Hostname: page-component-848d4c4894-pftt2 Total loading time: 0 Render date: 2024-05-16T21:16:10.531Z Has data issue: false hasContentIssue false

Enhancement of posterior brain functional networks in bilingual older adults

Published online by Cambridge University Press:  26 April 2019

Jaisalmer de Frutos-Lucas*
Affiliation:
Biological and Health Psychology Department, Universidad Autonoma de Madrid, 28049, Spain Laboratory of Cognitive and Computational Neuroscience, Center for Biomedical Technology, 28223, Spain
David López-Sanz
Affiliation:
Laboratory of Cognitive and Computational Neuroscience, Center for Biomedical Technology, 28223, Spain Department of Experimental Psychology, Universidad Complutense de Madrid, 28223, Spain
Pablo Cuesta
Affiliation:
Laboratory of Cognitive and Computational Neuroscience, Center for Biomedical Technology, 28223, Spain Electrical Engineering and Bioengineering Lab. Department of Industrial Engineering, University of La Laguna, Tenerife, 38206, Spain
Ricardo Bruña
Affiliation:
Laboratory of Cognitive and Computational Neuroscience, Center for Biomedical Technology, 28223, Spain Department of Experimental Psychology, Universidad Complutense de Madrid, 28223, Spain CIBER-BBN: Networking Research Center on Bioengineering, Biomaterials and Nanomedicine, 50018, Spain
Sofía de la Fuente
Affiliation:
Edinburgh Medical School: Usher Institute of Population Health Sciences & Informatics. The University of Edinburgh, EH8 9AG, Scotland, United Kingdom
Noelia Serrano
Affiliation:
Laboratory of Cognitive and Computational Neuroscience, Center for Biomedical Technology, 28223, Spain Department of Experimental Psychology, Universidad Complutense de Madrid, 28223, Spain
María Eugenia López
Affiliation:
Laboratory of Cognitive and Computational Neuroscience, Center for Biomedical Technology, 28223, Spain Department of Experimental Psychology, Universidad Complutense de Madrid, 28223, Spain
María Luisa Delgado-Losada
Affiliation:
Department of Experimental Psychology, Universidad Complutense de Madrid, 28223, Spain
Ramón López-Higes
Affiliation:
Department of Experimental Psychology, Universidad Complutense de Madrid, 28223, Spain
Alberto Marcos
Affiliation:
Neurology Department, Hospital Clinico San Carlos, 28040, Spain
Fernando Maestú
Affiliation:
Laboratory of Cognitive and Computational Neuroscience, Center for Biomedical Technology, 28223, Spain Department of Experimental Psychology, Universidad Complutense de Madrid, 28223, Spain
*
Address for correspondence: Jaisalmer de Frutos-Lucas, E-mail: jaisalmer.defrutos@ctb.upm.es

Abstract

Bilingualism has been said to improve cognition and even delay the onset of Alzheimer's disease (AD). This research aimed to investigate whether bilingualism leaves a neurophysiological trace even when people are highly educated. We expected bilinguals to present better preserved brain functional networks, which could be a trace of higher cognitive reserve. With this purpose, we conducted a magnetoencephalographic study with a group of healthy older adults. We estimated functional connectivity using phase-locking value and found five clusters in parieto-occipital regions in which bilinguals exhibited greater functional connectivity than monolinguals. These clusters included brain regions typically implicated in language processing. Furthermore, these functional changes correlated with caudate volumes (a key region in language shifting and control) in the bilingual sample. Interestingly, decreased Functional Connectivity between posterior brain regions had already been identified as an indicator of aging/preclinical AD but, according to our study, bilingualism seems to exert the opposite effect.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2019

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

Equal contributors.

