Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-14T13:25:15.137Z Has data issue: false hasContentIssue false

Individual differences in bilingual experience modulate executive control network and performance: behavioral and structural neuroimaging evidence

Published online by Cambridge University Press:  11 September 2020

Federico Gallo*
Affiliation:
Centre for Cognition and Decision Making, Institute for Cognitive Neuroscience, National Research University Higher School of Economics, Moscow, Russian Federation Centre for Neurolinguistics and Psycholinguistics, Vita-Salute San Raffaele University, Milan, Italy
Nikolay Novitskiy
Affiliation:
Department of Linguistics and Modern Languages, The Chinese University of Hong Kong, Hong Kong, China Brain and Mind Institute, The Chinese University of Hong Kong, Hong Kong, China
Andriy Myachykov
Affiliation:
Centre for Cognition and Decision Making, Institute for Cognitive Neuroscience, National Research University Higher School of Economics, Moscow, Russian Federation Northumbria University, Newcastle-upon-Tyne, United Kingdom
Yury Shtyrov
Affiliation:
Centre for Cognition and Decision Making, Institute for Cognitive Neuroscience, National Research University Higher School of Economics, Moscow, Russian Federation Center of Functionally Integrative Neuroscience, Aarhus University, Aarhus, Denmark
*
Address for correspondence: Federico Gallo, E-mail: [email protected]

Abstract

Dual/multiple language use has been shown to affect cognition and its neural substrate, although the replicability of such findings varies, partially due to neglecting the role of interindividual variability in bilingual experience. To address this, we operationalized the main bilingual experience factors as continuous variables, investigating their effects on executive control performance and neural substrate deploying a Flanker task and structural magnetic resonance imaging. First, higher L2 proficiency predicted better executive performance. Second, neuroimaging results indicated that bilingualism-related neuroplasticity may peak at a certain stage of bilingual experience and eventually revert, possibly following functional specialization. Importantly, experienced bilinguals optimized behavioral performance independently of volumetric variations, suggesting a degree of performance gain even with lower GMV. Hence, the effects of bilingualism on cognition may evolve with experience, with improvements in functional efficiency eventually replacing structural changes. We conclude that individual differences in bilingual experience modulate cognitive and neural consequences of bilingualism.

Type
Research Article
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abutalebi, J and Green, D (2007) Bilingual language production: The neurocognition of language representation and control. Journal of neurolinguistics 20, 242275.CrossRefGoogle Scholar
Abutalebi, J, Della Rosa, PA, Green, DW, Hernandez, M, Scifo, P, Keim, R, Cappa, SF and Costa, A (2012) Bilingualism tunes the anterior cingulate cortex for conflict monitoring. Cerebral Cortex 22, 20762086.CrossRefGoogle ScholarPubMed
Abutalebi, J, Della Rosa, PA, Ding, G, Weekes, B, Costa, A and Green, DW (2013) Language proficiency modulates the engagement of cognitive control areas in multilinguals. Cortex 49, 905911.CrossRefGoogle ScholarPubMed
Abutalebi, J, Canini, M, Della Rosa, PA, Sheung, LP, Green, DW and Weekes, BS (2014) Bilingualism protects anterior temporal lobe integrity in aging. Neurobiology of aging 35, 21262133.CrossRefGoogle Scholar
