Cerebral language organization in bilingual patients
Yasser Aladdin, MD,
Thomas J. Snyder, PhD and
S. Nizam Ahmed, MD, FRCPC
From the Departments of Neurology (Y.A., S.N.A.) and Psychiatry (T.J.S.), University of Alberta, Edmonton, Alberta, Canada.
Address correspondence and reprint requests to Dr. S. Nizam Ahmed, Division of Neurology, University of Alberta Hospital, 2E3 Walter McKenzie Center, 8440-112 St., Edmonton, AB, Canada T6G 2B7 snahmed{at}ualberta.ca
Background: Ictal and postictal language dysfunction is commonand strongly predictive of language laterality in monolingualpatients. For bilingual patients, selective dysfunction hasbeen reported for a single language with focal cerebral lesions,electrical brain stimulation, and intracarotid sodium amytal.
Methods: Two right-handed Ukrainian-English bilingual patientswith left perisylvian structural lesions, late onset complex-partialseizures, and postictal aphasia for English are presented anddiscussed with regard to mechanisms of selective aphasia andfactors contributory to language lateralization in bilingualpatients.
Results: Ukrainian was the native language of both patientswith English acquired after 7 years of age. Regular/video-EEGshowed left temporal epileptogenesis. A 56-year-old man, whohad a left hemorrhagic stroke at age 50 and had not spoken Ukrainianfor 40 years, was unable to speak English for 20 minutes postictallybut had global preservation of Ukrainian. A 71-year-old woman,who had a left temporal epidermoid cyst and had not spoken Ukrainiansince childhood, had 10- to 15-minute postictal expressive aphasiain English but not Ukrainian and preservation of comprehensionin both languages.
Conclusions: These cases are instructive and consistent withthe literature on cerebral organization of language in bilingualindividuals. For both patients, postictal aphasia with preservationof Ukrainian is consistent with findings from clinical and experimentalstudies indicating that later age of second language acquisition(>6 years) rather than language proficiency is a primaryfactor in language laterality. Second, global aphasia in theman with a late lesion vs expressive aphasia with preservationof comprehension of English in the woman with a prenatal/earlylesion is consistent with the atypical language laterality describedfor individuals with left-sided lesions sustained prior to age5. Although neither Wada test nor fMRI was done to assure lefthemisphere laterality of spoken Ukrainian and English, thisis probable, and the selective postictal aphasia observed forboth patients is consistent with the differential intrahemisphericorganization reported for the two languages of bilingual individuals.Possible mechanisms of selective postictal aphasia, e.g., activeinhibition, and differences in language networks in bilingualpatients are discussed.
Ictal and postictal language dysfunction is common and stronglypredictive of language laterality in monolingual patients. Forbilingual patients, selective dysfunction has been reportedfor a single language with focal cerebral lesions, electricalbrain stimulation, and intracarotid sodium amytal. We reporttwo right-handed Ukrainian-English bilingual patients with leftperisylvian structural lesions, late onset complex-partial seizures,and postictal aphasia for English, and discuss mechanisms ofselective aphasia and factors contributory to language lateralizationin bilingual patients.
Case A.
The first patient was a 56-year-old, right-handed bilingualman born to Ukrainian parents, who first learned to speak Englishat the age of 7. At 50 years of age, he sustained a hemorrhagicstroke involving the left perisylvian region due to a rupturedanterior communicating aneurysm. Several months later, he beganhaving seizures. The semiology of his seizures was characterizedby recurrent episodes of confusion lasting 1–2 minuteswith secondary progression to generalized tonic-clonic seizures.Seizures were stereotypically followed by inability to speakEnglish for 15 to 20 minutes with preservation of his nativeUkrainian. Interestingly, he had not spoken Ukrainian for thepast 40 years and his daily communication, even at home, wasentirely in English. Unfortunately, the content of his verbaloutput could not be translated during the postictal period.On admission, cranial CT showed encephalomalacia of the leftfrontotemporal operculum from the previous stroke. EEG recordingdisplayed paroxysmal epileptiform discharges emanating fromthe left temporal region. Ultimately, total control of seizureswas achieved by carbamazepine monotherapy.