References

Abutalebi, J, Annoni, JM, Zimine, I, Pegna, AJ, Seghier, ML, Lee-Jahnke, H, Lazeyras, F, Cappa, SF and Khateb, A (2008) Language control and lexical competition in bilinguals: An event-related fMRI study. Cerebral Cortex 18(7), 14961505. https://doi.org/10.1093/cercor/bhm182CrossRefGoogle Scholar
Abutalebi, J, Brambati, SM, Annoni, J-M, Moro, A, Cappa, SF and Perani, D (2007) The Neural Cost of the Auditory Perception of Language Switches: An Event-Related Functional Magnetic Resonance Imaging Study in Bilinguals. Journal of Neuroscience 27(50), 1376213769. https://doi.org/10.1523/JNEUROSCI.3294-07.2007CrossRefGoogle 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(9), 21262133. https://doi.org/10.1016/j.neurobiolaging.2014.03.010CrossRefGoogle Scholar
Abutalebi, J and Green, DW (2016) Neuroimaging of language control in bilinguals: Neural adaptation and reserve. Bilingualism 19(4), 689698. https://doi.org/10.1017/S1366728916000225CrossRefGoogle Scholar
Adesope, OO, Lavin, T, Thompson, T and Ungerleider, C (2010) A Systematic Review and Meta-Analysis of the Cognitive Correlates of Bilingualism. Review of Educational Research 80(2), 207245. https://doi.org/10.3102/0034654310368803CrossRefGoogle Scholar
Alladi, S, Bak, TH, Duggirala, V, Surampudi, B, Shailaja, M, Shukla, AK, Chaudhuri, JR and Kaul, S (2013) Bilingualism delays age at onset of dementia, independent of education and immigration status. Neurology 81(22), 19381944. https://doi.org/10.1212/01.wnl.0000436609.20587.65CrossRefGoogle ScholarPubMed
Anderson, JAE, Grundy, JG, De Frutos, J, Barker, RM, Grady, C and Bialystok, E (2018) Effects of bilingualism on white matter integrity in older adults. NeuroImage 167 (November 2017), 143150. https://doi.org/10.1016/j.neuroimage.2017.11.038CrossRefGoogle ScholarPubMed
Andrews-hanna, JR, Snyder, AZ, Vincent, JL, Lustig, C, Head, D, Raichle, ME and Buckner, RL (2009) Disruption of Large-Scale Brain Systems in Advanced Aging. Neuron 56(5), 924935. https://doi.org/10.1016/j.neuron.2007.10.038.DisruptionCrossRefGoogle Scholar
Ansaldo, AI, Ghazi-Saidi, L and Adrover-Roig, D (2015) Interference control in elderly bilinguals: Appearances can be misleading. Journal of Clinical and Experimental Neuropsychology 37(5), 455470. https://doi.org/10.1080/13803395.2014.990359CrossRefGoogle ScholarPubMed
Arenaza-Urquijo, EM, Landeau, B, La Joie, R, Mevel, K, Mézenge, F, Perrotin, A, Desgranges, B, Bartrés-Faz, D and Chételat, G (2013) Relationships between years of education and gray matter volume, metabolism and functional connectivity in healthy elders. NeuroImage 83, 450457. https://doi.org/10.1016/j.neuroimage.2013.06.053CrossRefGoogle ScholarPubMed
Bak, TH, Nissan, JJ, Allerhand, MM and Deary, IJ (2014) Does bilingualism influence cognitive aging? Annals of Neurology 75(6), 959963. https://doi.org/10.1002/ana.24158CrossRefGoogle ScholarPubMed
Bastin, C, Yakushev, I, Bahri, MA, Fellgiebel, A, Eustache, F, Landeau, B, Scheurich, A, Feyers, D, Collette, F, Chételat, G and Salmon, E (2012) Cognitive reserve impacts on inter-individual variability in resting-state cerebral metabolism in normal aging. NeuroImage 63(2), 713722. https://doi.org/10.1016/j.neuroimage.2012.06.074CrossRefGoogle ScholarPubMed
Berken, JA, Chai, X, Chen, J-K, Gracco, VL and 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.1960-15.2016CrossRefGoogle ScholarPubMed
Berroir, P, Ghazi-Saidi, L, Dash, T, Adrover-Roig, D, Benali, H and Ansaldo, AI (2017) Interference control at the response level: Functional networks reveal higher efficiency in the bilingual brain. Journal of Neurolinguistics 43, 416. https://doi.org/10.1016/j.jneuroling.2016.09.007CrossRefGoogle Scholar
