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Striking loss of second language in bilingual patients with semantic dementia

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Abstract

Background

Studies of bilingual or multilingual patients with neurodegenerative diseases that disrupt language like the primary progressive aphasias (PPA) may contribute valuable information on language organization in the bilingual brain and on the factors affecting language decline. There is limited literature on bilingual PPA and in particular on semantic dementia, a type of PPA with selective loss of semantic memory. We studied the nature and severity of naming and comprehension deficits across languages in bilingual patients with semantic dementia (SD).

Methods

Sixteen bilingual patients with SD and 34 bilingual age-matched controls were administered the modified Boston Naming Test and components of Cambridge Semantic Battery. The patients’ performance on picture naming and word comprehension was compared across languages and with controls. The most proficient language on self-rating was labelled as L1 and less proficient as L2.

Results

We observed striking loss of second language (L2) in SD for both receptive and expressive language, even in patients who were premorbidly fluent in their L2. Naming and comprehension in every patient’s L2 were impaired relative to both their own first-language (L1) scores and controls’ L2 scores. Furthermore, item-specific correct responses in each patient’s L2 were a subset of their successes in L1.

Discussion

A striking contrast in performance between two languages in bilingual patients with SD indicates that a bilingual’s L2 or less proficient language is more vulnerable to neurodegeneration. Our findings also support a common semantic network in the brain for the different languages of bilinguals.

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References

  1. Grosjean F (2010) Bilingual: life and reality. Harvard University Press, Cambridge

    Book  Google Scholar 

  2. Lorenzen B, Murray LL (2008) Bilingual aphasia: a theoretical and clinical review. Am J Speech Lang Pathol 17:299–317. https://doi.org/10.1044/1058-0360(2008/026)

    Article  PubMed  Google Scholar 

  3. Mesulam M (1982) Slowly progressive aphasia without generalized dementia. Ann Neurol 11:592–598. https://doi.org/10.1002/ana.410110607

    Article  CAS  PubMed  Google Scholar 

  4. Mesulam MM (2001) Primary progressive aphasia. Ann Neurol 49:425–432. https://doi.org/10.1002/ana.91

    Article  CAS  PubMed  Google Scholar 

  5. Gorno-Tempini ML, Dronkers N, Rankin KP, Ogar JM, Phengrasamy L, Rosen HJ et al (2004) Cognition and anatomy in three variants of primary progressive aphasia. Ann Neurol 55:335–346. https://doi.org/10.1002/ana.10825

    Article  PubMed  PubMed Central  Google Scholar 

  6. Gorno-Tempini ML, Hillis AE, Weintraub S, Kertesz A, Mendez M, Cappa SF et al (2011) Classification of primary progressive aphasia and its variants. Neurology 76:1006–1014. https://doi.org/10.1212/WNL.0b013e31821103e6

    Article  PubMed  PubMed Central  Google Scholar 

  7. Warrington EK (1975) Selective impairment of semantic memory. Q J Exp Psychol 27:635–657. https://doi.org/10.1080/14640747508400525

    Article  CAS  PubMed  Google Scholar 

  8. Snowden JS, Goulding PJ, Neary D (1989) Semantic dementia: a form of circumscribed cerebral atrophy. Behav Neurol 2:167–182. https://doi.org/10.1136/jnnp.70.3.323

    Article  Google Scholar 

  9. Hodges JR, Patterson K, Oxbury S, Funnell E (1992) Semantic dementia: progressive fluent aphasia with temporal lobe atrophy. Brain 115:1783–1806. https://doi.org/10.1093/brain/115.6.1783

    Article  PubMed  Google Scholar 

  10. Hodges JR, Patterson K (2007) Semantic dementia: a unique clinicopathological syndrome. Lancet Neurol 6:1004–1014. https://doi.org/10.1016/S1474-4422(07)70266-1

    Article  CAS  PubMed  Google Scholar 

  11. Mendez MF (2004) Semantic dementia in multilingual patients. J Neuropychiatry Clin Neurosci 16:381. https://doi.org/10.1176/appi.neuropsych.16.3.381

    Article  Google Scholar 

  12. Liu YC, Yip PK, Fan YM, Meguro K (2012) A potential protective effect in multilingual patients with semantic dementia: two case reports of patients speaking Taiwanese and Japanese. Acta Neurol Taiwanica 21:25–30

    Google Scholar 

  13. Filley CM, Ramsberger G, Menn L, Wu J, Reid BY, Reid AL (2006) Primaryprogressive aphasia in a bilingual woman. Neurocase 12:296–299. https://doi.org/10.1080/13554790601126047

    Article  PubMed  Google Scholar 

  14. Hernandez M, Cano A, Costa A, Sebastian-Galles N, Juncadella M, Gascon-Bayarri J (2008) Grammatical category-specific deficits in bilingual aphasia. Brain Lang 107:68–80. https://doi.org/10.1016/j.bandl.2008.01.006