Abutalebi, J, Guidi, L, Borsa, V, Canini, M, Della Rosa, PA, Parris, BA and Weekes, BS (2015) Bilingualism provides a neural reserve for aging populations. Neuropsychologia 69, 201210.CrossRefGoogle ScholarPubMed
Abutalebi, J and Green, DW (2016) Neuroimaging of language control in bilinguals: neural adaptation and reserve. Bilingualism: Language and cognition 19, 689698.CrossRefGoogle Scholar
Bates, D, Maechler, M, Bolker, B and Walker, S (2014) lme4: Linear Mixed-Effects Models Using Eigen and S4. Available online at: http://cran.r-project.org/package=lme4Google Scholar
Becker, M, Schubert, T, Strobach, T, Gallinat, J and Kühn, S (2016) Simultaneous interpreters vs. professional multilingual controls: Group differences in cognitive control as well as brain structure and function. Neuroimage 134, 250260.CrossRefGoogle ScholarPubMed
Bialystok, E, Craik, FI and Luk, G (2012) Bilingualism: consequences for mind and brain. Trends in cognitive sciences 16, 240250.CrossRefGoogle ScholarPubMed
Bialystok, E (2016) The signal and the noise: Finding the pattern in human behavior. Linguistic Approaches to Bilingualism 6, 517534.CrossRefGoogle Scholar
Bialystok, E (2017) The bilingual adaptation: How minds accommodate experience. Psychological bulletin 143, 233.CrossRefGoogle ScholarPubMed
Blumenfeld, HK and Marian, V (2007) Constraints on parallel activation in bilingual spoken language processing: Examining proficiency and lexical status using eye-tracking. Language and cognitive processes 22, 633660.CrossRefGoogle Scholar
Boekel, W, Wagenmakers, EJ, Belay, L, Verhagen, J, Brown, S and Forstmann, BU (2015) A purely confirmatory replication study of structural brain-behavior correlations. Cortex 66, 115133.CrossRefGoogle ScholarPubMed
Dahnke, R, Ziegler, G and Gaser, C (2012) Local adaptive segmentation. HBM 2012. http://www.neuro.unijena.de/hbm2012/HBM2012-Dahnke02.pdfGoogle Scholar
Del Maschio, N, Sulpizio, S, Gallo, F, Fedeli, D, Weekes, BS and Abutalebi, J (2018) Neuroplasticity across the lifespan and aging effects in bilinguals and monolinguals. Brain and cognition 125, 118126.CrossRefGoogle ScholarPubMed
Del Maschio, N, Sulpizio, S, Toti, M, Caprioglio, C, Del Mauro, G, Fedeli, D and Abutalebi, J (2019) Second language use rather than second language knowledge relates to changes in white matter microstructure. Journal of Cultural Cognitive Science, 111.Google Scholar
DeLuca, V, Rothman, J, Bialystok, E and Pliatsikas, C (2019) Redefining bilingualism as a spectrum of experiences that differentially affects brain structure and function. Proceedings of the National Academy of Sciences 116, 75657574.CrossRefGoogle ScholarPubMed
Diamond, A (2013) Executive functions. Annual review of psychology 64, 135168.CrossRefGoogle ScholarPubMed
Dong, Y and Xie, Z (2014) Contributions of second language proficiency and interpreting experience to cognitive control differences among young adult bilinguals. Journal of Cognitive Psychology 26, 506519.CrossRefGoogle Scholar
ESS Round 8: European Social Survey Round 8 Data (2016) Data file edition 2.1. NSD - Norwegian Centre for Research Data, Norway – Data Archive and distributor of ESS data for ESS ERIC. doi:10.21338/NSD-ESS8-2016.CrossRefGoogle Scholar
Fan, J, McCandliss, BD, Sommer, T, Raz, A and Posner, MI (2002) Testing the efficiency and independence of attentional networks. Journal of cognitive neuroscience 14, 340347.CrossRefGoogle ScholarPubMed
Gallo, F, Myachykov, A, Shtyrov, Y and Abutalebi, J (2020) Cognitive and Brain Reserve in Bilinguals: Field Overview and Explanatory Mechanisms. Journal of Cultural Cognitive Science, doi:10.1007/s41809-020-00058-1. Published online by Springer Nature, May 13, 2020.CrossRefGoogle Scholar