Bialystok, E (2017) The bilingual adaptation: How minds accommodate experience. Psychological Bulletin 143(3), 233262. https://doi.org/10.1037/bul0000099CrossRefGoogle ScholarPubMed
Bialystok, E, Craik, FIM and Freedman, M (2007) Bilingualism as a protection against the onset of symptoms of dementia. Neuropsychologia 45(2), 459464. https://doi.org/10.1016/j.neuropsychologia.2006.10.009CrossRefGoogle ScholarPubMed
Calvo, A and Bialystok, E (2014) Independent effects of bilingualism and socioeconomic status on language ability and executive functioning. Cognition 130(3), 278288. https://doi.org/10.1016/j.cognition.2013.11.015CrossRefGoogle ScholarPubMed
Chai, XJ, Berken, JA, Barbeau, EB, Soles, J, Callahan, M, Chen, J-K and Klein, D (2016) Intrinsic Functional Connectivity in the Adult Brain and Success in Second-Language Learning. Journal of Neuroscience 36(3), 755761. https://doi.org/10.1523/JNEUROSCI.2234-15.2016CrossRefGoogle ScholarPubMed
Correia, JM, Jansma, B, Hausfeld, L, Kikkert, S and Bonte, M (2015) EEG decoding of spoken words in bilingual listeners: From words to language invariant semantic-conceptual representations. Frontiers in Psychology 6(FEB), 110. https://doi.org/10.3389/fpsyg.2015.00071CrossRefGoogle ScholarPubMed
Costa, A, Hernández, M and Sebastián-Gallés, N (2008) Bilingualism aids conflict resolution: Evidence from the ANT task. Cognition 106(1), 5986. https://doi.org/10.1016/j.cognition.2006.12.013CrossRefGoogle ScholarPubMed
Cox, SR, Bak, TH, Allerhand, M, Redmond, P, Starr, JM, Deary, IJ and MacPherson, SE (2016) Bilingualism, social cognition and executive functions: A tale of chickens and eggs. Neuropsychologia 91, 299306. https://doi.org/10.1016/j.neuropsychologia.2016.08.029CrossRefGoogle ScholarPubMed
Craik, FIM, Bialystok, E and Freedman, M (2010) Delaying the onset of Alzheimer disease: Bilingualism as a form of cognitive reserve. Neurology 75(19), 17261729. https://doi.org/10.1212/WNL.0b013e3181fc2a1cCrossRefGoogle ScholarPubMed
Crane, PK, Gruhl, JC, Erosheva, EA, Gibbons, LE, McCurry, SM, Rhoads, K, Rhoads, K, Nguyen, V, Arani, K, Masaki, K and White, L (2010) Use of spoken and written Japanese did not protect Japanese-American men from cognitive decline in late life. Journals of Gerontology - Series B Psychological Sciences and Social Sciences 65 B(6), 654666. https://doi.org/10.1093/geronb/gbq046CrossRefGoogle Scholar
Cuesta, P, Garcés, P, Castellanos, NP, López, ME, Aurtenetxe, S, Bajo, R, Pineda-Pardo, JA, Bruña, R, Marín, AG, Delgado, M, Barabash, A, I, , Cabranes, JA, Fernandez, A, Del Pozo, F, Sancho, M, Marcos, A, Nakamura, A and Maestú, F (2015) Influence of the APOE ε4 allele and mild cognitive impairment diagnosis in the disruption of the MEG resting state functional connectivity in sources space. Journal of Alzheimer's Disease 44(2), 493505. https://doi.org/10.3233/JAD-141872CrossRefGoogle ScholarPubMed
Damoiseaux, JS, Beckmann, CF, Arigita, EJS, Barkhof, F, Scheltens, P, Stam, CJ, Smith, SM and Rombouts, SARB (2008) Reduced resting-state brain activity in the default network in normal aging. Cerebral Cortex 18(8), 18561864. https://doi.org/10.1093/cercor/bhm207CrossRefGoogle ScholarPubMed
Delbeuck, X, Linden, M Van der and Collette, F (2003) Alzheimer’ Disease as a Disconnection Syndrome? Neuropsychology Review 13(2), 7992. https://doi.org/10.1023/A:1023832305702CrossRefGoogle Scholar
