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Research Article

The impact of bilingualism on brain reserve and metabolic connectivity in Alzheimer's dementia

Daniela Perani, Mohsen Farsad, Tommaso Ballarini, Francesca Lubian, Maura Malpetti, Alessandro Fracchetti, Giuseppe Magnani, Albert March, and Jubin Abutalebi
PNAS February 14, 2017 114 (7) 1690-1695; first published January 30, 2017; https://doi.org/10.1073/pnas.1610909114
Daniela Perani
aFaculty of Psychology, Vita-Salute San Raffaele University, 20132 Milan, Italy;
bIn Vivo Human Molecular and Structural Neuroimaging Unit, Division of Neuroscience, San Raffaele Scientific Institute, 20132 Milan, Italy;
cNuclear Medicine Unit, San Raffaele Hospital, 20132 Milan, Italy;
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  • For correspondence: perani.daniela@hsr.it
Mohsen Farsad
dNuclear Medicine Unit, Azienda Sanitaria dell’Alto Adige, 39100 Bolzano, Italy;
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Tommaso Ballarini
bIn Vivo Human Molecular and Structural Neuroimaging Unit, Division of Neuroscience, San Raffaele Scientific Institute, 20132 Milan, Italy;
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Francesca Lubian
eMemory Clinic, Geriatric Department, Azienda Sanitaria dell'Alto Adige, 39100 Bolzano, Italy;
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Maura Malpetti
aFaculty of Psychology, Vita-Salute San Raffaele University, 20132 Milan, Italy;
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Alessandro Fracchetti
fDepartment of Physics, Azienda Sanitaria dell'Alto Adige, 39100 Bolzano, Italy;
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Giuseppe Magnani
gDepartment of Neurology, San Raffaele Hospital, 20132 Milan, Italy
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Albert March
eMemory Clinic, Geriatric Department, Azienda Sanitaria dell'Alto Adige, 39100 Bolzano, Italy;
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Jubin Abutalebi
aFaculty of Psychology, Vita-Salute San Raffaele University, 20132 Milan, Italy;
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  1. Edited by Leslie G. Ungerleider, National Institute of Mental Health, Bethesda, MD, and approved December 23, 2016 (received for review July 5, 2016)

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Significance

Recent epidemiological studies report that lifelong bilingualism may delay dementia onset. However, the underlying neural mechanism of these protective effects is largely unknown. Using fluorodeoxyglucose and PET to investigate brain metabolism and neural connectivity in individuals with Alzheimer’s dementia, we unravel the neural mechanism responsible for the bilingual individuals’ ability to cope better with Alzheimer’s dementia. These findings foster the view that lifelong bilingualism contributes to brain cognitive reserve.

Abstract

Cognitive reserve (CR) prevents cognitive decline and delays neurodegeneration. Recent epidemiological evidence suggests that lifelong bilingualism may act as CR delaying the onset of dementia by ∼4.5 y. Much controversy surrounds the issue of bilingualism and its putative neuroprotective effects. We studied brain metabolism, a direct index of synaptic function and density, and neural connectivity to shed light on the effects of bilingualism in vivo in Alzheimer’s dementia (AD). Eighty-five patients with probable AD and matched for disease duration (45 German-Italian bilingual speakers and 40 monolingual speakers) were included. Notably, bilingual individuals were on average 5 y older than their monolingual peers. In agreement with our predictions and with models of CR, cerebral hypometabolism was more severe in the group of bilingual individuals with AD. The metabolic connectivity analyses crucially supported the neuroprotective effect of bilingualism by showing an increased connectivity in the executive control and the default mode networks in the bilingual, compared with the monolingual, AD patients. Furthermore, the degree of lifelong bilingualism (i.e., high, moderate, or low use) was significantly correlated to functional modulations in crucial neural networks, suggesting both neural reserve and compensatory mechanisms. These findings indicate that lifelong bilingualism acts as a powerful CR proxy in dementia and exerts neuroprotective effects against neurodegeneration. Delaying the onset of dementia is a top priority of modern societies, and the present in vivo neurobiological evidence should stimulate social programs and interventions to support bilingual or multilingual education and the maintenance of the second language among senior citizens.

  • bilingualism
  • Alzheimer’s dementia
  • fluorine-18-fluorodeoxyglucose PET
  • brain reserve
  • brain metabolic connectivity

Footnotes

  • ↵1To whom correspondence should be addressed. Email: perani.daniela{at}hsr.it.
  • Author contributions: D.P. and J.A. designed research; D.P., M.F., T.B., F.L., M.M., A.F., G.M., A.M., and J.A. performed research; T.B. and M.M. analyzed data; and D.P., T.B., M.M., and J.A. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1610909114/-/DCSupplemental.

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Bilingualism, brain reserve, and dementia
Daniela Perani, Mohsen Farsad, Tommaso Ballarini, Francesca Lubian, Maura Malpetti, Alessandro Fracchetti, Giuseppe Magnani, Albert March, Jubin Abutalebi
Proceedings of the National Academy of Sciences Feb 2017, 114 (7) 1690-1695; DOI: 10.1073/pnas.1610909114

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Bilingualism, brain reserve, and dementia
Daniela Perani, Mohsen Farsad, Tommaso Ballarini, Francesca Lubian, Maura Malpetti, Alessandro Fracchetti, Giuseppe Magnani, Albert March, Jubin Abutalebi
Proceedings of the National Academy of Sciences Feb 2017, 114 (7) 1690-1695; DOI: 10.1073/pnas.1610909114
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Proceedings of the National Academy of Sciences: 114 (7)
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