Where, when and why brain activation differs for bilinguals and monolinguals during picture naming and reading aloud
Parker-Jones, O., Green, D. W., Grogan, A., Pliatsikas, C., Filippopolitis, K., Ali, N., Lee, H. L., Ramsden, S., Gazarian, K., Prejawa, S., Seghier, M. L. and Price, C. J. (2012) Where, when and why brain activation differs for bilinguals and monolinguals during picture naming and reading aloud. Cerebral Cortex, 22 (4). pp. 892-902. ISSN 1460-2199
To link to this article DOI: 10.1093/cercor/bhr161
Using functional magnetic resonance imaging, we found that when bilinguals named pictures or read words aloud, in their native or nonnative language, activation was higher relative to monolinguals in 5 left hemisphere regions: dorsal precentral gyrus, pars triangularis, pars opercularis, superior temporal gyrus, and planum temporale. We further demonstrate that these areas are sensitive to increasing demands on speech production in monolinguals. This suggests that the advantage of being bilingual comes at the expense of increased work in brain areas that support monolingual word processing. By comparing the effect of bilingualism across a range of tasks, we argue that activation is higher in bilinguals compared with monolinguals because word retrieval is more demanding; articulation of each word is less rehearsed; and speech output needs careful monitoring to avoid errors when competition for word selection occurs between, as well as within,language.
• Abutalebi J. 2008. Neural aspects of second language representation and language control. Acta Psychol. 128:466--478. • Abutalebi J, Annoni JM, Zimine I, Pegna AJ, Seghier ML, Lee-Jahnke H, Lazeyras F, Cappa SF, Khateb A. 2008. Language control and lexical competition in bilinguals: an event-related fMRI study. Cereb Cortex 18:1496--1505. • Abutalebi J, Green DW. 2007. Bilingual language production: the neurocognition of language representation and control. J Neurolinguist. 20:242--275. • Andersson JLR, Hutton C, Ashburner J, Turner R, Friston K. 2001. Modelling geometric deformations in EPI time series. Neuroimage. 13:903--919. • Bohland JW, Guenther FH. 2006. An fMRI investigation of syllable sequence production. Neuroimage. 32:821--841. • Britton B, Blumstein SE, Myers EB, Grindrod C. 2009. The role of the spectral and durational properties on hemispheric asymmetries in vowel perception. Neuropsychologia. 47:1096--1106. • Brown S, Laird AR, Pfordresher PQ, Thelen SM, Turkeltaub P, Liotti M. 2009. The somatotopy of speech: phonation and articulation in the human motor cortex. Brain Cogn. 70:31--41. • Callan DE, Jones JA, Callan AM, Akahane-Yamada R. 2004. Phonetic perceptual identification by native- and second-language speakers differentially activates brain regions involved with acoustic phonetic processing and those involved with articulatory-auditory/ orosensory internal models. Neuroimage. 22:1182--1194. • Chee MW, Hon N, Lee HL, Soon CS. 2001. Relative language proficiency modulates BOLD signal change when bilinguals perform semantic judgments: blood oxygen level dependent. Neuroimage.13:1155--1163. • Crinion J, Turner R, Grogan A, Hanakawa T, Noppeney U, Devlin JT, Aso T, Urayama S, Fukuyama H, Stockton K, et al. 2006. Language control in the bilingual brain. Science. 312:1537--1540. • Devlin JT, Matthews PM, Rushworth MF. 2003. Semantic processing in the left inferior prefrontal cortex: a combined functional magnetic resonance imaging and transcranial magnetic stimulation study. J Cogn Neurosci. 15:71--84. • Dhanjal NS, Handunnetthi L, Patel MC, Wise RJ. 2008. Perceptual systems controlling speech production. J Neurosci. 28:9969--9975. • Dronkers NF. 1996. A new brain region for coordinating speech articulation. Nature. 