Case B.
This was a 71-year-old, right-handed, bilingual woman born toUkrainian parents. She learned English after beginning school.At 52 years of age she presented with recurrent episodes ofdisorientation that occasionally evolved into generalized tonic-clonicseizures lasting for 10 minutes. Postictally, her comprehensionof English remained intact but her responses to questions werein normal Ukrainian as translated by an interpreter. This unilingualexpressive aphasia in English lasted for 10–15 minuteswith gradual recovery. Of note is that her day-to-day communicationswere mainly in English for the last 50 years. The cranial CTrevealed a left frontotemporal perisylvian cyst which was subsequentlyresected and identified as an epidermoid cyst (figure 1). EEGrecording showed interictal epileptiform discharges and frequentfocal seizures originating in the left temporal region (figure 2).She continues to have infrequent seizures following surgery.
The approach to an analysis of selective aphasia in multilingualpatients can be facilitated using the following conceptual parameters,as discussed below: laterality of language function, intrahemisphericorganization of language, patterns of language recovery, andhigher cortical control and switching mechanisms.
Laterality of language functions in multilingual individuals.
The cortical representation of different languages in multilingualindividuals is controversial because of inconsistent findingsin the literature.1–3 Two key hypotheses have been proposedon the basis of experimental studies of normal multilingualsubjects: the age and the stage hypotheses.1 The age hypothesisemphasizes the age of second language (L2) acquisition as mostimportant in L2 laterality; acquisition after 6 years resultsin identical lateralization of L1 and L2. The stage hypothesisemphasizes that degree of L2 proficiency is the primary determinantof language laterality. In a meta-analysis of 66 behavioralstudies of language laterality, monolingual subjects and latebilingual subjects showed a reliable left hemispheric dominanceacross language tasks regardless of proficiency, whereas earlybilingual subjects demonstrated a tendency for bihemisphericcontributions.1,2 Left hemispheric dominance was more prominentin those less proficient in L2, especially if the L2 was English.Hence, earlier acquisition of L2 predicts a divergent patternof cerebral lateralization with right hemispheric contributions.Both of our patients were late bilingual individuals who acquiredEnglish after the age of 6 and accordingly would have left hemispheredominance for both languages. The dual aphasia with rapid L1recovery in strict left-sided lesions argues in favor of thecontention that age rather than proficiency was the primarydeterminant of language laterality in our patients.
Intrahemispheric organization of language in multilingual subjects.
Various clinical studies support the differential localizationmodel in bilingual patients where two languages occupy distinctbut overlapping loci within the dominant hemisphere. Electrocorticographicstimulation of the dominant perisylvian region in bilingualpatients revealed different but overlapping areas for each language.2–4Sequential recovery of two languages over different time courseswas also observed after the Wada test.5 At the lexical level,fMRI studies confirmed the shared neural substrates for L1 andL2 with distinct neuronal populations displaying language specificresponses.6 The lesions in both of our patients spanned grossanatomic landmarks and disruption of both languages would havebeen expected. The sequential recovery may be explained by thedifferential localization model with limited seizure propagationto the neural population of English and relative sparing ofUkrainian. The fact that Case B postictally comprehended bothlanguages but spoke only English could implicate minimal posteriorseizure spread and/or right hemisphere representation of comprehensionassociated with her epidermoid cyst acquired at an early age.Nevertheless, the concept of separate but overlapping topographyfor each language remains too simple to explain this phenomenon.The other possibility is that the complexity of the networkfor each language could be different and perhaps related tothe time of acquisition. A language acquired earlier may havea more extensive and thus more resistant network, whereas oneestablished later would have a more superficial and easily disruptednetwork.
Patterns of language recovery in multilingual patients.
Six major patterns of language recovery in bilingual patientshave been historically observed.7,8
Parallel recovery when both languages are impaired and restoredat the same pace.
Differential recovery when languages recoverat different ratesrelative to their premorbid levels.
Selectiverecovery (30%) with recovery of one language but notthe other.
Antagonistic recovery where one language recovers to a certainextent before regression occurs as the other language beginsto recover.
