Hostname: page-component-f554764f5-nwwvg Total loading time: 0 Render date: 2025-04-22T02:41:50.581Z Has data issue: false hasContentIssue false
  • English
  • Français

Neuroplasticity and cognitive reserve effects in the Caudate Nucleus of young bilingual adults

Published online by Cambridge University Press:  23 June 2023

Federico Gallo Open the ORCID record for Federico Gallo [Opens in a new window] ,
Liliia Terekhina ,
Yury Shtyrov  and
Andriy Myachykov
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
Liliia Terekhina
Affiliation:
Centre for Cognition and Decision Making, Institute for Cognitive Neuroscience, National Research University Higher School of Economics, Moscow, Russian Federation
Yury Shtyrov
Affiliation:
Center of Functionally Integrative Neuroscience, Aarhus University, Aarhus, Denmark
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
*
Corresponding Author: Dr Federico Gallo Centre for Cognition and Decision Making, Institute for Cognitive Neuroscience, National Research University Higher School of Economics Krivokolenniy Pereulok, 3, Entrance 2, Moscow, Russian Federation E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

This study investigates bilingualism-induced neuroplastic and cognitive-reserve effects in the Caudate Nucleus (CN), a structure believed to support both bilingual language control and domain-general executive functioning. We computed a generalized bilingualism index incorporating several dimensions of bilingual experience in a sample of bilingual young adults and tested whether this index would predict behavioral executive performance (measured using a Flanker task) and volumetric differences in the CN. Moreover, we investigated whether bilingualism mitigates the relationship between CN volume and executive performance, a sign of cognitive reserve. Our results indicate that bilingualism facilitates executive performance and induces an inverted U-shaped neuroplastic trajectory in bilateral CN, consistently with the view that structural increases are replaced by functional improvements as bilingual experience progresses. The emergence of bilingualism-induced cognitive reserve effects in CN further supports the view that bilinguals rely progressively less on the availability of structural resources in the face of increased functional efficiency.

Keywords

bilingual experiencecaudate nucleusexecutive functionsstructural MRIcognitive reserveFlanker task
Type
Research Article
Information
Bilingualism: Language and Cognition , Volume 27 , Issue 1 , January 2024 , pp. 107 - 116
Check for updates
Copyright
Copyright © The Author(s), 2023. 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.)