384:159--161. • Fridriksson J, Moser D, Ryalls J, Bonilha L, Rorden C, Baylis G. 2009. Modulation of frontal lobe speech areas associated with the production and perception of speech movements. J Speech Lang Hear Res. 52:812--819. • Gollan TH, Acenas LA. 2004. What is a TOT? Cognate and translation effects on tip-of-the-tongue states in Spanish-English and Tagalog- English bilinguals. J Exp Psychol Learn Mem Cogn. 30:246--269. • Gollan TH, Montoya RI, Bonanni MP. 2005. Proper names get stuck on bilingual and monolingual speakers’ tip of the tongue equally often. Neuropsychology. 19:278--287. • Gollan TH, Montoya RI, Cera CM, Sandoval TC. 2008. More use almost always means a smaller frequency effect: aging, bilingualism, and the weaker links hypothesis. J Mem Lang. 58:787--814. • Gollan TH, Montoya RI, Werner GA. 2002. Semantic and letter fluency in Spanish-English bilinguals. Neuropsychology. 16:562--576. • Graves WW, Grabowski TJ, Mehta S, Gordon JK. 2007. A neural signature of phonological access: distinguishing the effects of word frequency from familiarity and length in overt picture naming. J Cogn Neurosci. 19:617--631. • Green DW. 1986. Control, activation, and resource: a framework and a model for the control of speech in bilinguals. Brain Lang. 27:210--223. • Green DW. 1998. Mental control of the bilingual lexico-semantic system. Biling Lang Cogn. 1:67--81. • Green DW, Grogan A, Crinion J, Ali N, Sutton C, Price CJ. 2010. Language control and parallel recovery of language in individuals with aphasia. Aphasiology. 24:188--209. • Grogan A, Green DW, Ali N, Crinion J, Price CJ. 2009. Structural correlates of semantic and phonemic fluency ability first and second languages. Cereb Cortex. 19:2690--2698. • Grosjean F. 1992. Another view of bilingualism. In: Harris RJ, editor. Cognitive processing in bilinguals. Amsterdam: Elsevier. p. 51--62. • Grosjean F. 1998. Studying bilinguals: methodological and conceptual issues. Biling Lang Cogn. 1:131--140. • Grosjean F. 2001. The bilingual’s language modes. In: Nicol J, editor. One mind, two languages: bilingual language processing. Oxford: Blackwell. p. 1--22. • Hu W, Lee HL, Zhang Q, Liu T, Geng LB, Seghier ML, Shakeshaft C, Twomey T, Green DW, Yang YM, et al. 2010. Developmental dyslexia in Chinese and English populations: dissociating the effect of dyslexia from language differences. Brain. 133:1694--1706. • Ivanova I, Costa A. 2008. Does bilingualism hamper lexical access in speech production. Acta Psychol. 127:277--288. • Jescheniak JD, Schriefers H. 1998. Discrete serial versus cascaded processing in lexical access in speech production: further evidence from the coactivation of near-synonyms. J Exp Psychol Learn Mem Cogn. 24:1256--1274. • Kay J, Lesser R, Coltheart M. 1992. Psycholinguistic assessment of language processing in aphasia. Hove (UK): Psychology Press. • Khateb A, Abutalebi J, Michel CM, Pegna AJ, Lee-Jahnke H, Annoni JM. 2007. Language selection in bilinguals: a spatio-temporal analysis of electric brain activity. Int J Psychophysiol. 65:201--213. • Kittredge AK, Dell GS, Verkuilen J, Schwartz MF. 2008. Where is the effect of frequency in word production? Insights from aphasic picture-naming errors. Cogn Neuropsychol. 25:463--492. • Koechlin E, Ody C, Kouneiher F. 2003. The architecture of cognitive control in the human prefrontal cortex. Science. 302:1181--1185. • Kovelman I, Baker SA, Petitto LA. 2008. Bilingual and monolingual brains compared: a functional magnetic resonance imaging investigation of syntactic processing and a possible ‘‘neural signature’’ of bilingualism. J Cogn Neurosci. 20:153--169. • Kovelman I, Shalinsky MH, Berens MS, Petitto LA. 2008. Shining new light on the brain’s ‘‘bilingual signature’’: a functional Near Infrared Spectroscopy investigation of semantic processing. Neuroimage. 39:1457--1471. • Kovelman I, Shalinsky MH, White KS, Schmitt SN, Berens MS, Paymer N, Petitto LA. 2009. Dual language use in sign-speech bimodal bilinguals: fNIRS brain-imaging evidence. Brain Lang. 109:112--123. • Leff AP, Iverson P, Schofield TM, Kilner JM, Crinion JT, Friston K, Price CJ. 2009. Vowel specific mismatch responses in the anterior superior temporal gyrus: an fMRI study. Cortex. 