Desikan, RS, Ségonne, F, Fischl, B, Quinn, BT, Dickerson, BC, Blacker, D, Buckner, RL, Dale, AM, Maguire, RP, Hyman, B, Albert, MS and Killiany, RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31(3), 968980.CrossRefGoogle ScholarPubMed
Deuker, L, Bullmore, ET, Smith, M, Christensen, S, Nathan, PJ, Rockstroh, B and Bassett, DS (2009) Reproducibility of graph metrics of human brain functional networks. NeuroImage 47(4), 14601468. https://doi.org/10.1016/j.neuroimage.2009.05.035CrossRefGoogle ScholarPubMed
Estanga, A, Ecay-Torres, M, Ibañez, A, Izagirre, A, Villanua, J, Garcia-Sebastian, M, Iglesias Gaspar, MT, Otaegui Arrazola, A, Iriondo, A, Clerigue, M and Martinez-Lage, P (2017) Beneficial effect of bilingualism on Alzheimer's disease CSF biomarkers and cognition. Neurobiology of Aging 50, 144151. https://doi.org/10.1016/j.neurobiolaging.2016.10.013CrossRefGoogle ScholarPubMed
Fransson, P and Marrelec, G (2008) The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: Evidence from a partial correlation network analysis. Neuroimage 42(3), 1178-1184.CrossRefGoogle Scholar
Friederici, AD (2006) What's in control of language? Nature Neuroscience 9(8), 991992. https://doi.org/10.1038/nn0806-991CrossRefGoogle ScholarPubMed
European Commission Special Eurobarometer (2012) Europeans and their languages (386). Available at: http://ec.europa.eu/publicopinion/archives/ebs/ebs243Google Scholar
Fischl, B, Salat, DH, Busa, E, Albert, M, Dieterich, M, Haselgrove, C, van der Kouwe, A, Killiany, R, Kennedy, D, Klaveness, S, Montillo, A, Makris, N, Rosen, B and Dale, AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33 341355. Available at http://www.ncbi.nlm.nih.gov/pubmed/11832223CrossRefGoogle ScholarPubMed
Fuller-Thomson, E (2015) Emerging evidence contradicts the hypothesis thatbilingualism delays dementia onset. A Commentary on “Age of dementia diagnosis incommunity dwelling bilingual and monolingual Hispanic Americans” by Lawton et al., 2015. Cortex 66, 170172. https://doi.org/10.1016/j.cortex.2015.01.024CrossRefGoogle Scholar
Garcés, P, López-Sanz, D, Maestú, F and Pereda, E (2017) Choice of magnetometers and gradiometers after signal space separation. Sensors (Switzerland) 17(12), 113. https://doi.org/10.3390/s17122926CrossRefGoogle ScholarPubMed
García-Pentón, L, Pérez Fernández, A, Iturria-Medina, Y, Gillon-Dowens, M and Carreiras, M (2014) Anatomical connectivity changes in the bilingual brain. NeuroImage 84, 495504. https://doi.org/10.1016/j.neuroimage.2013.08.064CrossRefGoogle ScholarPubMed
Gold, BT, Kim, C, Johnson, NF, Kryscio, RJ and Smith, CD (2013) Lifelong Bilingualism Maintains Neural Efficiency for Cognitive Control in Aging. Journal of Neuroscience 33(2), 387396. https://doi.org/10.1523/JNEUROSCI.3837-12.2013CrossRefGoogle 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(14), 38263830. https://doi.org/10.1016/j.neuropsychologia.2011.09.041CrossRefGoogle Scholar
Grabner, RH, Brunner, C, Leeb, R, Neuper, C and Pfurtscheller, G (2007) Event-related EEG theta and alpha band oscillatory responses during language translation. Brain Research Bulletin 72(1), 5765. https://doi.org/10.1016/j.brainresbull.2007.01.001CrossRefGoogle ScholarPubMed
Grady, CL, Luk, G, Craik, FIM and Bialystok, E (2015) Brain network activity in monolingual and bilingual older adults. Neuropsychologia 66, 170181. https://doi.org/10.1016/j.neuropsychologia.2014.10.042CrossRefGoogle ScholarPubMed
Gramfort, A, Papadopoulo, T, Olivi, E and Clerc, M (2010) OpenMEEG: opensource software for quasistatic bioelectromagnetics. Biomedical Engineering Online 9, 45. https://doi.org/10.1186/1475-925X-9-45CrossRefGoogle ScholarPubMed