Article purchase

Temporarily unavailable

References

Abutalebi, J., & Green, D. (2007). Bilingual language production: The neurocognition of language representation and control. Journal of Neurolinguistics, 20(3), 242–275. https://doi.org/10.1016/j.jneuroling.2006.10.003CrossRefGoogle Scholar
Abutalebi, J., & Green, D. W. (2016). Neuroimaging of language control in bilinguals: Neural adaptation and reserve. Bilingualism, 19(4), 689–698. https://doi.org/10.1017/S1366728916000225CrossRefGoogle Scholar
Abutalebi, J., Della Rosa, P. A., Ding, G., Weekes, B., Costa, A., & Green, D. W. (2013). Language proficiency modulates the engagement of cognitive control areas in multilinguals. Cortex, 49(3), 905–911. https://doi.org/https://doi.org/10.1016/j.cortex.2012.08.018CrossRefGoogle ScholarPubMed
Anderson, J. C., & Gerbing, D. W. (1988). Structural equation modeling in practice: A review and recommended two-step approach. Psychological Bulletin, 103(3), 411.CrossRefGoogle Scholar
Baayen, R. H., & Milin, P. (2010). Analyzing reaction times. International Journal of Psychological Research, 3(2), 12–28.CrossRefGoogle Scholar
Badgaiyan, R. D., & Wack, D. (2011). Evidence of Dopaminergic Processing of Executive Inhibition. PLOS ONE, 6(12), e28075. https://doi.org/10.1371/journal.pone.0028075CrossRefGoogle ScholarPubMed
Beatty-Martínez, A. L., Navarro-Torres, C. A., Dussias, P. E., Bajo, M. T., Guzzardo Tamargo, R. E., & Kroll, J. F. (2020). Interactional context mediates the consequences of bilingualism for language and cognition. In Journal of Experimental Psychology: Learning, Memory, and Cognition (Vol. 46, pp. 1022–1047). American Psychological Association. https://doi.org/10.1037/xlm0000770Google Scholar
Bialystok, E. (2017). The bilingual adaptation: How minds accommodate experience. Psychological Bulletin, 143(3), 233–262. https://doi.org/10.1037/bul0000099CrossRefGoogle ScholarPubMed
Bialystok, E., & Craik, F. I. M. (2022). How does bilingualism modify cognitive function? Attention to the mechanism. Psychonomic Bulletin & Review, 29(4), 1246–1269. https://doi.org/10.3758/s13423-022-02057-5CrossRefGoogle ScholarPubMed
Bialystok, E., Craik, F. I. M., & Luk, G. (2012). Bilingualism: consequences for mind and brain. Trends in Cognitive Sciences, 16(4), 240–250. https://doi.org/https://doi.org/10.1016/j.tics.2012.03.001CrossRefGoogle ScholarPubMed
Boekel, W., Wagenmakers, E.-J., Belay, L., Verhagen, J., Brown, S., & Forstmann, B. U. (2015). A purely confirmatory replication study of structural brain-behavior correlations. Cortex, 66, 115–133. https://doi.org/https://doi.org/10.1016/j.cortex.2014.11.019CrossRefGoogle ScholarPubMed
Branzi, F. M., Della Rosa, P. A., Canini, M., Costa, A., & Abutalebi, J. (2016). Language Control in Bilinguals: Monitoring and Response Selection. Cerebral Cortex, 26(6), 2367–2380. https://doi.org/10.1093/cercor/bhv052CrossRefGoogle ScholarPubMed
Burgaleta, M., Sanjuán, A., Ventura-Campos, N., Sebastian-Galles, N., & Ávila, C. (2016). Bilingualism at the core of the brain. Structural differences between bilinguals and monolinguals revealed by subcortical shape analysis. NeuroImage, 125, 437–445.Google ScholarPubMed
Cools, R., & D'Esposito, M. (2011). Inverted-U–Shaped Dopamine Actions on Human Working Memory and Cognitive Control. Biological Psychiatry, 69(12), e113–e125. https://doi.org/https://doi.org/10.1016/j.biopsych.2011.03.028CrossRefGoogle ScholarPubMed
Court, J. H., & Raven, J. (1992). Raven manual: Section 3. The standard progressive matrices. Oxford: Oxford Psychologists Press.Google Scholar
Dahnke, R., Ziegler, G., & Gaser, C. (2012). Local adaptive segmentation. Beijing. HBM. Available Online at: http://Dbm.Neuro.Uni-Jena.de/HBM2012/HBM2012-Dahnke02.Pdf.Google Scholar
Del Maschio, N., Sulpizio, S., Gallo, F., Fedeli, D., Weekes, B. S., & Abutalebi, J. (2018). Neuroplasticity across the lifespan and aging effects in bilinguals and monolinguals. Brain and Cognition, 125. https://doi.org/10.1016/j.bandc.2018.06.007CrossRefGoogle ScholarPubMed
DeLuca, V., Rothman, J., Bialystok, E., & Pliatsikas, C. (2019a). Redefining bilingualism as a spectrum of experiences that differentially affects brain structure and function. Proceedings of the National Academy of Sciences, 116(15), 7565 LP –7574. https://doi.org/10.1073/pnas.1811513116CrossRefGoogle ScholarPubMed
