Bilingualism as a gradient measure modulates functional connectivity of language and control networks

There is currently no agreement on which factor modulates most effectively and enduringly brain plasticity in bilingual individuals. Grouping heterogeneous linguistic profiles under a dichotomous condition (bilingualism versus monolingualism) may obscure critical aspects of language experience underlying neural changes, thus leading to variable and often conflicting findings. In the present study, we overcome these limitations by analyzing the individual and joint contribution of L2 AoA, proficiency and usage - all measured as continuous variables - on the resting-state functional connectivity of the brain networks mediating the specific demands of bilingual language processing: the language network and the executive control network. Our results indicate that bilingual experience - defined as a continuous and multifaceted phenomenon - impacts brain plasticity by modulating the functional connectivity both within and between language and control networks. Each experience-related factor considered played a role in changing the connectivity of these regions. Moreover, the effect of AoA was modulated by proficiency and usage. These findings shed new light on the importance of modeling bilingualism as a gradient measure rather than an all-or-none phenomenon.

[1]  Xi-Nian Zuo,et al.  Individual Variability and Test-Retest Reliability Revealed by Ten Repeated Resting-State Brain Scans over One Month , 2015, PloS one.

[2]  Arturo E. Hernandez,et al.  The effect of age of acquisition, socioeducational status, and proficiency on the neural processing of second language speech sounds , 2015, Brain and Language.

[3]  Albert Costa,et al.  Language proficiency modulates the engagement of cognitive control areas in multilinguals , 2013, Cortex.

[4]  Ferath Kherif,et al.  The Role of the Left Head of Caudate in Suppressing Irrelevant Words , 2010, Journal of Cognitive Neuroscience.

[5]  Hiroyuki Oya,et al.  Sensory–motor networks involved in speech production and motor control: An fMRI study , 2015, NeuroImage.

[6]  E Capitani,et al.  Raven's coloured progressive matrices: normative values on 305 adult normal controls. , 1987, Functional neurology.

[7]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[8]  D. Poeppel,et al.  Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language , 2004, Cognition.

[9]  A. Friederici The brain basis of language processing: from structure to function. , 2011, Physiological reviews.

[10]  R. Harald Baayen,et al.  Statistics in Psycholinguistics: A critique of some current gold standards , 2004 .

[11]  J. Abutalebi,et al.  The relationship between bilingual experience and gyrification in adulthood: A cross-sectional surface-based morphometry study , 2019, Brain and Language.

[12]  Albert Costa,et al.  Neural basis of bilingual language control , 2018, Annals of the New York Academy of Sciences.

[13]  Daniel Rueckert,et al.  Human brain mapping: A systematic comparison of parcellation methods for the human cerebral cortex , 2017, NeuroImage.

[14]  Peter Q. Pfordresher,et al.  The somatotopy of speech: Phonation and articulation in the human motor cortex , 2009, Brain and Cognition.

[15]  N. Abrahamsson AGE OF ONSET AND NATIVELIKE L2 ULTIMATE ATTAINMENT OF MORPHOSYNTACTIC AND PHONETIC INTUITION , 2012, Studies in Second Language Acquisition.

[16]  D. Green,et al.  Neuroimaging of language control in bilinguals: neural adaptation and reserve , 2016 .

[17]  L. Colombo,et al.  Stima del quoziente intellettivo tramite l'applicazione del TIB (Test Breve di Intelligenza) , 2002 .

[18]  P. Skehan Individual Differences in Second Language Learning , 1989, Studies in Second Language Acquisition.

[19]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[20]  Debra Titone,et al.  Bilingual experience and resting-state brain connectivity: Impacts of L2 age of acquisition and social diversity of language use on control networks , 2018, Neuropsychologia.

[21]  Feng Liu,et al.  Decreased interhemispheric functional connectivity in insula and angular gyrus/supramarginal gyrus: Significant findings in first-episode, drug-naive somatization disorder , 2016, Psychiatry Research: Neuroimaging.

[22]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[23]  Michael T. Ullman Chapter 76 – The Declarative/Procedural Model: A Neurobiological Model of Language Learning, Knowledge, and Use , 2016 .

[24]  Chris Rorden,et al.  Temporal lobe networks supporting the comprehension of spoken words , 2017, Brain : a journal of neurology.

[25]  Ping Li,et al.  The emergence of competing modules in bilingualism , 2005, Trends in Cognitive Sciences.

[26]  D. Peng,et al.  Event-related potential evidence for parallel activation of two languages in bilingual speech production , 2006, Neuroreport.

[27]  C. Pliatsikas,et al.  The effects of bilingualism on the white matter structure of the brain , 2015, Proceedings of the National Academy of Sciences.

[28]  Meng Li,et al.  Onset age of L2 acquisition influences language network in early and late Cantonese-Mandarin bilinguals , 2017, Brain and Language.

[29]  Thomas Potter,et al.  Effects of Brain Parcellation on the Characterization of Topological Deterioration in Alzheimer's Disease , 2019, Front. Aging Neurosci..

[30]  Jubin Abutalebi,et al.  The neural basis of first and second language processing , 2005, Current Opinion in Neurobiology.

[31]  Magnus Lindgren,et al.  Growth of language-related brain areas after foreign language learning , 2012, NeuroImage.

[32]  Noelia Ventura-Campos,et al.  Bilingualism at the core of the brain. Structural differences between bilinguals and monolinguals revealed by subcortical shape analysis , 2016, NeuroImage.

[33]  Ping Li,et al.  Second language lexical development and cognitive control: A longitudinal fMRI study , 2015, Brain and Language.