Grant, A, Dennis, NA and Li, P (2014) Cognitive control, cognitive reserve, and memory in the aging bilingual brain. Frontiers in Psychology 5(DEC), 110. https://doi.org/10.3389/fpsyg.2014.01401CrossRefGoogle ScholarPubMed
Grundy, JG, Anderson, JAE and Bialystok, E (2017) Neural correlates of cognitive processing in monolinguals and bilinguals. Annals of the New York Academy of Sciences 183201. https://doi.org/10.1111/nyas.13333CrossRefGoogle ScholarPubMed
Guzmán-Vélez, E and Tranel, D (2015) Does bilingualism contribute to cognitive reserve? Cognitive and neural perspectives. Neuropsychology 29(1), 139.CrossRefGoogle ScholarPubMed
Hardmeier, M, Hatz, F, Bousleiman, H, Schindler, C, Stam, CJ and Fuhr, P (2014) Reproducibility of functional connectivity and graph measures based on the phase lag index (PLI) and weighted phase lag index (wPLI) derived from high resolution EEG. PloS One 9(10), e108648. https://doi.org/10.1371/journal.pone.0108648CrossRefGoogle ScholarPubMed
Hernández, M, Martin, CD, Barceló, F and Costa, A (2013) Where is the bilingual advantage in task-switching? Journal of Memory and Language 69(3), 257276. https://doi.org/10.1016/j.jml.2013.06.004CrossRefGoogle Scholar
Hsu, CT, Jacobs, AM and Conrad, M (2015) Can Harry Potter still put a spell on us in a second language? An fMRI study on reading emotion-laden literature in late bilinguals. Cortex 63, 282295. https://doi.org/10.1016/j.cortex.2014.09.002CrossRefGoogle Scholar
Hudspeth, AJ, Jessell, TM, Kandel, ER, Schwartz, JH and Siegelbaum, SA (Eds) (2013) Principles of neural science. McGraw-Hill, Health Professions Division.Google Scholar
Jin, S-H, Seol, J, Kim, JS and Chung, CK (2011) How reliable are the functional connectivity networks of MEG in resting states? Journal of Neurophysiology 106(6), 28882895. https://doi.org/10.1152/jn.00335.2011CrossRefGoogle ScholarPubMed
Jones, D, Knopman, DS, Gunter, JL, Graff-Radford, J, Vemuri, P, Boeve, BF, Petersen, RC,Weiner, MW and Jack, CR (2015) Cascading network failure across the Alzheimer's disease spectrum. Brain 139(2), 547562. https://doi.org/10.1093/brain/awv338CrossRefGoogle ScholarPubMed
Jones, DT, Machulda, MM, Vemuri, P, McDade, EM, Zeng, G, Senjem, ML, Gunter, SA, Przybelski, RT, Avula, DS, Knopman, BF, Boeve, RC, Petersen, and Jack, CR (2011) Age-related changes in the default mode network are more advanced in Alzheimer disease. Neurology 77, 15241531. https://doi.org/10.1212/WNL.0b013e318233b33dCrossRefGoogle ScholarPubMed
Klimova, B, Valis, M and Kuca, K (2017) Bilingualism as a strategy to delay the onset of Alzheimer's disease. Clinical Interventions in Aging 12, 17311737. https://doi.org/10.2147/CIA.S145397CrossRefGoogle ScholarPubMed
Kousaie, S, Chai, XJ, Sander, KM and Klein, D (2017) Simultaneous learning of two languages from birth positively impacts intrinsic functional connectivity and cognitive control. Brain and Cognition 117(March), 4956. https://doi.org/10.1016/j.bandc.2017.06.003CrossRefGoogle ScholarPubMed
Lachaux, J-P, Rodriguez, E, Martinerie, J and Varela, FJ (1999) Measuring Phase Synchrony in Brain Signals. Human Brain Mapping 8, 194208.3.0.CO;2-C>CrossRefGoogle ScholarPubMed
Ley 14/1970, de 4 de agosto, General de Educación y Financiamiento de la Reforma Educativa. Boletín Oficial del Estado, núm. 187, de 6 de agosto de 1970, páginas 12525 a 12546 https://www.boe.es/buscar/doc.php?id=BOE-A-1970-852Google Scholar
