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Different patterns of brain volume loss in bilingual versus monolingual speakers with primary progressive aphasia

Stephanie M. Grasso1*, Jessica De Leon2, Ariane Welch2, Zachary Miller2, Wendy Shwe2, Maria Luisa Gorno-Tempini2 and Maya L. Henry1
  • 1 University of Texas at Austin, United States
  • 2 Department of Neurology, University of California, San Francisco, United States

Bilingualism has been associated with regional volumetric enhancements in language and cognitive control networks in neurotypical individuals (e.g., García-Pentón, Fernández García, Costello, Duñabeitia & Carreiras, 2016). Although studies have recently begun to investigate whether these brain regions show evidence of a protective benefit in bilingual speakers with mild neurocognitive disorder or Alzheimer’s dementia (Duncan, Nikelski, Pilon, Steffener, Chertkow, & Phillips, 2018), such an effect has yet to be examined in language-prominent neurodegenerative syndromes, or primary progressive aphasia (PPA). In this retrospective study we examined whether bilingual speakers demonstrated a slower rate of volume loss relative to monolinguals in regions previously shown to be volumetrically enhanced in neurotypical bilinguals. We selected 8mm regions-of-interest (ROIs) based on previous literature (for a review see García-Pentón et al., 2016) and compared the rate of gray matter volume change between mono- and bi-lingual speakers with semantic (svPPA) or nonfluent/agrammatic (nfvPPA) variant PPA. We hypothesized that bilingual speakers with PPA would demonstrate neural reserve (slower rate of volume loss) in regions shown to have enhanced volume in healthy bilingual speakers. Seventy-six individuals with PPA (Gorno-Tempini et al., 2011) were included in this study (48 monolingual speakers and 28 bilingual speakers). Two T1-weighted magnetic resonance images were available for each participant and the average time between visits was fourteen months. Images were segmented using voxel-based morphometry (VBM8 via SPM12). Gray matter volumes were analyzed using a mixed-effects linear regression with the dependent variable of ROI volume and a two-way interaction prediction term of speaker status (mono- and bi-lingual) and time (days between visits), and a random intercept of participant, within each PPA variant. Age and years of education were included as covariates in the model. Results indicated that bilingual individuals with svPPA demonstrated significantly less volume loss in a left orbitofrontal cortex (LOFC) and a right anterior middle cingulate ROI. No significant differences were observed between bilingual and monolingual speakers with nfvPPA. In our svPPA cohort, regions that differed significantly in rate of brain volume change comprise areas that are both volumetrically enhanced in bilinguals and shown to be susceptible with disease progression (e.g., Iaccarino et al., 2015). As such, this finding may reflect a complex interplay between network-based enhancement and susceptibility. In our nfvPPA cohort, the null finding may stem from the fact that individuals with this diagnosis often present with prominent motor speech impairment, which may or may not be accompanied by linguistic deficits. Bilingualism has not been shown to confer benefits to motoric abilities in other neurodegenerative conditions (e.g., Hindle et al., 2015). Future studies should continue to investigate which neurodegenerative syndromes demonstrate a protective benefit of bilingualism. This may inform theoretical models regarding bilingual language and cognition, as well as cognitive and neural reserve more broadly.

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Acknowledgements

This research was supported by Grant R01NS050915 awarded to Dr. Maria Luisa Gorno-Tempini by the National Institute of Neurological Disorders and Stroke; Grant R01DC016291 awarded to Dr. Maya L. Henry and Grant F31DC016229 awarded to Stephanie M. Grasso, MA, CCC-SLP by the National Institute on Deafness and Communicative Disorders.

References

Duncan, H. D., Nikelski, J., Pilon, R., Steffener, J., Chertkow, H., & Phillips, N. A. (2018). Structural brain differences between monolingual and multilingual patients with mild cognitive impairment and Alzheimer disease: Evidence for cognitive reserve. Neuropsychologia, 109(May 2017), 270–282. https://doi.org/10.1016/j.neuropsychologia.2017.12.036 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, 31(3), 303–327. https://doi.org/10.1080/23273798.2015.1068944 Gorno-Tempini, M. L., Hillis, a. E., Weintraub, S., Kertesz, a., Mendez, M., Cappa, S. F., … Grossman, M. (2011). Classification of primary progressive aphasia and its variants. Neurology, 76(11), 1006–1014. https://doi.org/10.1212/WNL.0b013e31821103e6 Hindle, J. V, Martin-forbes, P. A., Bastable, A. J. M., Pye, K. L., Martyr, A., Whitaker, C. J., … Ll, C. (2015). Cognitive Reserve in Parkinson ’ s Disease : The Effects of Welsh-English Bilingualism on Executive Function, 2015. https://doi.org/10.1155/2015/943572 Iaccarino, L., Crespi, C., Anthony, P., Rosa, D., Catrical, E., Guidi, L., … Perani, D. (2015). The Semantic Variant of Primary Progressive Aphasia : Clinical and Neuroimaging Evidence in Single Subjects, 1–17. https://doi.org/10.1371/journal.pone.0120197

Keywords: primary progressive aphasia, bilingualism, semantic variant (svPPA), nonfluent agrammatic primary progressive aphasia, Multilingualism

Conference: Academy of Aphasia 57th Annual Meeting, Macau, Macao, SAR China, 27 Oct - 29 Oct, 2019.

Presentation Type: Poster presentation

Topic: Eligible for student award

Citation: Grasso SM, De Leon J, Welch A, Miller Z, Shwe W, Gorno-Tempini M and Henry ML (2019). Different patterns of brain volume loss in bilingual versus monolingual speakers with primary progressive aphasia. Front. Hum. Neurosci. Conference Abstract: Academy of Aphasia 57th Annual Meeting. doi: 10.3389/conf.fnhum.2019.01.00049

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Received: 06 May 2019; Published Online: 09 Oct 2019.

* Correspondence: Ms. Stephanie M Grasso, University of Texas at Austin, Austin, United States, smgrasso@utexas.edu