Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-22T22:47:46.910Z Has data issue: false hasContentIssue false

Linguistic immersion and structural effects on the bilingual brain: a longitudinal study

Published online by Cambridge University Press:  24 July 2018

VINCENT DELUCA
Affiliation:
School of Psychology and Clinical Language Sciences, University of Reading, UK
JASON ROTHMAN
Affiliation:
School of Psychology and Clinical Language Sciences, University of Reading, UK UiT the Arctic University of Norway
CHRISTOS PLIATSIKAS*
Affiliation:
School of Psychology and Clinical Language Sciences, University of Reading, UK
*
Address for correspondence: Christos Pliatsikas, School of Psychology and Clinical Language Sciences, University of Reading, RG6 6AL, UK[email protected]

Abstract

Learning and using additional languages can result in structural changes in the brain. However, the time course of these changes, as well as the factors the predict them, are still not well understood. In this longitudinal study we test the effects of bilingual immersion on brain structure of adult sequential bilinguals not undergoing any language training, who were scanned twice, three years apart. We observed significant increases in grey matter volume in the lower left cerebellum, mean white matter diffusivity in the frontal cortex, and reshaping of the left caudate nucleus and amygdala and bilateral hippocampus. Moreover, both prior length of immersion and L2 age of acquisition were significant predictors of volumetric change in the cerebellum. Taken together, these results indicate that bilingualism-induced neurological changes continue to take place across the lifespan and are strongly related to the quantity and quality of bilingual immersion, even in highly-immersed adult bilingual populations.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

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.)

Footnotes

*This research was supported by a Research and Impact fund awarded by Centre for Literacy and Multilingualism (CeLM), University of Reading, as well as by the Centre for Integrative Neuroscience and Neurodynamics (CINN) at the University of Reading. We also gratefully acknowledge the reviewers for their helpful comments and suggestions to the manuscript. Finally, we thank Wafa Islam for assistance with the study, and our participants.

References

Abutalebi, J., Canini, M., Della Rosa, P. A., Green, D. W., & Weekes, B. S. (2015). The neuroprotective effects of bilingualism upon the inferior parietal lobule: A Structural Neuroimaging Study in Aging Chinese Bilinguals. Journal of Neurolinguistics, 33, 313. https://doi.org/10.1016/j.jneuroling.2014.09.008Google Scholar
Abutalebi, J., Della Rosa, P. A., Castro Gonzaga, A. K., Keim, R., Costa, A., & Perani, D. (2013). The role of the left putamen in multilingual language production. Brain and Language, 125 (3), 307315. https://doi.org/10.1016/j.bandl.2012.03.009Google Scholar
Abutalebi, J., & Green, D. W. (2016). Neuroimaging of language control in bilinguals: neural adaptation and reserve. Bilingualism: Language and Cognition, (April), 110. https://doi.org/10.1017/S1366728916000225Google Scholar
Ashburner, J., & Friston, K. J. (2000). Voxel-Based Morphometry – The Methods. NeuroImage, 11 (6), 805821. https://doi.org/10.1006/nimg.2000.0582Google Scholar
Bak, T. H. (2016). Cooking pasta in La Paz. Linguistic Approaches to Bilingualism, 5 (2016), 119. https://doi.org/10.1075/lab.16002.bakGoogle Scholar