Li, L, Abutalebi, J, Zou, L, Yan, X, Liu, L, Feng, X, Wang, R, Guo, T and Ding, G (2015) Bilingualism alters brain functional connectivity between “control” regions and “language” regions: Evidence from bimodal bilinguals. Neuropsychologia 71, 236247. https://doi.org/10.1016/j.neuropsychologia.2015.04.007CrossRefGoogle ScholarPubMed
Litvak, V, Mattout, J, Kiebel, S, Phillips, C, Henson, R, Kilner, J, Barnes, G, Oostenveld, R, Daunizeau, J, Flandin, G, Penny, W and Friston, K (2011) EEG and MEG data analysis in SPM8. Computational Intelligence and Neuroscience 852961. https://doi.org/10.1155/2011/852961Google ScholarPubMed
Liu, YC, Liu, YY, Yip, PK, Meguro, M and Meguro, K (2017) Speaking one more language in early life has only minor effects on cognition in Taiwanese with low education level: the Taishan Project. Psychogeriatrics 17, 256261. https://doi.org/10.1111/psyg.12230CrossRefGoogle ScholarPubMed
Lobo, A, Ezquerra, J, Gomez Burgada, F, Sala, JM and Seva Dıaz, A (1979) Cognocitive mini-test (a simple practical test to detect intellectual changes in medical patients). Actas luso españolas Neurol. Psiquiatr. y ciencias afines. 7 189202. Available at: http://europepmc.org/abstract/med/474231Google Scholar
López-Sanz, D, Bruña, R, Garcés, P, Martín-Buro, MC, Walter, S, Delgado, ML, Montenegro, M, Lopez-Higes, R, Marcos, A and Maestú, F (2017a) Functional Connectivity Disruption in Subjective Cognitive Decline and Mild Cognitive Impairment: A Common Pattern of Alterations. Frontiers in Aging Neuroscience 9, 109. https://doi.org/10.3389/fnagi.2017.00109CrossRefGoogle Scholar
López-Sanz, D, Garcés, P, Álvarez, B, Delgado-Losada, ML, López-Higes, R and Maestú, F (2017b) Network Disruption in the Preclinical Stages of Alzheimer's Disease: From Subjective Cognitive Decline to Mild Cognitive Impairment. International Journal of Neural Systems 27(8), 1750041. https://doi.org/10.1142/S0129065717500411CrossRefGoogle Scholar
Lopez, ME, Aurtenetxe, S, Pereda, E, Cuesta, P, Castellanos, NP, Bruña, R, Niso, G, Maestu, F and Bajo, R (2014) Cognitive reserve is associated with the functional organization of the brain in healthy aging: A MEG study. Frontiers in Aging Neuroscience 6(JUN), 19. https://doi.org/10.3389/fnagi.2014.00125Google ScholarPubMed
Luk, G, Bialystok, E, Craik, FI and Grady, CL (2011) Lifelong bilingualism maintains white matter integrity in older adults. Journal of Neuroscience 31(46), 16808-16813.CrossRefGoogle ScholarPubMed
Luk, G, Green, DW, Abutalebi, J and Grady, C (2012) Cognitive control for language switching in bilinguals: A quantitative meta-analysis of functional neuroimaging studies. Language and cognitive processes 27(10), 1479-1488.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(5), 605-621.CrossRefGoogle Scholar
Maris, E and Oostenveld, R (2007) Nonparametric statistical testing of EEG- and MEG-data. Journal of Neuroscience Methods 164(1), 177190. https://doi.org/10.1016/j.jneumeth.2007.03.024CrossRefGoogle ScholarPubMed
Mesulam, MM (1990) Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Annals of Neurology: Official Journal of the American Neurological Association and the Child Neurology Society 28(5), 597-613.CrossRefGoogle Scholar
Mesulam, M (1998) From sensation to perception. Brain 121, 10131052. https://doi.org/10.1093/brain/121.6.1013CrossRefGoogle Scholar
Moritz-Gasser, S and Duffau, H (2009) Cognitive processes and neural basis of language switching: Proposal of a new model. NeuroReport 20(18), 15771580. https://doi.org/10.1097/WNR.0b013e328333907eCrossRefGoogle ScholarPubMed
