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Discussion forum
Executive control, brain aging and bilingualism Brian T. Gold a,b,c,* a
Department of Anatomy and Neurobiology, University of Kentucky, Lexington, KY, USA Magnetic Resonance Imaging and Spectroscopy Center, University of Kentucky, Lexington, KY, USA c Sanders-Brown Center on Aging, University of Kentucky, Lexington, KY, USA b
A number of studies have suggested that bilingualism enhances executive control (EC) functions, which may boost cognitive reserve in aging (c.f. Bialystok & Craik, 2010). In a review article Paap, Johnson, and Sawi (2015) have called putative bilingual advantages into question. The authors put forth a wide-ranging set of criticisms, including that some studies in this field have been conducted with small sample sizes, that bilingualism is confounded immigration status in some studies, and that a consistent pattern of imagingbehavioral correlations have yet to emerge in the field. While acknowledging these points, this commentary will argue that looking at the big picture nonetheless indicates much support for bilingualism as a cognitive reserve variable in aging.
1. Bilingualism, immigration status and cognitive reserve in aging One of the potentially most important benefits of bilingualism is that it may slow cognitive declines in aging and age-related neurodegenerative disease (Bialystok, Craik, & Freedman, 2007; Craik, Bialystok, & Freedman, 2010). Paap et al. note that bilingualism has been confounded with immigration status in a number of studies with older adult participants. The authors describe the results of several studies in which bilingualism was not associated with better cognitive functions in aging when immigration status was controlled. Unfortunately, however, Paap et al. fail to describe results from two critically important studies which contained large sample sizes and provided evidence for bilingualism as a reserve variable independent of immigration status (Alladi et al., 2013; Bak, Nissan, Allerhand, & Deary, 2014).
In the study of Alladi et al. (2013), participants (N ¼ 648) were individuals born and raised in India who were involved in a longitudinal dementia study, 391 of whom were multilingual. Results indicated that bilingual patients developed clinical symptoms suggestive of Alzheimer's disease or other dementia an average of 4.5 years later than monolingual patients. In the study of Bak et al. (2014), participants (N ¼ 853) were individuals born and raised in Scotland who were part of the Lothian Birth Cohort 1936 study and underwent baseline cognitive testing in 1947 (at 11 years of age) and were then retested in 2008e2010 (at a mean age of 72.5 years old). Results indicated that older adult bilinguals performed significantly better than their monolingual peers on measures of fluid intelligence, verbal fluency and visual search speed even after controlling for childhood scores on these measures. Together, results from these studies provide strong evidence that bilingual influences on cognitive functions in aging do not depend upon immigration status.
2. Neuroimaging results have not been informative Paap et al. argue that neuroimaging results have not been informative in the bilingual literature because results do not align with the behavioral data in a consistent and cohesive way. However, this seems to be an unreasonable expectation for potential reserve variable in its relative infancy of study. Indeed, putative reserve variables that have been studied for much longer than bilingualism such as education, socioeconomic status, and diet have yet to be linked with specific cognitive processes, or specific brain systems, let alone with consistent cognitive-neuroimaging relationships. A more pertinent question, at least within the field of aging
* Department of Anatomy and Neurobiology, University of Kentucky College of Medicine, Lexington, KY, 40536-0298, USA. E-mail address:
[email protected]. http://dx.doi.org/10.1016/j.cortex.2015.06.014 0010-9452/© 2015 Elsevier Ltd. All rights reserved.