Beckmann, C. F., Mackay, C. E., Filippini, N., & Smith, S. M. (2009). Group comparison of resting-state FMRI data using multi-subject ICA and dual regression. NeuroImage, 47 (Suppl 1), S148. https://doi.org/10.1073/pnas.0811879106Google Scholar
Beckmann, C. F., & Smith, S. M. (2004). Probabilistic Independent Component Analysis for Functional Magnetic Resonance Imaging. IEEE Transactions on Medical Imaging, 23 (2), 137152. https://doi.org/10.1109/TMI.2003.822821Google Scholar
Beckmann, C. F., & Smith, S. M. (2005). Tensorial extensions of independent component analysis for multisubject FMRI analysis. NeuroImage, 25 (1), 294311. https://doi.org/10.1016/j.neuroimage.2004.10.043Google Scholar
Behrens, T. E. J., Woolrich, M. W., Jenkinson, M., Johansen-Berg, H., Nunes, R. G., Clare, S., Matthews, P. M., Brady, J. M., & Smith, S. M. (2003). Characterization and Propagation of Uncertainty in Diffusion-Weighted MR Imaging. Magnetic Resonance in Medicine, 50 (5), 10771088. https://doi.org/10.1002/mrm.10609Google Scholar
Bellander, M., Berggren, R., Mårtensson, J., Brehmer, Y., Wenger, E., Li, T. Q., Bodammer, N. C., Shing, Y. L., Werkle-Bergner, M., & Lövdén, M. (2016). Behavioral correlates of changes in hippocampal gray matter structure during acquisition of foreign vocabulary. NeuroImage, 131, 205213. https://doi.org/10.1016/j.neuroimage.2015.10.020Google Scholar
Berken, J. A., Chai, X. J., Chen, J.-K., Gracco, V. L., & Klein, D. (2016). Effects of Early and Late Bilingualism on Resting-State Functional Connectivity. Journal of Neuroscience, 36 (4), 11651172. https://doi.org/10.1523/JNEUROSCI.1960-15.2016Google Scholar
Berken, J. A., Gracco, V. L., Chen, J. K., & Klein, D. (2016). The timing of language learning shapes brain structure associated with articulation. Brain Structure and Function, 221 (7), 35913600. https://doi.org/10.1007/s00429-015-1121-9Google Scholar
Berken, J. A., Gracco, V. L., & Klein, D. (2017). Early bilingualism, language attainment, and brain development. Neuropsychologia, 98, 220227. https://doi.org/10.1016/j.neuropsychologia.2016.08.031Google Scholar
Bialystok, E. (2016). The signal and the noise: Finding the pattern in human behavior. Linguistic Approaches to Bilingualism, 6 (5), 517534. https://doi.org/10.1075/lab.15040.biaGoogle Scholar
Bialystok, E. (2017). The Bilingual Adaptation: How Minds Accommodate Experience. Psychological Bulletin, 143 (3), 233262. https://doi.org/10.1037/bul0000099Google Scholar
Booth, J. R., Wood, L., Lu, D., Houk, J. C., & Bitan, T. (2007). The role of the basal ganglia and cerebellum in language processing. Brain Research, 1133, 136144. https://doi.org/10.1016/j.brainres.2006.11.074Google Scholar
Burgaleta, M., Sanjuán, A., Ventura-Campos, N., Sebastián-Gallés, N., & Ávila, C. (2016). Bilingualism at the core of the brain. Structural differences between bilinguals and monolinguals revealed by subcortical shape analysis. NeuroImage, 125, 437445. https://doi.org/10.1016/j.neuroimage.2015.09.073Google Scholar
Coggins, P. E., Kennedy, T. J., & Armstrong, T. A. (2004). Bilingual corpus callosum variability. Brain and Language, 89 (1), 6975. https://doi.org/10.1016/S0093-934X(03)00299-2Google Scholar
Cummine, J., & Boliek, C. A. (2013). Understanding white matter integrity stability for bilinguals on language status and reading performance. Brain Structure and Function, 218 (2), 595601. https://doi.org/10.1007/s00429-012-0466-6Google Scholar
