Second language learning induces grey matter volume increase in people with multiple sclerosis


Autoři: Rainer Ehling aff001;  Matthias Amprosi aff003;  Benjamin Kremmel aff004;  Gabriel Bsteh aff003;  Kathrin Eberharter aff004;  Matthias Zehentner aff004;  Ruth Steiger aff005;  Noora Tuovinen aff003;  Elke R. Gizewski aff005;  Thomas Benke aff003;  Thomas Berger aff003;  Carol Spöttl aff004;  Christian Brenneis aff001;  Christoph Scherfler aff003
Působiště autorů: Department of Neurology, Clinic for Rehabilitation Münster, Münster, Austria aff001;  Karl Landsteiner Institut für Interdisziplinäre Forschung am Reha Zentrum Münster, Münster, Austria aff002;  Department of Neurology, Medical University of Innsbruck, Innsbruck, Austria aff003;  Language Testing Research Group Innsbruck, Department for Subject Specific Education, University of Innsbruck, Innsbruck, Austria aff004;  Department of Neuroradiology, Medical University of Innsbruck, Innsbruck, Austria aff005;  Neuroimaging Research Core Facility, Medical University Innsbruck, Innsbruck, Austria aff006
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0226525

Souhrn

Background

Grey matter volume (GMV) decline is a frequent finding in multiple sclerosis (MS), the most common chronic neurological disease in young adults. Increases of GMV were detected in language related brain regions following second language (L2) learning in healthy adults. Effects of L2 learning in people with MS (pwMS) have not been investigated so far.

Methods

This study prospectively evaluated the potential of an eight-week L2 training on grey matter plasticity measured by 3T-MRI, L2 proficiency and health-related quality of life (HRQoL) in people with relapsing-remitting MS (pwMS, n = 11) and healthy, sex- and age-matched controls (HCs; n = 12).

Results

Categorical voxel-based analysis revealed significantly less GMV bilaterally of the insula extending to the temporal pole in pwMS at baseline. Following L2 training, significant increases of GMV were evident in the right hippocampus, parahippocampus and putamen of pwMS and in the left insula of HCs. L2 training resulted in significant improvements of listening comprehension, speaking fluency and vocabulary knowledge in both pwMS and HCs. GMV increases of right hippocampus and parahippocampus significantly correlated with vocabulary knowledge gain and L2 learning was associated with a significant increase of HRQoL in pwMS.

Conclusion

Our findings demonstrate distinct patterns of GMV increases of language related brain regions in pwMS and HCs and indicate disease-related compensatory cortical and subcortical plasticity to acquire L2 proficiency in pwMS.

Klíčová slova:

Central nervous system – Cognitive impairment – Human learning – Language – Language acquisition – Learning – Magnetic resonance imaging – Multiple sclerosis


Zdroje

1. Thompson AJ, Baranzini SE, Geurts J, Hemmer B, Ciccarelli O. Multiple sclerosis. Lancet. 2018; 391: 1622–1636. doi: 10.1016/S0140-6736(18)30481-1 29576504

2. Calabrese M, Magliozzi R, Ciccarelli O, Geurts JJ, Reynolds R, Martin R. Exploring the origins of grey matter damage in multiple sclerosis. Nat Rev Neurosci. 2015; 16: 147–158. doi: 10.1038/nrn3900 25697158

3. Audoin B, Davies GR, Finisku L, Chard DT, Thompson AJ, Miller DH. Localization of grey matter atrophy in early RRMS: a longitudinal study. J Neurol. 2006; 253: 1495–1501. doi: 10.1007/s00415-006-0264-2 17093899

4. Chard D, Miller D. Grey matter pathology in clinically early multiple sclerosis: evidence from magnetic resonance imaging. J Neurol Sci. 2009; 282: 5–11. doi: 10.1016/j.jns.2009.01.012 19201002

5. Rao S, Leo G, Bernardin L, Unverzagt F. Cognitive dysfunction in multiple sclerosis: frequency, patterns, and predictions. Neurology. 1991; 41: 685–691. doi: 10.1212/wnl.41.5.685 2027484

6. Chiaravalloti ND, DeLuca J. Cognitive impairment in multiple sclerosis. Lancet Neurol. 2008; 7: 1139–1151. doi: 10.1016/S1474-4422(08)70259-X 19007738

7. Sumowski JF, Benedict R, Enzinger C, Filippi M, Geurts JJ, Hamalainen P, et al. Cognition in multiple sclerosis: State of the field and priorities for the future. Neurology. 2018; 90: 278–288. doi: 10.1212/WNL.0000000000004977 29343470

8. Achiron A, Barak Y. Cognitive changes in early MS: a call for a common framework. J Neurol Sci. 2006; 245: 47–51. doi: 10.1016/j.jns.2005.05.019 16635495