DeLuca, V., Rothman, J., & Pliatsikas, C. (2019b). Linguistic immersion and structural effects on the bilingual brain: a longitudinal study. Bilingualism: Language and Cognition, 22(5), 1160–1175. https://doi.org/DOI: 10.1017/S1366728918000883CrossRefGoogle Scholar
Dyer, S. M., Harrison, S. L., Laver, K., Whitehead, C., & Crotty, M. (2018). An overview of systematic reviews of pharmacological and non-pharmacological interventions for the treatment of behavioral and psychological symptoms of dementia. International Psychogeriatrics, 30(3), 295–309. https://doi.org/10.1017/S1041610217002344CrossRefGoogle ScholarPubMed
ESS Round 10: European Social Survey Round 10 Data. (2020). Data file edition 1.2. Sikt - Norwegian Agency for Shared Services in Education and Research, Norway – Data Archive and distributor of ESS data for ESS ERIC. https://doi.org/10.21338/NSD-ESS10-2020.Google Scholar
Fan, J., McCandliss, B. D., Sommer, T., Raz, A., & Posner, M. I. (2002). Testing the Efficiency and Independence of Attentional Networks. Journal of Cognitive Neuroscience, 14(3), 340–347. https://doi.org/10.1162/089892902317361886CrossRefGoogle ScholarPubMed
Gallo, F., Kalpouzos, G., Laukka, E. J., Wang, R., Qiu, C., Bäckman, L., Marseglia, A., Fratiglioni, L., & Dekhtyar, S. (2021a). Cognitive Trajectories and Dementia Risk: A Comparison of Two Cognitive Reserve Measures. In Frontiers in Aging Neuroscience (Vol. 13, p. 540). https://www.frontiersin.org/article/10.3389/fnagi.2021.737736CrossRefGoogle Scholar
Gallo, F., Novitskiy, N., Myachykov, A., & Shtyrov, Y. (2021b). Individual differences in bilingual experience modulate executive control network and performance: behavioral and structural neuroimaging evidence. Bilingualism: Language and Cognition, 24(2), 293–304. https://doi.org/DOI:10.1017/S1366728920000486CrossRefGoogle Scholar
Grahn, J. A., Parkinson, J. A., & Owen, A. M. (2008). The cognitive functions of the caudate nucleus. Progress in Neurobiology, 86(3), 141–155. https://doi.org/https://doi.org/10.1016/j.pneurobio.2008.09.004CrossRefGoogle ScholarPubMed
Green, D. W., & Abutalebi, J. (2013). Language control in bilinguals: The adaptive control hypothesis. Journal of Cognitive Psychology, 25(5), 515–530. https://doi.org/10.1080/20445911.2013.796377CrossRefGoogle ScholarPubMed
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, 1396(1), 183–201. https://doi.org/10.1111/nyas.13333CrossRefGoogle ScholarPubMed
Gullifer, J. W., & Titone, D. (2020). Characterizing the social diversity of bilingualism using language entropy. Bilingualism: Language and Cognition, 23(2), 283–294. https://doi.org/DOI:10.1017/S1366728919000026CrossRefGoogle Scholar
Hervais-Adelman, A., Moser-Mercer, B., Michel, C. M., & Golestani, N. (2015). fMRI of Simultaneous Interpretation Reveals the Neural Basis of Extreme Language Control. Cerebral Cortex, 25(12), 4727–4739. https://doi.org/10.1093/cercor/bhu158CrossRefGoogle ScholarPubMed
Hilchey, M. D., & Klein, R. M. (2011). Are there bilingual advantages on nonlinguistic interference tasks? Implications for the plasticity of executive control processes. Psychonomic Bulletin & Review, 18(4), 625–658. https://doi.org/10.3758/s13423-011-0116-7CrossRefGoogle ScholarPubMed
Hooper, B., Faria, L. O., Fortes, L. de S., Wanner, S. P., & Albuquerque, M. R. (2022). Development and reliability of a test for assessing executive functions during exercise. Applied Neuropsychology: Adult, 29(4), 750–760. https://doi.org/10.1080/23279095.2020.1807984CrossRefGoogle ScholarPubMed
Kaushanskaya, M., & Marian, V. (2007). Bilingual language processing and interference in bilinguals: Evidence from eye tracking and picture naming. Language Learning, 57, 119–163.CrossRefGoogle Scholar
Kontis, V., Bennett, J. E., Mathers, C. D., Li, G., Foreman, K., & Ezzati, M. (2017). Future life expectancy in 35 industrialised countries: projections with a Bayesian model ensemble. The Lancet, 389(10076), 1323–1335. https://doi.org/10.1016/S0140-6736(16)32381-9CrossRefGoogle ScholarPubMed
