the task, and may be easier to perform for stressed patients and children. However, overt task, by activating phonological areas on both hemispheres and areas involved in pitch prosody control in the non-dominant hemisphere, is expected to modify the determination of the dominant hemisphere by the calculation of the lateralization index (LI). Objective Here, we analyzed the modifications in the LI and the interactions between cognitive networks during covert and overt speech task. Methods Thirty-three volunteers participated in this study, all but four were right-handed. They performed three functional sessions consisting of (1) covert and (2) overt generation of a short sentence semantically linked with an audibly presented word, from which we estimated the “Covert” and “Overt” contrasts, and a (3) resting-state session. The resting-state session was submitted to spatial independent component analysis to identify language network at rest (LANG), cingulo-opercular network (CO), and ventral attention network (VAN). The LI was calculated using the bootstrapping method. Results The LI of the LANG was the most left-lateralized (0.66 ± 0.38). The LI shifted from a moderate leftward lateralization for the Covert contrast (0.32 ± 0.38) to a right lateralization for the Overt contrast (− 0.13 ± 0.30). The LI significantly differed from each other. This rightward shift was due to the recruitment of right hemispheric temporal areas together with the nodes of the CO. Conclusion Analyzing the overt speech by fMRI allowed improvement in the physiological knowledge regarding the coordinated activity of the intrinsic connectivity networks. However, the rightward shift of the LI in this condition did not provide the basic information on the hemispheric language dominance. Overt linguistic task cannot be recommended for clinical purpose when determining hemispheric dominance for language.

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

“…We used a covert task design which did not allow to control the performance of the task which would be of importance in particular in patients with low cognitive status. An overt design would overcome this limitation but led to a right-shift of laterality indices in a study by Berro et al ( 2021 ). An additional control task as implemented in paradigms that are recommended by the American Society of Neuroradiology (Black et al, 2017 ) or the use of adaptive language mapping paradigms which showed strong lateralized activation maps in a study by Diachek et al ( 2022 ) would allow to control the performance of the task.…”