Functional separation of languages in the bilingual brain: a comparison of electrical stimulation language mapping in 25 bilingual patients and 117 monolingual control patients

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Object. The aim of this investigation was to address three questions in bilingualism research: 1) are multiple languages functionally separated within the bilingual brain; 2) are these languages similarly organized; and 3) does language organization in bilinguals mirror that in monolinguals?

Methods. During awake dominant-hemisphere craniotomy in each of 25 bilingual patients, the authors mapped both languages by using identical object-naming stimuli. Essential sites for primary (L1) and secondary (L2) languages were compared. Sites were photographically recorded and plotted onto an anatomically referenced grid system. Language organization in bilinguals was then compared with that in 117 monolinguals and 11 monolingual children.

Conclusions. The authors found distinct language-specific sites as well as shared sites that support both languages. The L1 and L2 representations were similar in total cortical extent but significantly different in anatomical distribution. The L2-specific sites were located exclusively in the posterior temporal and parietal regions, whereas the L1 and shared sites could be found throughout the mapped regions. Bilinguals possessed seven perisylvian language zones, in which L2 sites were significantly underrepresented when compared with the distribution of language sites in monolinguals. These L2-restricted zones overlapped the primary language areas found in monolingual children, indicating that these zones become dedicated to L1 processing. These findings support three conclusions. First, it is necessary to map both languages in bilinguals because L1 and L2 sites are functionally distinct. Second, differences exist in the organization of L1 and L2 sites, with L2-specific sites located exclusively in the posterior temporal and parietal lobes. Third, language organization comparisons in bilingual and monolingual brains demonstrate the presence of L2-restricted zones, which are dedicated to L1.

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Contributor Notes

Address reprint requests to: Timothy H. Lucas II, M.D., Department of Neurological Surgery, University of Washington, Box 356470, 1959 Pacific Street, Seattle, Washington 98195–6470. email: tlucas@u.washington.edu.
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References
  • 1.

    Chee MWHon NLee HLet al: Relative language proficiency modulates BOLD signal change when bilinguals perform semantic judgments. Blood oxygen level dependent. Neuroimage 13:115511632001Chee MW Hon N Lee HL et al: Relative language proficiency modulates BOLD signal change when bilinguals perform semantic judgments. Blood oxygen level dependent. Neuroimage 13:1155–1163 2001

    • Search Google Scholar
    • Export Citation
  • 2.

    Chee MWSoon CSLee HL: Common and segregated neuronal networks for different languages revealed using functional magnetic resonance adaptation. J Cogn Neurosci 15:85972003Chee MW Soon CS Lee HL: Common and segregated neuronal networks for different languages revealed using functional magnetic resonance adaptation. J Cogn Neurosci 15:85–97 2003

    • Search Google Scholar
    • Export Citation
  • 3.

    Chee MWTan EWThiel T: Mandarin and English single word processing studied with functional magnetic resonance imaging. J Neurosci 19:305030561999Chee MW Tan EW Thiel T: Mandarin and English single word processing studied with functional magnetic resonance imaging. J Neurosci 19:3050–3056 1999

    • Search Google Scholar
    • Export Citation
  • 4.

    Chee MWLWeekes BLee KMet al: Overlap and dissociation of semantic processing of Chinese characters, English words, and pictures: evidence from fMRI. Neuroimage 12:3924032000Chee MWL Weekes B Lee KM et al: Overlap and dissociation of semantic processing of Chinese characters English words and pictures: evidence from fMRI. Neuroimage 12:392–403 2000

    • Search Google Scholar
    • Export Citation
  • 5.

    Dehaene SDupoux EMehler Jet al: Anatomical variability in the cortical representation of first and second language. Neuroreport 8:380938151997Dehaene S Dupoux E Mehler J et al: Anatomical variability in the cortical representation of first and second language. Neuroreport 8:3809–3815 1997

    • Search Google Scholar
    • Export Citation
  • 6.

    Gomez-Tortosa EMartin EMGaviria Met al: Selective deficit in one language in a bilingual patient following surgery in the left perisylvian area. Brain Lang 48:3203251995Gomez-Tortosa E Martin EM Gaviria M et al: Selective deficit in one language in a bilingual patient following surgery in the left perisylvian area. Brain Lang 48:320–325 1995

    • Search Google Scholar
    • Export Citation
  • 7.

    Hasegawa MCarpenter PAJust MA: An fMRI study of bilingual sentence comprehension and workload. Neuroimage 15:6476602002Hasegawa M Carpenter PA Just MA: An fMRI study of bilingual sentence comprehension and workload. Neuroimage 15:647–660 2002

    • Search Google Scholar
    • Export Citation
  • 8.