9. Amato MP, Portaccio E, Goretti B, Zipoli V, Battaglini M, Bartolozzi ML, et al. Association of neocortical volume changes with cognitive deterioration in relapsing-remitting multiple sclerosis. Arch Neurol. 2007; 64: 1157–1161. doi: 10.1001/archneur.64.8.1157 17698706

10. Roosendaal SD, Moraal B, Pouwels PJ, Vrenken H, Castelijns JA, Barkhof F, et al. Accumulation of cortical lesions in MS: relation with cognitive impairment. Mult Scler. 2009; 15: 708–714. doi: 10.1177/1352458509102907 19435749

11. MacKenzie-Graham A, Kurth F, Itoh Y, Wang HJ, Montag MJ, Elashoff R, et al. Disability-Specific Atlases of Gray Matter Loss in Relapsing-Remitting Multiple Sclerosis. JAMA Neurol 2016; 73: 944–953. doi: 10.1001/jamaneurol.2016.0966 27294295

12. Preziosa P, Rocca MA, Pagani E, Stromillo ML, Enzinger C, Gallo A, et al. Structural MRI correlates of cognitive impairment in patients with multiple sclerosis: A Multicenter Study. Hum Brain Mapp. 2016; 37: 1627–1644. doi: 10.1002/hbm.23125 26833969

13. Matías-Guiu JA, Cortés-Martínez A, Montero P, Pytel V, Moreno-Ramos T, Jorquera M, et al. Identification of Cortical and Subcortical Correlates of Cognitive Performance in Multiple Sclerosis Using Voxel-Based Morphometry. Front Neurol. 2018; 9: 920. doi: 10.3389/fneur.2018.00920 30420834

14. Osterhout L, Poliakov A, Inoue K, McLaughlin J, Valentine G, Pitkanen I, et al. Second-language learning and changes in the brain. J Neurolinguistics. 2008; 21: 509–521. doi: 10.1016/j.jneuroling.2008.01.001 19079740

15. Mårtensson J, Eriksson J, Bodammer NC, Lindgren M, Johansson M, Nyberg L, et al. Growth of language-related brain areas after foreign language learning. Neuroimage. 2012; 63: 240–244. doi: 10.1016/j.neuroimage.2012.06.043 22750568

16. Stein M, Federspiel A, Koenig T, Wirth M, Strik W, Wiest R, et al. Structural plasticity in the language system related to increased second language proficiency. Cortex. 2012; 48: 458–465. doi: 10.1016/j.cortex.2010.10.007 21106192

17. Antoniou M, Wright SM. Uncovering the Mechanisms Responsible for Why Language Learning May Promote Healthy Cognitive Aging. Front Psychol. 2017; 8: 2217. doi: 10.3389/fpsyg.2017.02217 29326636

18. Bartolotti J, Bradley K, Hernandez AE, Marian V. Neural signatures of second language learning and control. Neuropsychologia. 2017; 98: 130–138. doi: 10.1016/j.neuropsychologia.2016.04.007 27068064

19. Garbin G, Sanjuan A, Forn C, Bustamante JC, Rodriguez-Pujadas A, Belloch V, et al. Bridging language and attention: brain basis of the impact of bilingualism on cognitive control. Neuroimage. 2010; 53: 1272–1278. doi: 10.1016/j.neuroimage.2010.05.078 20558314

20. Ljungberg JK, Hansson P, Andrés P, Josefsson M, Nilsson LG. A longitudinal study of memory advantages in bilinguals. PLoS One. 2013; 8: e73029. doi: 10.1371/journal.pone.0073029 24023803

21. Bialystok E, Craik FI, Freedman M. Bilingualism as a protection against the onset of symptoms of dementia. Neuropsychologia. 2007; 45: 459–464. doi: 10.1016/j.neuropsychologia.2006.10.009 17125807

22. Council of Europe. Common European Framework of Reference for Languages: Learning, Teaching, Assessment. Strasbourg: Language Policy Unit. 2001. Available from: https://www.coe.int/en/web/common-european-framework-reference-languages (accessed 5 August 2019).

23. Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol. 2011; 69: 292–302. doi: 10.1002/ana.22366 21387374

24. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology. 1983; 33: 1444–1452. doi: 10.1212/wnl.33.11.1444 6685237

25. Scherer P, Baum K, Bauer H, Göhler H, Miltenburger C. Normalization of the Brief Repeatable Battery of Neuropsychological tests (BRB-N) for German-speaking regions. Application in relapsing-remitting and secondary progressive multiple sclerosis patients. Nervenarzt. 2004; 75: 984–990. doi: 10.1007/s00115-004-1729-0 15118827

26. Sepulcre J, Vanotti S, Hernández R, Sandoval G, Cáceres F, Garcea O. Cognitive impairment in patients with multiple sclerosis using the Brief Repeatable Battery-Neuropsychology test. Mult Scler. 2006; 12: 187–195. doi: 10.1191/1352458506ms1258oa 16629422

27. Flachenecker P, Müller G, König H, Meissner H, Toyka KV, Rieckmann P. "Fatigue" in multiple sclerosis. Development and validation of the "Würzburger Fatigue Inventory for MS". Nervenarzt. 2006; 77: 165–174. doi: 10.1007/s00115-005-1990-x 16160812

28. O’Sullivan B. Aptis Test Development Approach. British Council. 2015. Available from: https://www.britishcouncil.org/sites/default/files/tech_001_barry_osullivan_aptis_test_-_v5_0.pdf (accessed 5 August 2019).