Korenar, M., Treffers-Daller, J., & Pliatsikas, C. (2023). Dynamic effects of bilingualism on brain structure map onto general principles of experience-based neuroplasticity. Scientific Reports, 13(1), 3428. https://doi.org/10.1038/s41598-023-30326-3CrossRefGoogle ScholarPubMed
Kroll, J. F., Bobb, S. C., & Hoshino, N. (2014). Two Languages in Mind: Bilingualism as a Tool to Investigate Language, Cognition, and the Brain. Current Directions in Psychological Science, 23(3), 159–163. https://doi.org/10.1177/0963721414528511CrossRefGoogle ScholarPubMed
Kroll, J. F., Dussias, P. E., Bice, K., & Perrotti, L. (2015). Bilingualism, Mind, and Brain. Annual Review of Linguistics, 1, 377–394. https://doi.org/10.1146/annurev-linguist-030514-124937CrossRefGoogle ScholarPubMed
Lehtonen, M. H., Laine, M., Niemi, J., Thomsen, T., Vorobyev, V. A., & Hugdahl, K. (2005). Brain correlates of sentence translation in Finnish–Norwegian bilinguals. NeuroReport, 16(6). https://journals.lww.com/neuroreport/Fulltext/2005/04250/Brain_correlates_of_sentence_translation_in.18.aspxCrossRefGoogle ScholarPubMed
Li, X., Ng, K. K., Wong, J. J. Y., Lee, J. W., Zhou, J. H., & Yow, W. Q. (2021). Bilingual language entropy influences executive functions through functional connectivity and signal variability. Brain and Language, 222, 105026. https://doi.org/https://doi.org/10.1016/j.bandl.2021.105026CrossRefGoogle ScholarPubMed
Lövdén, M., Wenger, E., Mårtensson, J., Lindenberger, U., & Bäckman, L. (2013). Structural brain plasticity in adult learning and development. Neuroscience & Biobehavioral Reviews, 37(9, Part B), 2296–2310. https://doi.org/https://doi.org/10.1016/j.neubiorev.2013.02.014CrossRefGoogle ScholarPubMed
Ma, H., Hu, J., Xi, J., Shen, W., Ge, J., Geng, F., Wu, Y., Guo, J., & Yao, D. (2014). Bilingual Cognitive Control in Language Switching: An fMRI Study of English-Chinese Late Bilinguals. PLOS ONE, 9(9), e106468. https://doi.org/10.1371/journal.pone.0106468CrossRefGoogle ScholarPubMed
MacArthur Foundation. (2007). The MacArthur Research Network on Socioeconomic Status and Health. https://macses.ucsf.edu/research/psychosocial/subjective.php#measurementGoogle Scholar
Macfarlane, M. D., Looi, J. C. L., Walterfang, M., Spulber, G., Velakoulis, D., Crisby, M., Örndahl, E., Erkinjuntti, T., Garde, E., Waldemar, G., Wallin, A., & Wahlund, L.-O. (2013). Executive dysfunction correlates with caudate nucleus atrophy in patients with white matter changes on MRI: A subset of LADIS. Psychiatry Research: Neuroimaging, 214(1), 16–23. https://doi.org/https://doi.org/10.1016/j.pscychresns.2013.05.010CrossRefGoogle ScholarPubMed
Manjón, J. V., Coupé, P., Martí-Bonmatí, L., Collins, D. L., & Robles, M. (2010). Adaptive non-local means denoising of MR images with spatially varying noise levels. Journal of Magnetic Resonance Imaging, 31(1), 192–203. https://doi.org/https://doi.org/10.1002/jmri.22003CrossRefGoogle ScholarPubMed
Marian, V., Blumenfeld, H. K., & 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, 50(4), 940–967. https://doi.org/10.1044/1092-4388(2007/067)CrossRefGoogle ScholarPubMed
Marin-Marin, L., Costumero, V., Ávila, C., & Pliatsikas, C. (2022). Dynamic Effects of Immersive Bilingualism on Cortical and Subcortical Grey Matter Volumes. In Frontiers in Psychology (Vol. 13). https://www.frontiersin.org/articles/10.3389/fpsyg.2022.886222CrossRefGoogle ScholarPubMed
McMorris, T., & Hale, B. J. (2012). Differential effects of differing intensities of acute exercise on speed and accuracy of cognition: A meta-analytical investigation. Brain and Cognition, 80(3), 338–351. https://doi.org/https://doi.org/10.1016/j.bandc.2012.09.001CrossRefGoogle ScholarPubMed
Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9(1), 97–113. https://doi.org/https://doi.org/10.1016/0028-3932(71)90067-4CrossRefGoogle ScholarPubMed
Paap, K. R., & Sawi, O. (2014). Bilingual advantages in executive functioning: problems in convergent validity, discriminant validity, and the identification of the theoretical constructs. In Frontiers in Psychology (Vol. 5). https://www.frontiersin.org/articles/10.3389/fpsyg.2014.00962CrossRefGoogle ScholarPubMed
Pliatsikas, C. (2020). Understanding structural plasticity in the bilingual brain: The Dynamic Restructuring Model. Bilingualism: Language and Cognition, 23(2), 459–471. https://doi.org/DOI:10.1017/S1366728919000130CrossRefGoogle Scholar
