Involuntary language switching in two bilingual patients during the Wada test and intraoperative electrocortical stimulation
Introduction
People are considered bilingual when they use two or more languages or dialects in their everyday lives (Grosjean, 1994). According to this definition, more than half of the world population is bilingual (French and Jacquet, 2004, Harris and Mc Ghee Nelson, 1992). Research on bilinguals has traditionally concentrated on finding differences in the cerebral representation between languages, initiated by the observation that in some bilingual aphasics there is a differential recovery of languages (Albert & Obler, 1978). Although various patterns of language recovery have been described in these patients, no general principle seems to be compatible with all cases. For instance, the language preferentially recovered is not necessarily the native language, whereas in some cases one of the languages is never recovered. In other cases, patients may use one language with the accent of the other, even though both languages were spoken with native-like fluency before the cerebral accident (Paradis, 1998). Overall, in clinical studies ‘no differences have been reported between unilingual and bilingual aphasics with respect to localization, frequency of occurrence or any other parameter’ (Paradis, 1998).
A second source of information regarding multilingual language representation comes from subjects without language disorders. When reviewing functional neuroimaging studies (fMRI, PET, MEG), however, the cortical organization in bilinguals remains controversial. A number of studies have shown differences in localization of first and second languages in healthy subjects (Kim et al., 1997, Simos et al., 2001), but these results are disputed by others (Chee et al., 1999, Mahendra et al., 2003). When part of the cortical surface of bilingual patients is tested with electrocortical stimulation during surgery, all (four) studies report that L1 and L2 are represented in both distinct as well as shared cortical sites (King and Schell, 1987, Ojemann and Whitaker, 1978, Roux et al., 2004, Walker et al., 2004).
As the representation of language in the brain of multilingual subjects remains controversial, even less is known of how subjects manage to switch between different languages (Fabbro, 2001). Language switching (also named code-switching or language mixing) allows multilingual people to use a given language at will and to adjust to the appropriate environment, while at the same time non-targeted languages are suppressed (Muysken, 2000, Poplack, 1980). Some authors have suggested that switching between languages involves aspects of central executive function and is processed by frontal areas, although specific neural systems are not known (Hernandez et al., 2001, Penfield and Roberts, 1959). Pathological language switching is very rarely reported. In brain-damaged bilingual patients language switching may be inappropriate (e.g., when the listener does not understand the language) and occur involuntary (Paradis, 1995). One patient with a large left frontal tumour displayed pathological language switching without any other linguistic impairments (Fabbro, Skrap, & Aglioti, 2000). Functional neuroimaging studies in normal bilinguals have shown involvement of left inferior frontal, supramarginal and dorsolateral prefrontal areas during language switching (Hernandez et al., 2001, Price et al., 1999). We know of only one recent study where switching was induced temporarily; these were two bilingual patients that experienced involuntary language switching after receiving repeated transcranial magnetic stimulation on the left dorsolateral prefrontal cortex as treatment for depression (Holtzheimer, Fawaz, Wilson, & Avery, 2005).
In this article, we describe two invasive methods of brain mapping (namely the Wada test and intraoperative electrostimulation) that transiently induced functional disruption in two bilingual patients. In both cases, following global (Wada) or loco-regional (stimulation) inhibition, there was a transitory switch from the first to the second language. We conclude that both methods temporarily induced a disturbance of the neural networks that are involved in language switching.
Section snippets
Patient A (Dutch–English bilingual)
The 36-year old right-handed patient had a history of epilepsy since age 7. At age 25 he was diagnosed with a left temporal low-grade astrocytoma (pleomorphic xantoastrocytoma) via a stereotactic biopsy. He was admitted to the Dutch Epilepsy Surgery program for surgical relief of his intractable seizures, and had a Wada test as part of the preoperative workup. The patient is Dutch and speaks Dutch as native language (L1). He acquired his second language (English, L2) at age 12 in the normal
Discussion
We report two patients in whom the use of a second, acquired language was induced by means of techniques that functionally disrupt brain areas. In patient A, the left hemisphere was transiently anaesthetized with amobarbital, leading to a spontaneous change from his first to his second language. In patient B, electrocortical stimulation of the posterior part of the left inferior frontal gyrus induced a sudden change of language during counting. We realize that the clinical setting of these
Acknowledgment
The authors thank Jan Vermeulen (SEIN, Heemstede, The Netherlands) for assessment of the tasks during the Wada test.
References (40)
- et al.
The wada test: prediction of focus lateralization by asymmetric and symmetric recall
Epilepsy Research
(2000) - et al.
Differential recovery of languages in a bilingual patient: a case study using selective amytal test
Brain Language
(1990) The bilingual brain: cerebral representation of languages
Brain Language
(2001)- et al.
Understanding bilingual memory: models and data
Trends in Cognitive Sciences
(2004) - et al.
Language switching and language representation in spanish-english bilinguals: an fMRI study
Neuroimage
(2001) - et al.