    Article  PubMed  Google Scholar 

  15. Machado A, Rodrigues M, Simoes S, Santana I, Soares- Fernandes J (2010) The Portuguese who could no longer speak French: primary progressive aphasia in a bilingual man. J Neuropsychiatry Clin Neurosci 22:E31–E32. https://doi.org/10.1176/jnp.2010.22.1.123.e31

    Article  Google Scholar 

  16. Zanini S, Angeli V, Tavano A (2011) Primary progressive aphasia in a bilingual speaker: a single-case study. Clin Linguist Phon 25:553–564. https://doi.org/10.3109/02699206.2011.566464

    Article  PubMed  Google Scholar 

  17. Kambanaros M, Grohmann KK (2011) BATting multilingual primary progressive aphasia for Greek, English, and Czech. J Neurolinguist 25:520–537. https://doi.org/10.1016/j.jneuroling.2011.01.006

    Article  Google Scholar 

  18. Larner AJ (2012) Progressive non-fluent aphasia in a bilingual subject: Relative preservation of “Mother Tongue”. J Neuropsychiatry Clin Neurosci 24:E9–E10. https://doi.org/10.1176/appi.neuropsych.11010019

    Article  PubMed  Google Scholar 

  19. Druks J, Weekes BS (2013) Parallel deterioration to language processing in a bilingual speaker. Cogn Neuropsychol 30:578–596. https://doi.org/10.1080/02643294.2014.882814

    Article  PubMed  Google Scholar 

  20. Karpathiou N, Papatriantafyllou J, Kambanaros M (2018) Bilingualism in a case of the non-fluent/agrammatic variant of primary progressive aphasia. FrontCommun 3:1–16. https://doi.org/10.3389/fcomm.2018.00052

    Article  Google Scholar 

  21. Costa AS, Jokel R, Villarejo A, Llamas-Velasco S, Domoto-Reilley K, Wojtala J, Reetz K, Machado Á (2019) Bilingualism in primary progressive aphasia: a retrospective study on clinical and language characteristics. Alzheimer Dis Assoc Disord 33:47–53. https://doi.org/10.1097/WAD.0000000000000288

    Article  PubMed  PubMed Central  Google Scholar 

  22. Malcolm T, Lerman A, Korytkowska M, Vonk JMJ, Obler LK (2019) Primary progressive aphasia in bilinguals and multilinguals. In: Schwieter (ed) The handbook of neuroscience of multilingualism. Wiley, Hoboken, pp 572–591

    Chapter  Google Scholar 

  23. Census India (2001). http://www.censusindia.gov.in. Accessed 31 May 2019

  24. Ramanan S, Narayanan J, D’Souza TP, Malik KS, Ratnavalli E (2015) Total output and switching in category fluency successfully discriminates Alzheimer’s disease from Mild Cognitive Impairment, but not from frontotemporal dementia. Dement Neuropsychol 9:251–257. https://doi.org/10.1590/1980-57642015DN93000007

    Article  PubMed  PubMed Central  Google Scholar 

  25. Mioshi E, Dawson K, Mitchell J, Arnold R, Hodges JR (2006) The Addenbrooke’s Cognitive Examination Revised (ACE-R): a brief cognitive test battery for dementia screening. Int J Geriatr Psychiatry 21:1078–1085. https://doi.org/10.1002/gps.1610

    Article  PubMed  Google Scholar 

  26. Mathuranath PS, Hodges JR, Mathew R, Cherian PJ, George A, Bak TH (2004) Adaptation of the ACE for a Malayalam speaking population in southern India. Int J Geriatr Psychiatry 19:1188–1194. https://doi.org/10.1002/gps.1239

    Article  CAS  PubMed  Google Scholar 

  27. George A, Mathuranath PS (2007) Community-based naming agreement, familiarity, image agreement and visual complexity ratings among adult Indians. Ann Indian Acad Neurol 10:92–99. https://doi.org/10.4103/0972-2327.33216

    Article  Google Scholar 

  28. Adlam AL, Patterson K, Bozeat S, Hodges JR (2010) Cambridge Semantic Memory Test Battery: detection of semantic deficits in semantic dementia and Alzheimer’s disease. Neurocase 16:193–207. https://doi.org/10.1080/13554790903405693

    Article  PubMed  Google Scholar 

  29. Green DW (2003) The neural basis of the lexicon and the grammar in L2 acquisition: the convergence hypothesis. In: van Hout R, Hulk A, Kuiken F, Towell R (eds) The Interface between syntax and the lexicon in second language acquisition. John Benjamins, Amsterdam, pp 197–218

    Chapter  Google Scholar 

  30. Perani D, Abutalebi J (2005) The neural basis of first and second language processing. Curr Opin Neurobiol 15:202–206. https://doi.org/10.1016/j.conb.2005.03.00

    Article  CAS  PubMed  Google Scholar 

  31. Crinion J, Turner R, Grogan A, Hanakawa T, Noppeney U, Devlin JT et al (2006) Language control in the bilingual brain. Science 312:1537–1540. https://doi.org/10.1126/science.1127761