Elmer, S., Hänggi, J., & Jäncke, L. (2014). Processing demands upon cognitive, linguistic, and articulatory functions promote grey matter plasticity in the adult multilingual brain: Insights from simultaneous interpreters. Cortex, 54 (1), 179189. https://doi.org/10.1016/j.cortex.2014.02.014Google Scholar
Felton, A., Vazquez, D., Ramos-Nunez, A. I., Greene, M. R., Macbeth, A., Hernandez, A. E., & Chiarello, C. (2017). Bilingualism influences structural indices of interhemispheric organization. Journal of Neurolinguistics, 42 (May), 111. https://doi.org/10.1016/j.jneuroling.2016.10.004Google Scholar
Filippi, R., Richardson, F. M., Dick, F., Leech, R., Green, D. W., Thomas, M. S. C., & Price, C. J. (2011). The Right Posterior Paravermis and the Control of Language Interference. Journal of Neuroscience, 31 (29), 1073210740. https://doi.org/10.1523/JNEUROSCI.1783-11.2011Google Scholar
Frenck-Mestre, C., Anton, J. L., Roth, M., Vaid, J., & Viallet, F. (2005). Articulation in early and late bilinguals’ two languages: evidence from functional magnetic resonance imaging. Neuroreport, 16 (7), 761765. https://doi.org/10.1097/00001756-200505120-00021Google Scholar
García-Pentón, L., Fernández García, Y., Costello, B., Duñabeitia, J. A., & Carreiras, M. (2016). The neuroanatomy of bilingualism: how to turn a hazy view into the full picture. Language, Cognition and Neuroscience, 3798 (September), 125. https://doi.org/10.1080/23273798.2015.1068944Google Scholar
Geranpayeh, A. (2003). A quick review of the English Quick Placement Test. UCLES Research Notes, (12), 810.Google Scholar
Gold, B. T., Johnson, N. F., & Powell, D. K. (2013). Lifelong bilingualism contributes to cognitive reserve against white matter integrity declines in aging. Neuropsychologia, 51 (13), 28412846. https://doi.org/10.1016/j.neuropsychologia.2013.09.037Google Scholar
Green, D. W. (2011). Language control in different contexts: The behavioral ecology of bilingual speakers. Frontiers in Psychology, 2 (MAY), 20092012. https://doi.org/10.3389/fpsyg.2011.00103Google Scholar
Green, D. W., & Abutalebi, J. (2013). Language control in bilinguals: The adaptive control hypothesis. Journal of Cognitive Psychology, 25, 116. https://doi.org/10.1080/20445911.2013.796377Google Scholar
Grogan, A., Green, D. W., Ali, N., Crinion, J. T., & Price, C. J. (2009). Structural correlates of semantic and phonemic fluency ability in first and second languages. Cerebral Cortex, 19 (11), 26902698. https://doi.org/10.1093/cercor/bhp023Google Scholar
Grundy, J. G., Anderson, J. A. E., & Bialystok, E. (2017). Neural Correlates of Cognitive Processing in Monolinguals and Bilinguals. Annals of the New York Academy of Sciences. https://doi.org/10.1111/nyas.13333Google Scholar
Hofstetter, S., Friedmann, N., & Assaf, Y. (2016). Rapid language-related plasticity: microstructural changes in the cortex after a short session of new word learning. Brain Structure and Function. https://doi.org/10.1007/s00429-016-1273-2Google Scholar
Hosoda, C., Tanaka, K., Nariai, T., Honda, M., & Hanakawa, T. (2013). Dynamic Neural Network Reorganization Associated with Second Language Vocabulary Acquisition: A Multimodal Imaging Study. The Journal of Neuroscience, 33 (34), 1366313672. https://doi.org/10.1523/JNEUROSCI.0410-13.2013Google Scholar
Jenkinson, M., Beckmann, C. F., Behrens, T. E. J., Woolrich, M. W., & Smith, S. M. (2012). Fsl. NeuroImage, 62 (2), 782790. https://doi.org/10.1016/j.neuroimage.2011.09.015Google Scholar
Klein, D., Mok, K., Chen, J. K., & Watkins, K. E. (2014). Age of language learning shapes brain structure: A cortical thickness study of bilingual and monolingual individuals. Brain and Language, 131, 2024. https://doi.org/10.1016/j.bandl.2013.05.014Google Scholar