García-Pentón, L, Fernandez Garcia, Y, Costello, B, Duñabeitia, JA and Carreiras, M (2016) The neuroanatomy of bilingualism: how to turn a hazy view into the full picture. Language, Cognition and Neuroscience 31, 303327.CrossRefGoogle Scholar
Gaser, C (2020) CAT, A Computational Anatomy Toolbox for SPM. http://dbm.neuro.uni-jena.de/cat/Google Scholar
Gold, BT, Johnson, NF and Powell, DK (2013) Lifelong bilingualism contributes to cognitive reserve against white matter integrity declines in aging. Neuropsychologia 51, 28412846.CrossRefGoogle Scholar
Gollan, TH, Salmon, DP, Montoya, RI and Galasko, DR (2011) Degree of bilingualism predicts age of diagnosis of Alzheimer's disease in low-education but not in highly educated Hispanics. Neuropsychologia 49, 38263830.CrossRefGoogle Scholar
Green, DW and Abutalebi, J (2013) Language control in bilinguals: The adaptive control hypothesis. Journal of Cognitive Psychology 25, 515530.CrossRefGoogle ScholarPubMed
Grogan, A, Green, DW, Ali, N, Crinion, JT and Price, CJ (2009) Structural correlates of semantic and phonemic fluency ability in first and second languages. Cerebral cortex 19, 26902698.CrossRefGoogle ScholarPubMed
Grogan, A, Jones, ŌP, Ali, N, Crinion, J, Orabona, S, Mechias, ML, Ramsden, S, Green, DW and Price, CJ (2012) Structural correlates for lexical efficiency and number of languages in non-native speakers of English. Neuropsychologia 50, 13471352.CrossRefGoogle ScholarPubMed
Guo, T and Peng, D (2006) Event-related potential evidence for parallel activation of two languages in bilingual speech production. NeuroReport 17, 17571760.CrossRefGoogle ScholarPubMed
Hervais-Adelman, A, Egorova, N and Golestani, N (2018) Beyond bilingualism: multilingual experience correlates with caudate volume. Brain Structure and Function 223, 34953502.CrossRefGoogle ScholarPubMed
Iluz-Cohen, P and Armon-Lotem, S (2013) Language proficiency and executive control in bilingual children. Bilingualism: Language and Cognition 16, 884899.CrossRefGoogle Scholar
Kaushanskaya, M and Marian, V (2007) Bilingual language processing and interference in bilinguals: Evidence from eye tracking and picture naming. Language Learning 57, 119163.CrossRefGoogle Scholar
Kroll, JF, Bobb, SC and Hoshino, N (2014) Two languages in mind: bilingualism as a tool to investigate language, cognition, and the brain. Current Directions in Psychological Science 23, 159163.CrossRefGoogle Scholar
Kroll, JF, Dussias, PE, Bice, K and Perrotti, L (2015) Bilingualism, mind, and brain. Annual Review of Linguistics 1, 377394.CrossRefGoogle ScholarPubMed
Kuznetsova, A, Brockhoff, PB and Christensen, RHB (2017) lmerTest package: tests in linear mixed effects models. Journal of Statistical Software 82(13).CrossRefGoogle Scholar
Lehtonen, M, Soveri, A, Laine, A, Järvenpää, J, de Bruin, A and Antfolk, J (2018) Is bilingualism associated with enhanced executive functioning in adults? A meta-analytic review. Psychological bulletin 144, 394425.CrossRefGoogle ScholarPubMed
Li, P, Legault, J and Litcofsky, KA (2014) Neuroplasticity as a function of second language learning: anatomical changes in the human brain. Cortex 58, 301324.CrossRefGoogle ScholarPubMed
Lüdecke, D (2018) ggeffects: Tidy Data Frames of Marginal Effects from Regression Models. Journal of Open Source Software 3(26), 772. doi: 10.21105/joss.00772CrossRefGoogle Scholar
Luk, G, Anderson, JA, Craik, FI, Grady, C and Bialystok, E (2010) Distinct neural correlates for two types of inhibition in bilinguals: Response inhibition versus interference suppression. Brain and cognition 74(3), 347357.CrossRefGoogle ScholarPubMed
Luk, G, Bialystok, E, Craik, FI and Grady, CL (2011a) Lifelong bilingualism maintains white matter integrity in older adults. Journal of Neuroscience 31, 1680816813.CrossRefGoogle Scholar