    Article  CAS  PubMed  Google Scholar 

  32. Correia J, Formisano E, Valente G, Hausfeld L, Jansma Bonte M (2014) Brain-based translation: fMRI decoding of spoken words in bilinguals reveals language-independent semantic representations in anterior temporal lobe. J Neurosci 34:332–338. https://doi.org/10.1523/JNEUROSCI.1302-13.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Grogan A, Green DW, Ali N, Crinion JT, Price CJ (2009) Structural correlates of semantic and phonemic fluency ability in first and second languages. Cereb Cortex 19:2690–2698. https://doi.org/10.1093/cercor/bhp023

    Article  PubMed  PubMed Central  Google Scholar 

  34. Kroll JF, Stewart E (1994) Category interference in translation and picture naming: evidence for asymmetric connection between bilingual memory representations. J Mem Lang 33:149–174. https://doi.org/10.1006/jmla.1994.1008

    Article  Google Scholar 

  35. Patterson K, Lambon Ralph MA, Jefferies E, Woollams A, Jones R, Hodges JR et al (2006) “Presemantic” cognition in semantic dementia: six deficits in search of an explanation. J Cogn Neurosci 18:169–183. https://doi.org/10.1162/089892906775783714

    Article  PubMed  Google Scholar 

  36. Ellis AW, Lum C, Lambon Ralph MA (1996) On the use of regression techniques for the analysis of single case aphasic data. J Neurolinguistics 9:165–174. https://doi.org/10.1016/0911-6044(96),00008-5

    Article  Google Scholar 

  37. Lambon Ralph MA, Graham KS, Ellis AW, Hodges JR (1998) Naming in semantic dementia–what matters? Neuropsychologia 36:775–784. https://doi.org/10.1016/S0028-3932(97)00169-3

    Article  CAS  PubMed  Google Scholar 

  38. Woollams AM, Cooper-Pye E, Hodges JR, Patterson K (2008) Anomia: a doubly typical signature of semantic dementia. Neuropsychologia 46:2503–2514. https://doi.org/10.1016/j.neuropsychologia.2008.04.005

    Article  PubMed  Google Scholar 

  39. Morrison CM, Ellis AW (1995) Roles of word frequency and age of acquisition in word naming and lexical decision. J Exp Psychol Learn Mem Cogn 21:116–133. https://doi.org/10.1037/0278-7393.21.1.116

    Article  Google Scholar 

  40. Ellis AW, Ralph MAL (2000) Age of acquisition effects in adult lexical processing reflect loss of plasticity in maturing systems: insights from connectionist networks. J Expt Psychol Learn Mem Cogn 26:1103–1123. https://doi.org/10.1037/0278-7393.26.5.1103

    Article  CAS  Google Scholar 

  41. Lambon Ralph MA, Ehsan (2006) Age of acquisition effects depend on the mapping between representations and the frequency of occurrence: empirical and computational evidence. Vis Cogn 13:928–948. https://doi.org/10.1080/13506280544000110

    Article  Google Scholar 

  42. Perani D, Abutalebi J, Paulesu E, Brambati S, Scifo P, Cappa SF et al (2003) The role of age of acquisition and language usage in early, high-proficient bilinguals: a fMRI study during verbal fluency. Hum Brain Mapp 19:170–182. https://doi.org/10.1002/hbm.10110

    Article  PubMed  PubMed Central  Google Scholar 

  43. Wartenburger I, Heekeren HR, Abutalebi J, Cappa SF, Villringer A, Perani D (2003) Early setting of grammatical processing in the bilingual brain. Neuron 37:159–170. https://doi.org/10.1016/S0896-6273(02)01150-9

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank all the patients and their families for participating in the study and colleagues for referrals. Some of the findings from this study have been presented at the International Neuropsychological Society (INS) meeting in London, 6–8 July 2016, at the British Neuropsychological Society (BNS) meeting in London, 1 November 2018 and the International conference on Frontotemporal dementias in Sydney, 11–14 November 2018.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial or not-for-profit sectors.

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Authors and Affiliations

  1. Department of Neurology, Manipal Hospital, Bangalore, 560017, India

    Ratnavalli Ellajosyula & Jwala Narayanan

  2. Department of Neurology, Annasawmy Mudaliar Hospital, Bangalore, India

    Ratnavalli Ellajosyula

  3. Department of Neuropsychology, Annasawmy Mudaliar Hospital, Bangalore, India

    Jwala Narayanan

  4. Department of Clinical Neurosciences and MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, UK

    Karalyn Patterson

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  1. Ratnavalli Ellajosyula
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Correspondence to Ratnavalli Ellajosyula.

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On behalf of all the authors, the corresponding author states that there is no conflict of interest.

Ethical standard

The study has been approved by the hospital ethics committee.

Informed consent

All patients or their caregivers and controls gave informed consent according to the Declaration of Helsinki.

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Ellajosyula, R., Narayanan, J. & Patterson, K. Striking loss of second language in bilingual patients with semantic dementia. J Neurol 267, 551–560 (2020). https://doi.org/10.1007/s00415-019-09616-2

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  • DOI: https://doi.org/10.1007/s00415-019-09616-2

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