Kousaie, S., Chai, X. J., Sander, K. M., & Klein, D. (2017). Simultaneous learning of two languages from birth positively impacts intrinsic functional connectivity and cognitive control. Brain and Cognition, 117 (June), 4956. https://doi.org/10.1016/j.bandc.2017.06.003Google Scholar
Kroll, J. F., & Chiarello, C. (2016). Language experience and the brain: variability, neuroplasticity, and bilingualism. Language, Cognition and Neuroscience, 31 (3), 345348. https://doi.org/10.1080/23273798.2015.1086009Google Scholar
Kuhl, P. K., Stevenson, J., Corrigan, N. M., van den Bosch, J. J. F., Can, D. D., & Richards, T. L. (2016). Neuroimaging of the bilingual brain: Structural brain correlates of listening and speaking in a second language. Brain and Language, 162, 19. https://doi.org/10.1016/j.bandl.2016.07.004Google Scholar
Li, L., Abutalebi, J., Emmorey, K., Gong, G., Yan, X., Feng, X., Zou, L., & Ding, G. (2017). How bilingualism protects the brain from aging: Insights from bimodal bilinguals. Human Brain Mapping, 4124, 41094124. https://doi.org/10.1002/hbm.23652Google Scholar
Llano, D. A. (2013). Functional imaging of the thalamus in language. Brain and Language, 126 (1), 6272. https://doi.org/10.1016/j.bandl.2012.06.004Google Scholar
Long, M. H. (2007). Problems in SLA. Mahwah, NJ.: Lawrence Erlbaum Associates.Google Scholar
Luk, G., & Bialystok, E. (2013). Bilingualism is not a categorical variable: Interaction between language proficiency and usage. Journal of Cognitive Psychology, 25 (5), 605621. https://doi.org/10.1080/20445911.2013.795574Google Scholar
Luk, G., Bialystok, E., Craik, F. I. M., & Grady, C. L. (2011). Lifelong Bilingualism Maintains White Matter Integrity in Older Adults. Journal of Neuroscience, 31 (46), 1680816813. https://doi.org/10.1523/JNEUROSCI.4563-11.2011Google Scholar
Luk, G., Green, D. W., Abutalebi, J., & Grady, C. L. (2011). Cognitive control for language switching in bilinguals: A quantitative meta-analysis of functional neuroimaging studies. Language and Cognitive Processes, 27 (10), 14791488. https://doi.org/10.1080/01690965.2011.613209Google Scholar
Luk, G., & Pliatsikas, C. (2016). Converging diversity to unity: commentary on The neuroanatomy of bilingualism. Language, Cognition and Neuroscience, 31 (3), 349352. https://doi.org/10.1080/23273798.2015.1119289Google Scholar
Mamiya, P. C., Richards, T. L., Coe, B. P., Eichler, E. E., & Kuhl, P. K. (2016). Brain white matter structure and COMT gene are linked to second-language learning in adults. Proceedings of the National Academy of Sciences, 16. https://doi.org/10.1073/pnas.1606602113Google Scholar
Marian, V., & Spivey, M. J. (2003). Competing activation in bilingual language processing: Within- and between-language competition. Bilingualism: Language and Cognition, 6 (2), 97115. https://doi.org/10.1017/S1366728903001068Google Scholar
Mårtensson, J., Eriksson, J., Bodammer, N. C., Lindgren, M., Johansson, M., Nyberg, L., & Lövdén, M. (2012). Growth of language-related brain areas after foreign language learning. NeuroImage, 63 (1), 240244. https://doi.org/10.1016/j.neuroimage.2012.06.043Google Scholar
Mechelli, A., Crinion, J. T., Noppeney, U., O'Doherty, J., Ashburner, J., Frackowiak, R. S. J., & Price, C. J. (2004). Structural plasticity in the bilingual brain. Nature, 431 (7010), 1 p following 757; discussion following 757. https://doi.org/10.1038/nature03016Google Scholar