Successive recovery where recovery of L2 beginsafter L1 hasrecovered.
Mixed recovery with mutual interferencebetween languages duringrecovery process.
These descriptive categories emphasize the possible phenomenologicpatterns of recovery and do not correlate with specific anatomicor pathologic processes. Both of our patients had not been speakingUkrainian for many years, and the second patient responded appropriatelyto commands in English and correctly answered, in Ukrainian,questions presented in English. The recovery in both cases wasdifficult to categorize due to their short-lasting deficitsin English and the inherent difficulties in conducting formalneuropsychological assessments postictally to quantify the relativerecovery for both languages.
Higher cortical control and switching mechanisms.
Volitional alternation of verbal output between two languagesis under sustained higher cognitive system control. Involuntaryintrusions of linguistic elements from different languages representpathologic switching or mixing. Pathologic switching is a highercortical disorder of communication that usually relates to frontallobe lesions. Pathologic mixing is an aphasic disorder thatis generally associated with fluent aphasias due to left postrolandiclesions, and in bilingual aphasics with dementia.9 The anteriorloop of language that mediates language planning comprises thecortico-subcortical circuit between the prefrontal cortex andbasal ganglia in the dominant hemisphere.10 This loop is theneuroanatomic device for language selection control, and functionalneuroimaging demonstrates resolution of pathologic switchingand mixing with functional restoration of this cortico-subcorticalloop.11 Both patients had structural lesions spanning the frontotemporaloperculum with minor involvement of the white matter connectingthe frontal lobe with the basal ganglia. Neither mixing norswitching was observed interictally or postictally.
Postictal aphasia.
The mechanism underlying postictal aphasia (PA) may be relatedto active inhibition or postictal exhaustion induced by ictalactivities in language areas and their connections.12 The literatureis relatively scarce in substantiating the prevalence of PAin both monolingual and bilingual patients. In one series of68 patients with temporal lobe epilepsy (TLE), PA was foundin 51.6% and correctly lateralized the seizure onset to thedominant hemisphere in 81.3%.13 In another review, 92% of patientswith TLE with PA had their seizures originating from the dominanttemporal lobe.14 In another series of 64 patients with TLE,the positive predictive value of PA in lateralizing seizureonset to the dominant side was 80%.15 The seizures in both ofour patients originated electrographically from the left frontotemporalregion and correlated with PA for both languages. Nonetheless,objective evaluations of PA are difficult due to the overlapwith postictal behaviors like postictal confusion and fatiguethat can confound any linguistic analysis of postictal speech.This will be further complicated in cases of bihemispheric speechrepresentation or with seizure propagation to the contralateralhemisphere or, conceivably, in multilingual patients. The immediaterecovery of Ukrainian may reflect the relative resistance ofthe native language to postictal mechanisms, or simply and incidentally,relates to limited seizure propagations into their neural populationin both patients.
Focal seizures originating from the dominant perisylvian regionsresulted in postictal aphasia involving mainly the second languagein two late bilingual patients. The diffuse lesions in bothpatients do not conform to isolated anatomic or language-specificterritories. Postictal inhibition may selectively involve onecircuit subserving one language. This corroborates the notionthat neurobiological substrates mediating two languages sharea common topographic anatomy with relatively distinct functionalcircuits. Arguably, disruption of distinct switch mechanismsrather than an isolated functional circuitry of one languagecould be the defining pathology of this rather unusual phenomenon.
Monolingual and late bilingual patients have a reliable lefthemispheric dominance across language tasks regardless of proficiency,whereas early bilingual patients demonstrate a tendency forbihemispheric contributions.
The differential localizationmodel of bilingual speech indicatesthat the two languages occupydistinct but overlapping locior functional circuits withinthe dominant perisylvian region.
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Top.
Abstract.
CASE HISTORIES
20 minutes postictally but had global preservation of Ukrainian. A 71-year-old woman, who had a left temporal epidermoid cyst and had not spoken Ukrainian since childhood, had 10- to 15-minute postictal expressive aphasia in English but not Ukrainian and preservation of comprehension in both languages. 