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neuroscience, would be whether there is evidence that bilingualism benefits structural and functional EC systems that undergo pronounced age-related declines. This evidence does exist. For example, bilinguals have been found to show greater gray matter (GM) volume/density than monolinguals in the anterior cingulate cortex (Abutalebi et al., 2012) and inferior parietal cortex (Abutalebi et al., 2015). Importantly, the effect in the inferior parietal cortex is further correlated with age of acquisition, with greater length of time speaking two languages being associated with higher GM density in this region (Mechelli et al., 2004). Bilinguals have also been found to show greater white matter (WM) volume in the prefrontal cortex (Olsen et al., 2015) and better WM microstructure than monolinguals in several tracts connecting portions of the EC network (Luk, Bialystok, Craik, & Grady, 2011). In addition, several studies have noted stronger resting state functional connectivity between EC structures in bilinguals compared to monolinguals (Grady, Luk, Craik, & Bialystok, 2015; Luk et al., 2011). It is also worth noting that several meaningful imagingbehavioral correlations have been reported (Gold, Kim, Johnson, Kryscio, & Smith, 2013; Olsen et al., 2015). In an fMRI study, we found that older adult bilinguals showed lower response in frontal regions than monolinguals, and lower frontal response was correlated with faster task switching reaction time (Gold et al., 2013). In a different study, older adult bilinguals showed higher WM volume than monolinguals, and WM volume was negatively correlated with the Stroop interference effect. Paap et al. imply that results from our study are rendered moot by the fact that the group difference in reaction time did not quite reach conventional statistical significance of p < .05 (it was p ¼ .056). However, this seems to miss the big picture point that the pattern of lower frontal metabolic response and (marginally) faster response in bilinguals results provides one of several instances of a cohesive imagingbehavioral correlation. Specifically, it is consistent with the theory that bilingualism represents a form of practice effects on EC brain systems and their functions (Green & Abutalebi, 2013). As noted, neuroimaging differences in the field of bilingualism and aging have not always been directly correlated with behavioral effects. Importantly, though, even in the broader aging literature, the strength of association between EC measures and relevant imaging indices (e.g., GM volume in frontal regions) varies greatly across different EC measures (Yuan & Raz, 2014). The lack of behavioral-imaging correlations in some bilingual studies could thus reflect a suboptimal pairing between the neuroimaging indices and specific EC behavioral measures used in those studies. Alternatively, it is possible that bilingual advantages may be restricted to specific EC testsdas suggested by Paap et al. Future longitudinal studies should help decide between these two possibilities while controlling for potentially confounding variables.
Acknowledgments This work was supported in part by a grant from the National Institutes of Health Institute of Aging (R01-AG033036). The
content is solely the responsibility of the author and does not necessarily represent the official views of the NIH.
references
Abutalebi, J., Canini, M., Della Rosa, P. A., Sheung, L. P., 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, 3e13. Abutalebi, J., Della Rosa, P. A., Green, D. W., Hernandez, M., Scifo, P., Keim, R., et al. (2012). Bilingualism tunes the anterior cingulate cortex for conflict monitoring. Cerebral Cortex, 22(9), 2076e2086. Alladi, S., Bak, T. H., Duggirala, V., Surampudi, B., Shailaja, M., Shukla, A. K., et al. (2013). Bilingualism delays age at onset of dementia, independent of education and immigration status. Neurology, 81(22), 1938e1944. Bak, T. H., Nissan, J. J., Allerhand, M. M., & Deary, I. J. (2014). Does bilingualism influence cognitive aging? Annals of Neurology, 75(6), 959e963. Bialystok, E., & Craik, F. I. M. (2010). Cognitive and linguisitc processing in the bilingual mind. Current Directions in Psychological Science, 19, 19e23. Bialystok, E., Craik, F. I., & Freedman, M. (2007). Bilingualism as a protection against the onset of symptoms of dementia. Neuropsychologia, 45(2), 459e464. Craik, F. I., Bialystok, E., & Freedman, M. (2010). Delaying the onset of Alzheimer disease: bilingualism as a form of cognitive reserve. Neurology, 75(19), 1726e1729. Gold, B. T., Kim, C., Johnson, N. F., Kryscio, R. J., & Smith, C. D. (2013). Lifelong bilingualism maintains neural efficiency for cognitive control in aging. Journal of Neuroscience, 33(2), 387e396. Grady, C. L., Luk, G., Craik, F. I., & Bialystok, E. (2015). Brain network activity in monolingual and bilingual older adults. Neuropsychologia, 66, 170e181. Green, D. W., & Abutalebi, J. (2013). Language control in bilinguals: the adaptive control hypothesis. Journal of Cognitive Psychology (Hove, England), 25(5), 515e530. Luk, G., Bialystok, E., Craik, F. I., & Grady, C. L. (2011). Lifelong bilingualism maintains white matter integrity in older adults. Journal of Neuroscience, 31(46), 16808e16813. Mechelli, A., Crinion, J. T., Noppeney, U., O'Doherty, J., Ashburner, J., Frackowiak, R. S., et al. (2004). Neurolinguistics: structural plasticity in the bilingual brain. Nature, 431(7010), 757. Olsen, R. K., Pangelinan, M. M., Bogulski, C., Chakravarty, M. M., Luk, G., Grady, C. L., et al. (2015). The effect of lifelong bilingualism on regional grey and white matter volume. Brain Research, 1612, 128e139. Paap, K., Johnson, H. A., & Sawi, O. (2015). Bilingual advantages in executive functioning either do not exist or are restricted to very specific and undetermined circumstances. Cortex, 69, 265e278. http://dx.doi.org/10.1016/j.cortex.2015.04.014. Yuan, P., & Raz, N. (2014). Prefrontal cortex and executive functions in healthy adults: a meta-analysis of structural neuroimaging studies. Neuroscience & Biobehavioral Reviews, 42, 180e192.
Received 12 June 2015 Accepted 16 June 2015