Nakamura, A, Cuesta, P, Kato, T, Arahata, Y, Iwata, K, Yamagishi, M, Kuratsubo, I, Kato, K, Bundo, M, Diers, K, Fernández, A, Maestú, F and Ito, K (2017) Early functional network alterations in asymptomatic elders at risk for Alzheimer's disease. Scientific Reports 7(1), 111. https://doi.org/10.1038/s41598-017-06876-8CrossRefGoogle ScholarPubMed
Oberhuber, M, Hope, TMH, Seghier, ML, Parker Jones, O, Prejawa, S, Green, DW and Price, CJ (2016) Four Functionally Distinct Regions in the Left Supramarginal Gyrus Support Word Processing. Cerebral Cortex 26(11), 42124226. https://doi.org/10.1093/cercor/bhw251CrossRefGoogle ScholarPubMed
Olsen, RK, Pangelinan, MM, Bogulski, C, Chakravarty, MM, Luk, G, Grady, CL and 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.2015.02.034CrossRefGoogle ScholarPubMed
Oostenveld, R, Fries, P, Maris, E and Schoffelen, JM (2011) FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Computational Intelligence and Neuroscience 2011, 156869. https://doi.org/10.1155/2011/156869CrossRefGoogle ScholarPubMed
Paap, KR, Johnson, HA and Sawi, O (2014) Are bilingual advantages dependent upon specific tasks or specific bilingual experiences? Journal of Cognitive Psychology 26(6), 615639. https://doi.org/10.1080/20445911.2014.944914CrossRefGoogle Scholar
Perani, D, Farsad, M, Ballarini, T, Lubian, F, Malpetti, M, Fracchetti, A, Magnani, G, March, A and Abutalebi, J (2017) The impact of bilingualism on brain reserve and metabolic connectivity in Alzheimer's dementia. Proceedings of the National Academy of Sciences 114(7), 16901695. https://doi.org/10.1073/pnas.1610909114CrossRefGoogle ScholarPubMed
Pérez, A, Carreiras, M, Gillon Dowens, M and Duñabeitia, JA (2015) Differential oscillatory encoding of foreign speech. Brain and Language 147, 5157. https://doi.org/10.1016/j.bandl.2015.05.008CrossRefGoogle ScholarPubMed
Pfeffer, RI, Kurosaki, TT, Harrah, CH, Chance, JM and Filos, S (1982) Measurement of Functional Activities in Older Adults in the Community. J. Gerontol. 37, 323329. Available at: 0.1093/geronj/37.3.323.CrossRefGoogle Scholar
Pliatsikas, C and Luk, G (2016) Executive control in bilinguals: A concise review on fMRI studies. Bilingualism 19(4), 699705. https://doi.org/10.1017/S1366728916000249CrossRefGoogle Scholar
Price, CJ, Green, DW and Von Studnitz, R (1999) A functional imaging study of translation and language switching. Brain 122(12), 22212235. https://doi.org/10.1093/brain/122.12.2221CrossRefGoogle ScholarPubMed
Rosen, WG, Terry, RD, Fuld, PA, Katzman, R and Peck, A (1980) Pathological verification of ischemic score in differentiation of dementias. Ann. Neurol. 7, 486488. Available at: 10.1002/ana.410070516.CrossRefGoogle ScholarPubMed
Rossi, E, Cheng, H, Kroll, JF, Diaz, MT and Newman, SD (2017) Changes in white-matter connectivity in late second language learners: Evidence from diffusion tensor imaging. Frontiers in Psychology 8(NOV), 115. https://doi.org/10.3389/fpsyg.2017.02040CrossRefGoogle ScholarPubMed
Satz, P (1993) Brain Reserve Capacity on Symptom Onset After Brain Injury: A Formulation and Review of Evidence for Threshold Theory. Neuropsychology 7(3), 273295. https://doi.org/10.1037/0894-4105.7.3.273CrossRefGoogle Scholar
Schweizer, TA, Ware, J, Fischer, CE, Craik, FIM and Bialystok, E (2012) Bilingualism as a contributor to cognitive reserve: Evidence from brain atrophy in Alzheimer's disease. Cortex 48(8), 991996. https://doi.org/10.1016/j.cortex.2011.04.009CrossRefGoogle ScholarPubMed
Stam, CJ (2014) Modern network science of neurological disorders. Nature Reviews Neuroscience 15(10), 683–95. https://doi.org/10.1038/nrn3801CrossRefGoogle ScholarPubMed