45:517--526. • Liu H, Hu Z, Guo T, Peng D. 2010. Speaking words in two languages with one brain: neural overlap and dissociation. Brain Res. 1316:75--82. • Long DL, Prat CS. 2002. Working memory and Stroop interference: an individual differences investigation. Mem Cognit. 30:294--301. • Maess B, Friederici AD, Damian M, Meyer AS, Levelt JM. 2002. Semantic category interference in overt picture naming: sharpening current density localization by PCA. J Cogn Neurosci. 14:455--462. • Magiste E. 1979. The competing language systems of the multilingual: a developmental study of decoding and encoding processes. J Verb Learn Verb Behav. 18:79--89. • Meschyan G, Hernandez AE. 2006. Impact of language proficiency and orthographic transparency on bilingual word reading: an fMRI investigation. Neuroimage. 29:1135--1140. • Moser D, Fridriksson J, Bonilha L, Healy EW, Baylis G, Baker JM, Rorden C. 2009. Neural recruitment for the production of native and novel speech sounds. Neuroimage. 46:549--557. • Navarrete E, Basagni B, Alario XF, Costa A. 2006. Does word frequency affect lexical selection in speech production? Q J Exp Psychol. 10:1681--1690. • Nosarti C, Mechelli A, Green DW, Price C. 2010. The impact of second language learning on semantic and nonsemantic first language reading. Cerebral Cortex. 20:315--327. • Papoutsi M, de Zwart JA, Jansam JM, Pickering MJ, Bednar JA, Horwitz B. 2009. From phonemes to articulatory codes: an fMRI study of the role of Broca’s area in speech production. Cereb Cortex. 19:2156--2165. • Perani D, Paulesu E, Galles NS, Dupoux E, Dehaene S, Bettinardi V, Cappa SF, Fazio F, Mehler J. 1998. The bilingual brain: proficiency and age of acquisition of the second language. Brain Lang. 121:1841--1852. • Peterson RR, Savoy P. 1998. Lexical selection and phonological encoding during language production: evidence for cascaded processing. J Exp Psychol Learn Mem Cogn. 24:539--557. • Price CJ. 2010. The anatomy of language: a review of 100 fMRI studies published in 2009. Ann N Y Acad Sci. 1191:62--88. • Price CJ, Wise RJ, Warburton EA, Moore CJ, Howard D, Patterson K, Frackowiak R, Friston K. 1996. Hearing and saying: the functional neuro-anatomy of auditory word processing. Brain. 119:919--931. • Pyers JE, Gollan TH, Emmorey K. 2009. Bimodal bilinguals reveal the source of tip-of-the-tongue states. Cognition. 112:323--329. • Ransdell SE, Fischler I. 1987. Imagery skill and preference in bilinguals. Appl Cogn Psychol. 5:97--112. • Rodriguez-Fornells A, Rotte M, Heinze HJ, Nosselt T, Munte TF. 2002. Brain potential and functional MRI evidence for how to handle two languages with one brain. Nature. 415:1026--1029. • Rodriguez-Fornells A, van der Lugt A, Rotte M, Britti B, Heinze HJ,Mu nte TF. 2005. Second language interferes with word production in fluent bilinguals: brain potential and functional imaging evidence. J Cogn Neurosci. 17:422--433. • Shuster LI. 2009. The effect of sublexical and lexical frequency on speech production: an fMRI investigation. Brain Lang. 111:66--72. • Stroop JR. 1935. Studies of interference in serial verbal reactions. J Exp Psychol. 18:643--662. • Takaso H, Eisner F, Wise RJ, Scott SK. 2010. The effect of delayed auditory feedback on activity in the temporal lobe while speaking: a positron emission tomography study. J Speech Lang Hear Res. 53:226--236. • van Heuven WJ, Dijkstra T. 2010. Language comprehension in the bilingual brain: fMRI and ERP support psycholinguistic models. Brain Res Rev. 64:104--122. • Veltman DJ, Mechelli A, Friston K, Price CJ. 2002. The importance of distributed sampling in blocked functional magnetic resonance imaging designs. Neuroimage. 17:1203--1206. • Wise RJ, Greene J, Bu¨ chel C, Scott SK. 1999. Brain regions involved in articulation. Lancet. 353:1057--1061. • Wu YJ, Thierry G. 2010. Chinese-English bilinguals reading English hear Chinese. J Neurosci. 30:7646--7651. • Zheng ZZ, Munhall KG, Johnsrude IS. 2009. Functional overlap between regions involved in speech perception and in monitoring one’s own voice during speech production. J Cogn Neurosci. 22:1770--1781.