Mohades, S. G., Struys, E., Van Schuerbeek, P., Mondt, K., Van De Craen, P., & Luypaert, R. (2012). DTI reveals structural differences in white matter tracts between bilingual and monolingual children. Brain Research, 1435, 7280. https://doi.org/10.1016/j.brainres.2011.12.005Google Scholar
Mohades, S. G., Van Schuerbeek, P., Rosseel, Y., Van De Craen, P., Luypaert, R., & Baeken, C. (2015). White-matter development is different in bilingual and monolingual children: A longitudinal DTI study. PLoS ONE, 10 (2), 116. https://doi.org/10.1371/journal.pone.0117968Google Scholar
Nichols, E. S., & Joanisse, M. F. (2016). Functional activity and white matter microstructure reveal the independent effects of age of acquisition and proficiency on second-language learning. NeuroImage, 143, 1525. https://doi.org/10.1016/j.neuroimage.2016.08.053Google Scholar
Olsen, R. K., Pangelinan, M. M., Bogulski, C. A., Chakravarty, M. M., Luk, G., Grady, C. L., & Bialystok, E. (2015). The effect of lifelong bilingualism on regional grey and white matter volume. Brain Research, 1612, 128139. https://doi.org/10.1016/j.brainres.2015.02.034Google Scholar
Osterhout, L., Poliakov, A., Inoue, K., McLaughlin, J., Valentine, G., Pitkanen, I., Frenck-Mestre, C., & Hirschensohn, J. (2008). Second-language learning and changes in the brain. Journal of Neurolinguistics, 21 (6), 509521. https://doi.org/10.1016/j.jneuroling.2008.01.001Google Scholar
Patenaude, B., Smith, S. M., Kennedy, D. N., & Jenkinson, M. (2011). A Bayesian model of shape and appearance for subcortical brain segmentation. NeuroImage, 56 (3), 907922. https://doi.org/10.1016/j.neuroimage.2011.02.046Google Scholar
Pliatsikas, C. (forthcoming, 2019). Multilingualism and brain plasticity. In Schweiter, J. W. (Ed.), The Handbook of the Neuroscience of Multilingualism (pp. 09). Wiley Blackwell.Google Scholar
Pliatsikas, C., & Chondrogianni, V. (2015). Editorial: Learning a non-native language in a naturalistic environment: insights from behavioral and neuroimaging research. Frontiers in Psychology, 6 (July), 13. https://doi.org/10.3389/fpsyg.2015.01009Google Scholar
Pliatsikas, C., DeLuca, V. F., Moschopoulou, E., & Saddy, J. D. (2017). Immersive bilingualism reshapes the core of the brain. Brain Structure and Function, 222 (4), 17851795. https://doi.org/10.1007/s00429-016-1307-9Google Scholar
Pliatsikas, C., Johnstone, T., & Marinis, T. (2014a). fMRI evidence for the involvement of the procedural memory system in morphological processing of a second language. PLoS ONE, 9 (5). https://doi.org/10.1371/journal.pone.0097298Google Scholar
Pliatsikas, C., Johnstone, T., & Marinis, T. (2014b). Grey matter volume in the cerebellum is related to the processing of grammatical rules in a second language: A structural voxel-based morphometry study. Cerebellum, 13 (1), 5563. https://doi.org/10.1007/s12311-013-0515-6Google Scholar
Pliatsikas, C., & Luk, G. (2016). Executive control in bilinguals: a concise review of fMRI studies. Bilingualism: Language and Cognition, 53 (9), 16891699. https://doi.org/10.1017/CBO9781107415324.004Google Scholar
Pliatsikas, C., Moschopoulou, E., & Saddy, J. D. (2015). The effects of bilingualism on the white matter structure of the brain. Proceedings of the National Academy of Sciences, 112 (5), 13341337. https://doi.org/10.1073/pnas.1414183112Google Scholar
Rossi, E., Cheng, H., Kroll, J. F., Diaz, M. T., & Newman, S. D. (2017). Changes in White-Matter Connectivity in Late Second Language Learners: Evidence from Diffusion Tensor Imaging. Frontiers in Psychology, 8 (November), 115. https://doi.org/10.3389/fpsyg.2017.02040Google Scholar