Pliatsikas, C., DeLuca, V., Moschopoulou, E., & Saddy, J. D. (2017). Immersive bilingualism reshapes the core of the brain. Brain Structure and Function, 222(4), 1785–1795. https://doi.org/10.1007/s00429-016-1307-9CrossRefGoogle ScholarPubMed
Prince, M. J., Comas-Herrera, A., Knapp, M., Guerchet, M. M., & Karagiannidou, M. (2016). World Alzheimer Report 2016 - Improving healthcare for people living with dementia: Coverage, quality and costs now and in the future. Alzheimer's Disease International. https://www.alz.co.uk/research/world-report-2016Google Scholar
Rajapakse, J. C., Giedd, J. N., & Rapoport, J. L. (1997). Statistical approach to segmentation of single-channel cerebral MR images. IEEE Transactions on Medical Imaging, 16(2), 176–186. https://doi.org/10.1109/42.563663CrossRefGoogle ScholarPubMed
Reed, B. R., Mungas, D., Farias, S. T., Harvey, D., Beckett, L., Widaman, K., Hinton, L., & DeCarli, C. (2010). Measuring cognitive reserve based on the decomposition of episodic memory variance. Brain, 133(8), 2196–2209. https://doi.org/10.1093/brain/awq154CrossRefGoogle ScholarPubMed
Sideridis, G., Simos, P., Papanicolaou, A., & Fletcher, J. (2014). Using Structural Equation Modeling to Assess Functional Connectivity in the Brain: Power and Sample Size Considerations. Educational and Psychological Measurement, 74(5), 733–758. https://doi.org/10.1177/0013164414525397CrossRefGoogle ScholarPubMed
StataCorp. (2021). Stata Statistical Software: Release 17. College Station, TX: StataCorp LLC.Google Scholar
Stern, Y. (2009). Cognitive reserve. Neuropsychologia, 47(10), 2015–2028. https://doi.org/10.1016/j.neuropsychologia.2009.03.004CrossRefGoogle ScholarPubMed
Stern, Y., Arenaza-Urquijo, E. M., Bartrés-Faz, D., Belleville, S., Cantilon, M., Chetelat, G., Ewers, M., Franzmeier, N., Kempermann, G., Kremen, W. S., Okonkwo, O., Scarmeas, N., Soldan, A., Udeh-Momoh, C., Valenzuela, M., Vemuri, P., & Vuoksimaa, E. (2020). Whitepaper: Defining and investigating cognitive reserve, brain reserve, and brain maintenance. Alzheimer's & Dementia, 16(9), 1305–1311. https://doi.org/10.1016/j.jalz.2018.07.219CrossRefGoogle ScholarPubMed
Tohka, J., Zijdenbos, A., & Evans, A. (2004). Fast and robust parameter estimation for statistical partial volume models in brain MRI. NeuroImage, 23(1), 84–97. https://doi.org/https://doi.org/10.1016/j.neuroimage.2004.05.007CrossRefGoogle ScholarPubMed
Tucker, A. M., & Stern, Y. (2011). Cognitive reserve in aging. Current Alzheimer Research, 8(4), 354–360. https://doi.org/10.2174/156720511795745320CrossRefGoogle ScholarPubMed
van Heuven, W. J. B., Mandera, P., Keuleers, E., & Brysbaert, M. (2014). Subtlex-UK: A New and Improved Word Frequency Database for British English. Quarterly Journal of Experimental Psychology, 67(6), 1176–1190. https://doi.org/10.1080/17470218.2013.850521CrossRefGoogle ScholarPubMed
Wang, Y. A., & Rhemtulla, M. (2021). Power Analysis for Parameter Estimation in Structural Equation Modeling: A Discussion and Tutorial. Advances in Methods and Practices in Psychological Science, 4(1), 2515245920918253. https://doi.org/10.1177/2515245920918253CrossRefGoogle Scholar
Wimo, A., Guerchet, M., Ali, G.-C., Wu, Y.-T., Prina, A. M., Winblad, B., Jönsson, L., Liu, Z., & Prince, M. (2017). The worldwide costs of dementia 2015 and comparisons with 2010. Alzheimer's & Dementia: The Journal of the Alzheimer's Association, 13(1), 1–7. https://doi.org/10.1016/j.jalz.2016.07.150CrossRefGoogle ScholarPubMed
Zahodne, L. B., Manly, J. J., Brickman, A. M., Siedlecki, K. L., Decarli, C., & Stern, Y. (2013). Quantifying cognitive reserve in older adults by decomposing episodic memory variance: Replication and extension. Journal of the International Neuropsychological Society, 19(8), 854–862. https://doi.org/10.1017/S1355617713000738CrossRefGoogle ScholarPubMed
Zou, L., Ding, G., Abutalebi, J., Shu, H., & Peng, D. (2012). Structural plasticity of the left caudate in bimodal bilinguals. Cortex, 48(9), 1197–1206. https://doi.org/10.1016/j.cortex.2011.05.022CrossRefGoogle ScholarPubMed
Supplementary material: File

Gallo et al. supplementary material
Download undefined(File)
File 94.7 KB