Stern, Y (2002) What is cognitive reservce? Theory and research application of the reserve concept. Journal of the International Neuropsychological Society 448460.CrossRefGoogle ScholarPubMed
Stocco, A and Prat, CS (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.2014.07.005CrossRefGoogle ScholarPubMed
Suh, S, Yoon, HW, Lee, S, Chung, JY, Cho, ZH and Park, HW (2007) Effects of syntactic complexity in L1 and L2; An fMRI study of Korean-English bilinguals. Brain Research 1136(1), 178189. https://doi.org/10.1016/j.brainres.2006.12.043CrossRefGoogle ScholarPubMed
Taulu, S and Simola, J (2006) Spatiotemporal signal space separation method for rejecting nearby interference in MEG measurements. Physics in Medicine and Biology 51(7), 1759–68. https://doi.org/10.1088/0031-9155/51/7/008CrossRefGoogle ScholarPubMed
Van Veen, BD, van Drongelen, W, Yuchtman, M and Suzuki, A (1997) Localization of brain electrical activity via linearly constrained minimum variance spatial filtering. IEEE Transactions on Bio-Medical Engineering 44(9), 867–80. https://doi.org/10.1109/10.623056CrossRefGoogle ScholarPubMed
Varela, F, Lachaux, JP, Rodriguez, E and Martinerie, J (2001) The brainweb: Phase synchronization and large-scale integration. Nature Reviews Neuroscience 2(4), 229239. https://doi.org/10.1038/35067550CrossRefGoogle ScholarPubMed
Wong, B, Yin, B and O'Brien, B (2016) Neurolinguistics: Structure, function, and connectivity in the bilingual brain. BioMed research international 2016.CrossRefGoogle ScholarPubMed
Yesavage, JA, Brink, TL, Rose, TL, Lum, O, Huang, V, Adey, M and Leirer, VO (1983) Development and validation of a geriatric depression screening scale: A preliminary report. Journal of Psychiatric Research 17, 3749. Available at: 10.1016/0022- 3956(82)90033-4.CrossRefGoogle Scholar
Yu, M, Engels, MMA, Hillebrand, A, van Straaten, ECW, Gouw, AA, Teunissen, C, van der Flier, WM, Scheltens, P and Stam, CJ (2017) Selective impairment of hippocampus and posterior hub areas in Alzheimer's disease: an MEG-based multiplex network study. Brain 140(5), 14661485. https://doi.org/10.1093/brain/awx050CrossRefGoogle ScholarPubMed
Zahodne, LB, Schofield, PW, Farrell, MT, Stern, Y and Manly, JJ (2014) Bilingualism does not alter cognitive decline or dementia risk among spanish-speaking immigrants. Neuropsychology 28(2), 238246. https://doi.org/10.1037/neu0000014CrossRefGoogle ScholarPubMed
Zatorre, RJ, Belin, P, Crane, PK, Gruhl, JC, Erosheva, EA, Gibbons, LE, McCurry, SM, Rhoads, K, Nguyen, V, Arani, K, Masaki, M and White, L (2001) Use of spoken and written Japanese did not protect Japanese-American men from cognitive decline in late life. Cerebral Cortex (New York, N.Y.: 1991), 65 B(6), 654666. https://doi.org/10.1093/geronb/gbq046Google Scholar
Zhang, M, Li, J, Chen, C, Xue, G, Lu, Z, Mei, L, Xue, H, Xue, F, He, Q, Chen, C, Wei, M and Dong, Q (2014) Resting-state functional connectivity and reading abilities in first and second languages. NeuroImage 84, 546553. https://doi.org/10.1016/j.neuroimage.2013.09.006CrossRefGoogle ScholarPubMed
Zou, L, Abutalebi, J, Zinszer, B, Yan, X, Shu, H, Peng, D and Ding, G (2012) Second language experience modulates functional brain network for the native language production in bimodal bilinguals. NeuroImage 62(3), 13671375. https://doi.org/10.1016/j.neuroimage.2012.05.062CrossRefGoogle ScholarPubMed
Zou, L, Ding, G, Abutalebi, J, Shu, H and Peng, D (2012) Structural plasticity of the left caudate in bimodal bilinguals. Cortex 48(9), 11971206. https://doi.org/10.1016/j.cortex.2011.05.022iCrossRefGoogle ScholarPubMed