Rothman, J. (2008). Why all counter-evidence to the critical period hypothesis in second language acquisition is not equal or problematic. Language and Linguistics Compass, 2 (6), 10631088. https://doi.org/10.1111/j.1749-818X.2008.00098.xGoogle Scholar
Schumann, J. H. (1990). The role of the amygdala as a mediator of affect and cognition in second language acquisition. In Alatis, J. E. (Ed.), Georgetown University Round Table on Language and Linguistics (pp. 169176). Washington, DC: Georgetown University Press. Retrieved from https://repository.library.georgetown.edu/bitstream/handle/10822/555483/GURT_1990.pdf?sequence=1#page=179Google Scholar
Schumann, J. H. (2001). Appraisal psychology, neurobiology, and langauge. Annual Review of Applied Linguistics, 21, 2344. https://doi.org/https://doi.org/10.1017/S0267190501000022Google Scholar
Selinker, L. (1972). Interlanguage. International Review of Applied Linguistics, 10 (3), 209232.Google Scholar
Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C. E., Watkins, K. E., Ciccarelli, O., Cader, M. Z., Matthews, P. M., & Behrens, T. E. J. (2006). Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. NeuroImage, 31 (4), 14871505. https://doi.org/10.1016/j.neuroimage.2006.02.024Google Scholar
Smith, S. M., & Nichols, T. E. (2009). Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage, 44 (1), 8398. https://doi.org/10.1016/j.neuroimage.2008.03.061Google Scholar
Spivey, M. J., & Marian, V. (1999). Cross Talk Between Native and Second Languages: Partial Activation of an Irrelevant Lexicon. Psychological Science, 10 (3), 281284. https://doi.org/10.1111/1467-9280.00151Google Scholar
Stein, M., Federspiel, A., Koenig, T., Wirth, M., Strik, W., Wiest, R., Brandeis, D., & Dierks, T. (2012). Structural plasticity in the language system related to increased second language proficiency. Cortex, 48 (4), 458465. https://doi.org/10.1016/j.cortex.2010.10.007Google Scholar
Stein, M., Winkler, C., Kaiser, A. C., & Dierks, T. (2014). Structural brain changes related to bilingualism: Does immersion make a difference? Frontiers in Psychology, 5 (SEP), 17. https://doi.org/10.3389/fpsyg.2014.01116Google Scholar
Stocco, A., & Prat, C. S. (2014). Bilingualism trains specific brain circuits involved in flexible rule selection and application. Brain and Language, 137, 5061. https://doi.org/10.1016/j.bandl.2014.07.005Google Scholar
Stocco, A., Yamasaki, B. L., Natalenko, R., & Prat, C. S. (2014). Bilingual brain training:. A neurobiological framework of how bilingual experience improves executive function. International Journal of Bilingualism, 18 (1), 6792. https://doi.org/10.1177/1367006912456617Google Scholar
Thierry, G., & Wu, Y. J. (2007). Brain potentials reveal unconscious translation during foreign-language comprehension. Proceedings of the National Academy of Sciences, 104 (30), 1253012535. https://doi.org/10.1073/pnas.0609927104Google Scholar
Ullman, M. T. (2004). Contributions of memory circuits to language: The declarative/procedural model. Cognition, 92 (1–2), 231270. https://doi.org/10.1016/j.cognition.2003.10.008Google Scholar
Winkler, A. M., Ridgway, G. R., Webster, M. A., Smith, S. M., & Nichols, T. E. (2014). Permutation inference for the general linear model. NeuroImage, 92, 381397. https://doi.org/10.1016/j.neuroimage.2014.01.060Google Scholar
Wong, B., Yin, B., & Brien, B. O. (2016). Neurolinguistics:. Structure, Function, and Connectivity in the Bilingual Brain. BioMed Research International, 2016.Google Scholar