29. British Council. The United Kingdom's international organisation for cultural relations and educational opportunities 2019. Available from: https://www.britishcouncil.org/exam/aptis (accessed 28 September 2019).

30. De Jong NH, Groenhout R, Schoonen R, Hulstijn JH. Second language fluency: Speaking style or proficiency? Correcting measures of second language fluency for first language behavior. Applied Psycholinguistics. 2015; 36: 223–243.

31. Iwashita N, Brown A, McNamara T, O’Hagan S. Assessed Levels of Second Language Speaking Proficiency: How Distinct? Applied Linguistics. 2008; 29: 24–49.

32. De Jong NH, Wempe T. Praat script to detect syllable nuclei and measure speech rate automatically, Behavior Research Methods. 2009; 41: 385–390. doi: 10.3758/BRM.41.2.385 19363178

33. Boersma P, Weenink D. Praat: doing phonetics by computer [Computer program] 2019. Version 6.1.04. Available from: http://www.praat.org/ (accessed 28 September 2019).

34. Wesche MB, Paribakht TS. Assessing second language vocabulary knowledge: Depth vs. breadth. Canadian Modern Language Review. 1996; 53: 13–40.

35. Morfeld M, Kirchberger I, Bullinger M. SF-36 Fragebogen zum Gesundheitszustand. German Version of the Short Form-36 Health Survey. 2011. www.hogrefe.de

36. Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM. FSL. Neuroimage. 2012; 62: 782–790. doi: 10.1016/j.neuroimage.2011.09.015 21979382

37. Schmidt P, Gaser C, Arsic M, Buck D, Förschler A, Berthele A. An automated tool for detection of FLAIR-hyperintense white-matter lesions in Multiple Sclerosis. Neuroimage. 2012; 59: 3774–3783. doi: 10.1016/j.neuroimage.2011.11.032 22119648

38. Friston KJ, Ashburner J, Frith CD, Poline JB, Heather JD, Frackowiak RSJ. Spatial Registration and Normalization of Images. Hum Brain Mapp. 1995; 2: 165–189.

39. Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage. 2007; 38: 95–113. doi: 10.1016/j.neuroimage.2007.07.007 17761438

40. Mechelli A, Crinion JT, Noppeney U, O'Doherty J, Ashburner J, Frackowiak RS, et al. Neurolinguistics: structural plasticity in the bilingual brain. Nature. 2004; 431: 757. doi: 10.1038/431757a 15483594

41. Hosoda C, Tanaka K, Nariai T, Honda M, Hanakawa T. Dynamic neural network reorganization associated with second language vocabulary acquisition: a multimodal imaging study. J Neurosci. 2013; 33: 13663–13672. doi: 10.1523/JNEUROSCI.0410-13.2013 23966688

42. Klein D, Mok K, Chen JK, Watkins KE. Age of language learning shapes brain structure: a cortical thickness study of bilingual and monolingual individuals. Brain Lang. 2014; 131: 20–24. doi: 10.1016/j.bandl.2013.05.014 23819901

43. Dalton CM, Chard DT, Davies GR, Miszkiel KA, Altmann DR, Fernando K, et al. Early development of multiple sclerosis is associated with progressive grey matter atrophy in patients presenting with clinically isolated syndromes. Brain. 2004; 127: 1101–1107. doi: 10.1093/brain/awh126 14998914

44. Audoin B, Davies GR, Finisku L, Chard DT, Thompson AJ, Miller DH. Localization of grey matter atrophy in early RRMS: a longitudinal study. J Neurol. 2006; 253: 1495–1501. doi: 10.1007/s00415-006-0264-2 17093899

45. Henry RG, Shieh M, Okuda DT, Evangelista A, Gorno-Tempini ML, Pelletier D. Regional grey matter atrophy in clinically isolated syndromes at presentation. J Neurol Neurosurg Psychiatry. 2008; 79: 1236–1244. doi: 10.1136/jnnp.2007.134825 18469033

46. Bellander M, Berggren R, Mårtensson J, Brehmer Y, Wenger E, Li TQ, et al. Behavioral correlates of changes in hippocampal gray matter structure during acquisition of foreign vocabulary. Neuroimage. 2016; 131: 205–213. doi: 10.1016/j.neuroimage.2015.10.020 26477659