Luk, G, De Sa, E and Bialystok, E (2011b) Is there a relation between onset age of bilingualism and enhancement of cognitive control?. Bilingualism: Language and cognition 14, 588595.CrossRefGoogle Scholar
Luk, G and Bialystok, E (2013) Bilingualism is not a categorical variable: Interaction between language proficiency and usage. Journal of Cognitive Psychology 25, 605621.CrossRefGoogle Scholar
MacArthur foundation (2007) The MacArthur Research Network on Socioeconomic Status and Health. https://macses.ucsf.edu/research/psychosocial/subjective.php#measurementGoogle Scholar
Manjón, JV, Coupé, P, Martí-Bonmatí, L, Collins, DL and Robles, M (2010) Adaptive non-local means denoising of MR images with spatially varying noise levels. Journal of Magnetic Resonance Imaging 31, 192203.CrossRefGoogle ScholarPubMed
Marian, V, Blumenfeld, HK and Kaushanskaya, M (2007) The Language Experience and Proficiency Questionnaire (LEAP-Q): Assessing language profiles in bilinguals and multilinguals. Journal of Speech, Language, and Hearing Research.CrossRefGoogle ScholarPubMed
Masouleh, SK, Eickhoff, SB, Hoffstaedter, F, Genon, S, & Alzheimer's Disease Neuroimaging Initiative. (2019) Empirical examination of the replicability of associations between brain structure and psychological variables. Elife 8, e43464.CrossRefGoogle Scholar
Mechelli, A, Crinion, JT, Noppeney, U, O'doherty, J, Ashburner, J, Frackowiak, RS and Price, CJ (2004) Neurolinguistics: structural plasticity in the bilingual brain. Nature 431, 757757.CrossRefGoogle ScholarPubMed
Milton, J (2009) Measuring second language vocabulary acquisition (Vol. 45). Bristol: Multilingual Matters.CrossRefGoogle Scholar
Mishra, RK, Hilchey, MD, Singh, N and Klein, RM (2012) On the time course of exogenous cueing effects in bilinguals: higher proficiency in a second language is associated with more rapid endogenous disengagement. The Quarterly journal of experimental psychology 65, 15021510.CrossRefGoogle Scholar
Mishra, RK (2015) Let's not forget about language proficiency and cultural variations while linking bilingualism to executive control. Bilingualism: Language and Cognition 18, 3940.CrossRefGoogle Scholar
Neurobehavioral Systems, Inc. (2020) Presentation. https://www.neurobs.comGoogle Scholar
Neuromorphometrics, Inc. Building a Model of the Living Human Brain. http://Neuromorphometrics.com/Google Scholar
Novitskiy, N, Myachykov, A and Shtyrov, Y (2019a) Crosslinguistic interplay between semantics and phonology in late bilinguals: neurophysiological evidence. Bilingualism: Language and Cognition 22, 209227.CrossRefGoogle Scholar
Novitskiy, N, Shtyrov, Y and Myachykov, A (2019b) Conflict resolution ability in late bilinguals improves with increased second-language proficiency: ANT task evidence. Frontiers in Psychology 10, 2825.CrossRefGoogle Scholar
Oldfield, RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97113.CrossRefGoogle ScholarPubMed
Paap, KR, Johnson, HA and Sawi, O (2015) Bilingual advantages in executive functioning either do not exist or are restricted to very specific and undetermined circumstances. Cortex 69, 265278.CrossRefGoogle ScholarPubMed
Perani, D, Abutalebi, J, Paulesu, E, Brambati, S, Scifo, P, Cappa, SF and Fazio, F (2003) The role of age of acquisition and language usage in early, high-proficient bilinguals: An fMRI study during verbal fluency. Human brain mapping 19, 170182.CrossRefGoogle ScholarPubMed
Pliatsikas, C, Johnstone, T and Marinis, T (2014) Grey matter volume in the cerebellum is related to the processing of grammatical rules in a second language: a structural voxel-based morphometry study. The Cerebellum 13, 5563.CrossRefGoogle Scholar