Repetitive transcranial magnetic stimulation may induce language switching in bilingual patients
Brain Language
(2005) Selective deficit in one language is not a demonstration of different anatomical representation: comments on Gomez-Tortosa et al. (1995)
Brain Language
(1996)- et al.
Lateral frontal cortex oxygenation changes during translation and language switching revealed by non-invasive near-infrared multi-point measurements
Brain Research Bulletin
(2002) - et al.
Combined analysis of language tasks in fMRI improves assessment of hemispheric dominance for language functions in individual subjects
Neuroimage
(2001) - et al.
Phase navigator correction in 3D fMRI improves detection of brain activation: quantitative assessment with a graded motor activation procedure
Neuroimage
(1998)
Language function and dysfunction among Chinese- and English-speaking polyglots: cortical stimulation, Wada testing, and clinical studies
Brain Language
fMRI-determined language lateralization in patients with unilateral or bilateral language dominance according to the Wada test
Neuroimage
Analysis of fMRI time-series revisited – again
Neuroimage
The bilingual brain
Mandarin and English single word processing studied with functional magnetic resonance imaging
Journal of Neuroscience
Language control in the bilingual brain
Science
Intraoperative mapping of the subcortical language pathways using direct stimulations
An anatomo-functional study. Brain
Intra-operative direct electrical stimulations of the central nervous system: the Salpetriere experience with 60 patients
Acta Neurochirurgica (Wien.)
Pathological switching between languages after frontal lesions in a bilingual patient
Journal of Neurology Neurosurgery and Psychiatry
Bilingual sentence processing: relative clause attachment in english and spanish
Cited by (31)
General principles governing the amount of neuroanatomical overlap between languages in bilinguals
2021, Neuroscience and Biobehavioral ReviewsCitation Excerpt :Based on studies involving healthy individuals, we know that the constant language selection engages a left fronto-temporo-parietal network that is, however, not language-specific. Typically reported regions include the basal ganglia (the caudate), anterior cingulate cortex, inferior frontal gyrus, middle frontal gyrus, dorsolateral prefrontal cortex, superior temporal sulcus, and inferior parietal lobule (Borius et al., 2012; Calabria et al., 2018; Hernandez et al., 2001, 2000; Kho et al., 2007; Moritz-Gasser and Duffau, 2009; Price et al., 1999; Sierpowska et al., 2018, 2013; Wang et al., 2007, 2013). The network has been shown to be active when bilinguals speak each of their languages (Abutalebi et al., 2013; Abutalebi and Green, 2008; Calabria et al., 2018; Jones et al., 2012; Petitto and Kovelman, 2003).
Two dissociable semantic mechanisms predict naming errors and their responsive brain sites in awake surgery. DO80 revisited
2021, NeuropsychologiaCitation Excerpt :It is something similar to what happens in bilinguals between the dominant and non-dominant languages (Dylman and Barry, 2018), with different lexical entries for the same concept in each of the languages. In this regard, there are DCE studies provoking language switch errors when stimulating inferior frontal regions (Kho et al., 2007). According to precedent studies on aphasic speakers (Python et al., 2018), IFG deals with this lexical selection.
Bilingual language processing: A meta-analysis of functional neuroimaging studies
2020, Neuroscience and Biobehavioral ReviewsInvolvement of the middle frontal gyrus in language switching as revealed by electrical stimulation mapping and functional magnetic resonance imaging in bilingual brain tumor patients
2018, CortexCitation Excerpt :In fact, in a study evaluating the utility of preoperative fMRI in the prediction of whether a given cortical area would be deemed essential for language processing by ESM, a sensitivity of 66% for expressive linguistic tasks during fMRI was reported (Roux et al., 2003). Therefore, language fMRI mapping carried alone seems not completely advisable to make critical surgical decisions requiring the application of invasive methods of brain mapping such as ESM (Kho et al., 2007; Moritz-Gasser & Duffau, 2009; Roux et al., 2003). Importantly, even if our ESM results showed clear predominance of the MFG over IFG involvement in switching, we sustain that MFG is not an exclusive area in charge of this process.
A surgical approach to the anatomo-functional structure of language
2017, NeurochirurgieCitation Excerpt :Finally, some cases of stimulation-induced involuntary language switching have been reported. A L1 → L2 switching was observed during picture naming when stimulating inferior frontal gyrus [65], superior temporal sulcus and arcuate fasciculus [66], while L2 → L1 switching was reported during counting task when stimulating the superior temporal gyrus [67]. To date, it is not clear whether such language switching is due to a disruption of a language-specific network (e.g., the phonological representations of one language are no longer available, and in order to name the picture in spite of everything, another language is activated, thanks to the flexibility of cognitive control), or whether it reflects a dysfunction of the domain-general cognitive control itself [68] (that would for e.g. normally allow us to inhibit L2 when one wants to speak in L1).