47. Breitenstein C, Jansen A, Deppe M, Foerster AF, Sommer J, Wolbers T, et al. Hippocampus activity differentiates good from poor learners of a novel lexicon. Neuroimage. 2005; 25: 958–968. doi: 10.1016/j.neuroimage.2004.12.019 15808996

48. Draganski B, Gaser C, Kempermann G, Kuhn HG, Winkler J, Büchel C, et al. Temporal and spatial dynamics of brain structure changes during extensive learning. J Neurosci. 2006; 26: 6314–6317. doi: 10.1523/JNEUROSCI.4628-05.2006 16763039

49. Vigneau M, Beaucousin V, Hervé PY, Jobard G, Petit L, Crivello F, et al. What is right-hemisphere contribution to phonological, lexico-semantic, and sentence processing? Insights from a meta-analysis. Neuroimage. 2011; 54: 577–593. doi: 10.1016/j.neuroimage.2010.07.036 20656040

50. Viñas-Guasch N, Wu YJ. The role of the putamen in language: a meta-analytic connectivity modeling study. Brain Struct Funct. 2017; 222: 3991–4004. doi: 10.1007/s00429-017-1450-y 28585051

51. Hosoda C, Tanaka K, Nariai T, Honda M, Hanakawa T. Dynamic neural network reorganization associated with second language vocabulary acquisition: a multimodal imaging study. J Neurosci. 2013; 33: 13663–13672. doi: 10.1523/JNEUROSCI.0410-13.2013 23966688

52. Hervais-Adelman A, Moser-Mercer B, Michel CM, Golestani N. fMRI of Simultaneous Interpretation Reveals the Neural Basis of Extreme Language Control. Cereb Cortex. 2015; 25: 4727–4739. doi: 10.1093/cercor/bhu158 25037924

53. Calabria M, Costa A, Green DW, Abutalebi J. Neural basis of bilingual language control. Ann N Y Acad Sci. 2018; Jun 19. doi: 10.1111/nyas.13879 (Epub ahead of print). 29917244

54. Forn C, Rocca MA, Valsasina P, Boscá I, Casanova B, Sanjuan A, et al. Functional magnetic resonance imaging correlates of cognitive performance in patients with a clinically isolated syndrome suggestive of multiple sclerosis at presentation: an activation and connectivity study. Mult Scler. 2012; 18: 153–163. doi: 10.1177/1352458511417744 21828200

55. Chiaravalloti ND, Genova HM, DeLuca J. Cognitive rehabilitation in multiple sclerosis: the role of plasticity. Front Neurol. 2015; 6: 67. doi: 10.3389/fneur.2015.00067 25883585

56. Heiss WD, Thiel A, Kessler J, Herholz K. Disturbance and recovery of language function: correlates in PET activation studies. Neuroimage. 2003; 20 Suppl 1: 42–49.

57. Grzegorski T, Losy J. Cognitive impairment in multiple sclerosis—a review of current knowledge and recent research. Rev Neurosci. 2017; 28: 845–860. doi: 10.1515/revneuro-2017-0011 28787275

58. Sumowski JF, Rocca MA, Leavitt VM, Dackovic J, Mesaros S, Drulovic J, et al. Brain reserve and cognitive reserve protect against cognitive decline over 4.5 years in MS. Neurology. 2014; 82: 1776–1783. doi: 10.1212/WNL.0000000000000433 24748670

59. Cereda C, Ghika J, Maeder P, Bogousslavsky J. Strokes restricted to the insular cortex. Neurology. 2002; 59: 1950–1955. 12499489

60. Oh A, Duerden EG, Pang EW. The role of the insula in speech and language processing. Brain Lang. 2014; 135: 96–103. doi: 10.1016/j.bandl.2014.06.003 25016092

61. Pagani E, Rocca MA, De Meo E, Horsfield MA, Colombo B, Rodegher M, et al. Structural connectivity in multiple sclerosis and modeling of disconnection. Mult Scler. 2019; 1352458518820759. doi: 10.1177/1352458518820759 30625050

62. Nortvedt MW, Riise T, Myhr KM, Nyland HI. Quality of life in multiple sclerosis: measuring the disease effects more broadly. Neurology. 1999; 53: 1098–1103. doi: 10.1212/wnl.53.5.1098 10496273

63. Hickok G, Poeppel D. The cortical organization of speech processing. Nat Rev Neurosci. 2007; 8: 393–402. doi: 10.1038/nrn2113 17431404

64. Li P, Legault J, Litcofsky KA. Neuroplasticity as a function of second language learning: anatomical changes in the human brain. Cortex. 2014; 58: 301–324. doi: 10.1016/j.cortex.2014.05.001 24996640


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