Pliatsikas, C, DeLuca, V, Moschopoulou, E and Saddy, JD (2017) Immersive bilingualism reshapes the core of the brain. Brain Structure and Function 222, 17851795.CrossRefGoogle ScholarPubMed
Pliatsikas, C (2019) Understanding structural plasticity in the bilingual brain: The Dynamic Restructuring Model. Bilingualism: Language and Cognition, 113.Google Scholar
R Core Team. (2014) R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available online at: http://www.R-project.org/Google Scholar
Rajapakse, JC, Giedd, JN and Rapoport, JL (1997) Statistical approach to segmentation of single-channel cerebral MR images. IEEE transactions on medical imaging 16, 176186.CrossRefGoogle ScholarPubMed
Raven, J, Raven, JC and Court, JH (2000) Manual for Raven's progressive matrices and vocabulary scales. Section 3: The standard progressive matrices. Oxford, UK: Oxford Psychologists Press; San Antonio, TX: The Psychological Corporation.Google Scholar
Rosselli, M, Ardila, A, Lalwani, LN and Vélez-Uribe, I (2016) The effect of language proficiency on executive functions in balanced and unbalanced Spanish–English bilinguals. Bilingualism: Language and Cognition 19, 489503.CrossRefGoogle Scholar
Singh, N and Mishra, RK (2012) Does language proficiency modulate oculomotor control? Evidence from Hindi–English bilinguals. Bilingualism: Language and Cognition 15, 771781.CrossRefGoogle Scholar
Singh, N and Mishra, RK (2013) Second language proficiency modulates conflict-monitoring in an oculomotor Stroop task: Evidence from Hindi-English bilinguals. Frontiers in psychology 4, 322.CrossRefGoogle Scholar
Sorge, GB, Toplak, ME and Bialystok, E (2017) Interactions between levels of attention ability and levels of bilingualism in children's executive functioning. Developmental science 20, e12408.CrossRefGoogle ScholarPubMed
Surrain, S and Luk, G (2019) Describing bilinguals: A systematic review of labels and descriptions used in the literature between 2005–2015. Bilingualism: Language and Cognition 22, 115.CrossRefGoogle Scholar
Tao, L, Marzecová, A, Taft, M, Asanowicz, D and Wodniecka, Z (2011) The efficiency of attentional networks in early and late bilinguals: the role of age of acquisition. Frontiers in psychology 2, 123.CrossRefGoogle ScholarPubMed
Tohka, J, Zijdenbos, A and Evans, A (2004) Fast and robust parameter estimation for statistical partial volume models in brain MRI. Neuroimage 23, 8497.CrossRefGoogle ScholarPubMed
Treffers-Daller, J (2019) What defines language dominance in bilinguals?. Annual Review of Linguistics 5, 375393.CrossRefGoogle Scholar
Tucker, A and Stern, Y (2011) Cognitive reserve in aging. Current Alzheimer Research 8, 354360.CrossRefGoogle Scholar
Valian, V (2015) Bilingualism and cognition. Bilingualism: Language and Cognition 18(1), 324.CrossRefGoogle Scholar
Van Hell, JG and Dijkstra, T (2002) Foreign language knowledge can influence native language performance in exclusively native contexts. Psychonomic bulletin & review 9, 780789.CrossRefGoogle ScholarPubMed
Wu, YJ and Thierry, G (2010) Chinese–English bilinguals reading English hear Chinese. Journal of Neuroscience 30, 76467651.CrossRefGoogle ScholarPubMed
Xie, Z (2018) The Influence of Second Language (L2) Proficiency on Cognitive Control Among Young Adult Unbalanced Chinese-English Bilinguals. Frontiers in psychology 9, 412.CrossRefGoogle ScholarPubMed
Yeung, N (2014) Conflict monitoring and cognitive control. In: Ochsner, KN and Kosslyn, S (eds), The Oxford Handbook of Cognitive Neuroscience: Volume 2: The Cutting Edges. Oxford-New York. Oxford University Press.Google Scholar