    Hernandez AEMartinez AKohnert K: In search of the language switch: an fMRI study of picture naming in Spanish-English bilinguals. Brain Lang 73:4214312000Hernandez AE Martinez A Kohnert K: In search of the language switch: an fMRI study of picture naming in Spanish-English bilinguals. Brain Lang 73:421–431 2000

    • Search Google Scholar
    • Export Citation
  • 9.

    Illes JFrancis WSDesmond JEet al: Convergent cortical representation of semantic processing in bilinguals. Brain Lang 70:3473631999Illes J Francis WS Desmond JE et al: Convergent cortical representation of semantic processing in bilinguals. Brain Lang 70:347–363 1999

    • Search Google Scholar
    • Export Citation
  • 10.

    Kim KHRelkin NRLee KMet al: Distinct cortical areas associated with native and second languages. Nature 388:1711741997Kim KH Relkin NR Lee KM et al: Distinct cortical areas associated with native and second languages. Nature 388:171–174 1997

    • Search Google Scholar
    • Export Citation
  • 11.

    Klein DZatorre RJMilner Bet al: Left putaminal activation when speaking a second language: evidence from PET. Neuroreport 5:229522971994Klein D Zatorre RJ Milner B et al: Left putaminal activation when speaking a second language: evidence from PET. Neuroreport 5:2295–2297 1994

    • Search Google Scholar
    • Export Citation
  • 12.

    Klein DZatorre RJMilner Bet al: The neural substrates of bilingual language processing: evidence from positron emission tomography in Paradis M (ed): Aspects of Bilingual Aphasia. Oxford: Pergamon Press1995 pp 2336Klein D Zatorre RJ Milner B et al: The neural substrates of bilingual language processing: evidence from positron emission tomography in Paradis M (ed): Aspects of Bilingual Aphasia. Oxford: Pergamon Press 1995 pp 23–36

    • Search Google Scholar
    • Export Citation
  • 13.

    Lurito JTLowe MJSartorius Cet al: Comparison of fMRI and intraoperative direct cortical stimulation in localization of receptive language areas. J Comput Assist Tomogr 24:991052000Lurito JT Lowe MJ Sartorius C et al: Comparison of fMRI and intraoperative direct cortical stimulation in localization of receptive language areas. J Comput Assist Tomogr 24:99–105 2000

    • Search Google Scholar
    • Export Citation
  • 14.

    Ojemann GOjemann JLettich Eet al: Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 71:3163261989Ojemann G Ojemann J Lettich E et al: Cortical language localization in left dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg 71:316–326 1989

    • Search Google Scholar
    • Export Citation
  • 15.

    Ojemann GA: Awake operations with mapping in epilepsy in Schmidek HHSweet WH (eds): Operative Neurosurgical Techniques: Indications Methods and Resultsed 3. Philadelphia: WB Saunders1995 pp 13171322Ojemann GA: Awake operations with mapping in epilepsy in Schmidek HH Sweet WH (eds): Operative Neurosurgical Techniques: Indications Methods and Results ed 3. Philadelphia: WB Saunders 1995 pp 1317–1322

    • Search Google Scholar
    • Export Citation
  • 16.

    Ojemann GA: Cortical organization of language and verbal memory based on intraoperative investigations in Ottoson D (ed): Progress in Sensory Physiologyed 12. Berlin: Springer-Verlag1991 pp 193230Ojemann GA: Cortical organization of language and verbal memory based on intraoperative investigations in Ottoson D (ed): Progress in Sensory Physiology ed 12. Berlin: Springer-Verlag 1991 pp 193–230

    • Search Google Scholar
    • Export Citation
  • 17.

    Ojemann GAWhitaker HA: The bilingual brain. Arch Neurol 35:4094121978Ojemann GA Whitaker HA: The bilingual brain. Arch Neurol 35:409–412 1978

    • Search Google Scholar
    • Export Citation
  • 18.

    Ojemann SGBerger MSLettich Eet al: Localization of language function in children: results of electrical stimulation mapping. J Neurosurg 98:4654702003Ojemann SG Berger MS Lettich E et al: Localization of language function in children: results of electrical stimulation mapping. J Neurosurg 98:465–470 2003

    • Search Google Scholar
    • Export Citation
  • 19.

    Perani DDehaene SGrassi Fet al: Brain processing of native and foreign languages. Neuroreport 7:243924441996Perani D Dehaene S Grassi F et al: Brain processing of native and foreign languages. Neuroreport 7:2439–2444 1996

    • Search Google Scholar
    • Export Citation
  • 20.