[34]  G. Luk,et al.  Describing bilinguals: A systematic review of labels and descriptions used in the literature between 2005–2015 , 2017, Bilingualism: Language and Cognition.

[35]  X. Chai,et al.  Simultaneous learning of two languages from birth positively impacts intrinsic functional connectivity and cognitive control , 2017, Brain and Cognition.

[36]  Richard Taylor Interpretation of the Correlation Coefficient: A Basic Review , 1990 .

[37]  Albert Costa,et al.  Bilingualism tunes the anterior cingulate cortex for conflict monitoring. , 2012, Cerebral cortex.

[38]  Jubin Abutalebi,et al.  The impact of bilingualism on brain reserve and metabolic connectivity in Alzheimer's dementia , 2017, Proceedings of the National Academy of Sciences.

[39]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[40]  R. Turner,et al.  Language Control in the Bilingual Brain , 2006, Science.

[41]  Kevin Murphy,et al.  Towards a consensus regarding global signal regression for resting state functional connectivity MRI , 2017, NeuroImage.

[42]  Ping Li,et al.  Neural changes underlying successful second language word learning: An fMRI study , 2015, Journal of Neurolinguistics.

[43]  Jacob Cohen The Cost of Dichotomization , 1983 .

[44]  Albert Costa,et al.  How does the bilingual experience sculpt the brain? , 2014, Nature Reviews Neuroscience.

[45]  M. Silveri,et al.  The phonological short-term store-rehearsal system: Patterns of impairment and neural correlates , 1997, Neuropsychologia.

[46]  Brendan S. Weekes,et al.  Microstructural anatomical differences between bilinguals and monolinguals , 2017 .

[47]  Simone Sulpizio,et al.  Neuroplasticity across the lifespan and aging effects in bilinguals and monolinguals , 2018, Brain and Cognition.

[48]  Thomas E. Nichols,et al.  Functional connectomics from resting-state fMRI , 2013, Trends in Cognitive Sciences.

[49]  Albert Costa,et al.  The role of the left putamen in multilingual language production , 2013, Brain and Language.

[50]  Kate E. Watkins,et al.  Age of language learning shapes brain structure: A cortical thickness study of bilingual and monolingual individuals , 2014, Brain and Language.

[51]  Peter Hagoort,et al.  The neurobiology of language beyond single-word processing , 2019, Science.

[52]  E. M. Individual differences in second language learning , 2019 .

[53]  Michael J. Spivey,et al.  Bilingual and monolingual processing of competing lexical items , 2003, Applied Psycholinguistics.

[54]  M. Czisch,et al.  Increased sleep pressure reduces resting state functional connectivity , 2010, Magnetic Resonance Materials in Physics, Biology and Medicine.

[55]  R. Stefan Greulich,et al.  Language control in bilinguals: Intention to speak vs. execution of speech , 2015, Brain and Language.

[56]  A. Sanjuán,et al.  Neural bases of language switching in high and early proficient bilinguals , 2011, Brain and Language.

[57]  Takashi Hanakawa,et al.  Dynamic Neural Network Reorganization Associated with Second Language Vocabulary Acquisition: A Multimodal Imaging Study , 2013, The Journal of Neuroscience.

[58]  Richard S. J. Frackowiak,et al.  Neurolinguistics: Structural plasticity in the bilingual brain , 2004, Nature.

[59]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[60]  Michael S. C. Thomas,et al.  The Right Posterior Paravermis and the Control of Language Interference , 2011, Journal of Neuroscience.

[61]  A. Rodríguez-Fornells,et al.  Self-Assessment of Individual Differences in Language Switching , 2012, Front. Psychology.

[62]  T. Bak The impact of bilinguism on cognitive aging and dementia , 2015 .

[63]  Amanda V. Utevsky,et al.  Precuneus Is a Functional Core of the Default-Mode Network , 2014, The Journal of Neuroscience.

[64]  F. Craik,et al.  Lifelong Bilingualism Maintains White Matter Integrity in Older Adults , 2011, The Journal of Neuroscience.

[65]  Huafu Chen,et al.  Altered regional activity and inter-regional functional connectivity in psychogenic non-epileptic seizures , 2015, Scientific Reports.

[66]  Jason Rothman,et al.  Redefining bilingualism as a spectrum of experiences that differentially affects brain structure and function , 2019, Proceedings of the National Academy of Sciences.

[67]  D. Green,et al.  Lemma selection without inhibition of languages in bilingual speakers , 1998, Bilingualism: Language and Cognition.

[68]  Albert Costa,et al.  Are you really cursing? Neural processing of taboo words in native and foreign language , 2019, Brain and Language.

[69]  Viljami Sairanen,et al.  Bilingualism modulates the white matter structure of language-related pathways , 2017, NeuroImage.

[70]  Francesca M. Branzi,et al.  On the overlap between bilingual language control and domain-general executive control. , 2016, Acta Psychologica.

[71]  G. Ding,et al.  Bilingualism alters brain functional connectivity between “control” regions and “language” regions: Evidence from bimodal bilinguals , 2015, Neuropsychologia.

[72]  Denise Klein,et al.  Effects of Early and Late Bilingualism on Resting-State Functional Connectivity , 2016, The Journal of Neuroscience.

[73]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[74]  Susan L. Whitfield-Gabrieli,et al.  Conn: A Functional Connectivity Toolbox for Correlated and Anticorrelated Brain Networks , 2012, Brain Connect..

[75]  Thomas T. Liu,et al.  Anti-correlated networks, global signal regression, and the effects of caffeine in resting-state functional MRI , 2012, NeuroImage.

[76]  K. Hakuta,et al.  Degree of bilingualism modifies executive control in Hispanic children in the USA , 2018, International journal of bilingual education and bilingualism.