    Perani DPaulesu EGalles NSet al: The bilingual brain. Proficiency and age of acquisition of the second language. Brain 121:184118521998Perani D Paulesu E Galles NS et al: The bilingual brain. Proficiency and age of acquisition of the second language. Brain 121:1841–1852 1998

    • Search Google Scholar
    • Export Citation
  • 21.

    Pouratian NBookheimer SYO'Farrell AMet al: Optical imaging of bilingual cortical representations. Case report. J Neurosurg 93:6766812000Pouratian N Bookheimer SY O'Farrell AM et al: Optical imaging of bilingual cortical representations. Case report. J Neurosurg 93:676–681 2000

    • Search Google Scholar
    • Export Citation
  • 22.

    Pouratian NBookheimer SYRex DEet al: Utility of preoperative functional magnetic resonance imaging for identifying language cortices in patients with vascular malformations. J Neurosurg 97:21322002Pouratian N Bookheimer SY Rex DE et al: Utility of preoperative functional magnetic resonance imaging for identifying language cortices in patients with vascular malformations. J Neurosurg 97:21–32 2002

    • Search Google Scholar
    • Export Citation
  • 23.

    Rapport RLTan CTWhitaker HA: Language function and dysfunction among Chinese-and English-speaking polyglots: cortical stimulation, Wada testing, and clinical studies. Brain Lang 18:3423661983Rapport RL Tan CT Whitaker HA: Language function and dysfunction among Chinese-and English-speaking polyglots: cortical stimulation Wada testing and clinical studies. Brain Lang 18:342–366 1983

    • Search Google Scholar
    • Export Citation
  • 24.

    Roux FEBoulanouar KLotterie JAet al: Language functional magnetic resonance imaging in preoperative assessment of language areas: correlation with direct cortical stimulation. Neurosurgery 52:133513472003Roux FE Boulanouar K Lotterie JA et al: Language functional magnetic resonance imaging in preoperative assessment of language areas: correlation with direct cortical stimulation. Neurosurgery 52:1335–1347 2003

    • Search Google Scholar
    • Export Citation
  • 25.

    Roux FETremoulet M: Organization of language areas in bilingual patients: a cortical stimulation study. J Neurosurg 97:8578642002Roux FE Tremoulet M: Organization of language areas in bilingual patients: a cortical stimulation study. J Neurosurg 97:857–864 2002

    • Search Google Scholar
    • Export Citation
  • 26.

    Schlosser MJLuby MSpencer DDet al: Comparative localization of auditory comprehension by using functional magnetic resonance imaging and cortical stimulation. J Neurosurg 91:6266351999Schlosser MJ Luby M Spencer DD et al: Comparative localization of auditory comprehension by using functional magnetic resonance imaging and cortical stimulation. J Neurosurg 91:626–635 1999

    • Search Google Scholar
    • Export Citation
  • 27.

    Simos PGCastillo EMFletcher JMet al: Mapping of receptive language cortex in bilingual volunteers by using magnetic source imaging. J Neurosurg 95:76812001Simos PG Castillo EM Fletcher JM et al: Mapping of receptive language cortex in bilingual volunteers by using magnetic source imaging. J Neurosurg 95:76–81 2001

    • Search Google Scholar
    • Export Citation
  • 28.

    Walker JAQuinones-Hinojosa ABerger MS: Intraoperative speech mapping in 17 bilingual patients undergoing resection of a mass lesion. Neurosurgery 54:1131182004Walker JA Quinones-Hinojosa A Berger MS: Intraoperative speech mapping in 17 bilingual patients undergoing resection of a mass lesion. Neurosurgery 54:113–118 2004

    • Search Google Scholar
    • Export Citation
  • 29.

    Weber-Fox CNeville HJ. Maturational constraints on functional specialization for language processing: ERP and behavioral evidence in bilingual speakers. J Cogn Neurosci 8:2312561996Weber-Fox C Neville HJ. Maturational constraints on functional specialization for language processing: ERP and behavioral evidence in bilingual speakers. J Cogn Neurosci 8:231–256 1996

    • Search Google Scholar
    • Export Citation
  • 30.

    Yetkin FZMueller WMMorris GLet al: Functional MR activation correlated with intraoperative cortical mapping. AJNR 18:131113151997Yetkin FZ Mueller WM Morris GL et al: Functional MR activation correlated with intraoperative cortical mapping. AJNR 18:1311–1315 1997

    • Search Google Scholar
    • Export Citation
  • 31.

    Yetkin OZerrin Yetkin FHaughton VMet al: Use of functional MR to map language in multilingual volunteers. AJNR 17:4734771996Yetkin O Zerrin Yetkin F Haughton VM et al: Use of functional MR to map language in multilingual volunteers. AJNR 17:473–477 1996

    • Search Google Scholar
    • Export Citation
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