White-matter structure in the right hemisphere predicts Mandarin Chinese learning success

Journal of Neurolinguistics

Volumn 33, Issue , 2015, Pages 14-28

  Qi, Zhenghan ^a,b   Han, Michelle ^a,b   Garel, Keri ^a,b   San Chen, Ee ^a,b   Gabrieli, John D E ^a,b,c  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

Diffusion tensor imaging; Mandarin; Right hemisphere; Second language acquisition; White matter

Indexed keywords

ADULT; ARCUATE FASCICULUS; ARTICLE; DIFFUSION TENSOR IMAGING; FEMALE; FRACTIONAL ANISOTROPY; HEMISPHERIC DOMINANCE; HUMAN; HUMAN EXPERIMENT; IMAGE RECONSTRUCTION; INFERIOR LONGITUDINAL FASCICULUS; LANGUAGE ABILITY; LEARNING; LEARNING ENVIRONMENT; LEFT HEMISPHERE; MALE; MANDARIN CHINESE LEARNING; NERVE TRACT; PHONETICS; RIGHT HEMISPHERE; SUPERIOR LONGITUDINAL FASCICULUS PARIETAL BUNDLE; TASK PERFORMANCE; WHITE MATTER; WRITTEN LANGUAGE;

EID: 85027934529     PISSN: 09116044     EISSN: 18738052     Source Type: Journal    
DOI: 10.1016/j.jneuroling.2014.08.004     Document Type: Article

References (90)

1. Abutalebi J., Green D. Bilingual language production: the neurocognition of language representation and control. Journal of Neurolinguistics 2007, 20:242-275. 10.1016/j.jneuroling.2006.10.003.
2. Alexander A.L., Lee J.E., Lazar M., Field A.S. Diffusion tensor imaging of the brain. Neurotherapeutics 2007, 4(3):316-329.
3. Anwander A., Tittgemeyer M., von Cramon D.Y., Friederici A.D., Knösche T.R. Connectivity-based Parcellation of Broca's area. Cerebral Cortex (New York, N.Y.: 1991) 2007, 17(4):816-825. 10.1093/cercor/bhk034.
4. Archila-Suerte P., Zevin J., Ramos A.I., Hernandez A.E. The neural basis of non-native speech perception in bilingual children. NeuroImage 2013, 67:51-63. 10.1016/j.neuroimage.2012.10.023.
5. Basic S., Hajnsek S., Poljakovic Z., Basic M., Culic V., Zadro I. Determination of cortical language dominance using functional transcranial Doppler sonography in left-handers. Clinical Neurophysiology 2004, 115(1):154-160. 10.1016/S1388-2457(03)00281-5.
6. Baum S.R., Pell M.D. The neural bases of prosody: insights from lesion studies and neuroimaging. Aphasiology 1999, 13(8):581-608. 10.1080/026870399401957.
7. Beaulieu C. The basis of anisotropic water diffusion in the nervous system - a technical review. NMR in Biomedicine 2002, 15(7-8):435-455. 10.1002/nbm.782.
8. Bolger D.J., Perfetti C.A., Schneider W. Cross-cultural effect on the brain revisited: universal structures plus writing system variation. Human Brain Mapping 2005, 25(1):92-104. 10.1002/hbm.20124.
9. Catani M., Jones D.K., Ffytche D.H. Perisylvian language networks of the human brain. Annals of Neurology 2005, 57(1):8-16. 10.1002/ana.20319.
10. Cohen L., Dehaene S. Specialization within the ventral stream: the case for the visual word form area. NeuroImage 2004, 22(1):466-476. 10.1016/j.neuroimage.2003.12.049.
11. Crinion J.T., Green D.W., Chung R., Ali N., Grogan A., Price G.R., et al. Neuroanatomical markers of speaking Chinese. Human Brain Mapping 2009, 30(12):4108-4115. 10.1002/hbm.20832.
12. Cummine J., Boliek C.A. Understanding white matter integrity stability for bilinguals on language status and reading performance. Brain Structure & Function 2013, 218(2):595-601. 10.1007/s00429-012-0466-6.
13. D'Anselmo A., Reiterer S., Zuccarini F., Tommasi L., Brancucci A. Hemispheric asymmetries in bilinguals: tongue similarity affects lateralization of second language. Neuropsychologia 2013, 51(7):1187-1194. 10.1016/j.neuropsychologia.2013.03.016.
14. DiCiccio T.J., Efron B. Bootstrap confidence intervals. Statistical Science 1996, 11(3):189-228.
15. Dick A.S., Tremblay P. Beyond the arcuate fasciculus: consensus and controversy in the connectional anatomy of language. Brain: A Journal of Neurology 2012, 135(Pt 12):3529-3550. 10.1093/brain/aws222.
16. Dronkers N.F., Plaisant O., Iba-Zizen M.T., Cabanis E.A. Paul Broca's historic cases: high resolution MR imaging of the brains of Leborgne and Lelong. Brain: A Journal of Neurology 2007, 130(Pt 5):1432-1441. 10.1093/brain/awm042.
17. Ellmore T.M., Beauchamp M.S., Breier J.I., Slater J.D., Kalamangalam G.P., O'Neill T.J., et al. Temporal lobe white matter asymmetry and language laterality in epilepsy patients. NeuroImage 2010, 49(3):2033-2044. 10.1016/j.neuroimage.2009.10.055.
18. Epelbaum S., Pinel P., Gaillard R., Delmaire C., Perrin M., Dupont S., et al. Pure alexia as a disconnection syndrome: new diffusion imaging evidence for an old concept. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior 2008, 44(8):962-974. 10.1016/j.cortex.2008.05.003.
19. Flöel A., de Vries M.H., Scholz J., Breitenstein C., Johansen-Berg H. White matter integrity in the vicinity of Broca's area predicts grammar learning success. NeuroImage 2009, 47(4):1974-1981. 10.1016/j.neuroimage.2009.05.046.
20. Friederici A.D. Pathways to language: fiber tracts in the human brain. Trends in Cognitive Sciences 2009, 13(4):175-181. 10.1016/j.tics.2009.01.001.
21. Gandour J., Tong Y., Wong D., Talavage T., Dzemidzic M., Xu Y., et al. Hemispheric roles in the perception of speech prosody. NeuroImage 2004, 23(1):344-357. 10.1016/j.neuroimage.2004.06.004.
22. García-Pentón L., Pérez Fernández A., Iturria-Medina Y., Gillon-Dowens M., Carreiras M. Anatomical connectivity changes in the bilingual brain. NeuroImage 2014, 84:495-504. 10.1016/j.neuroimage.2013.08.064.
23. Glasser M.F., Rilling J.K. DTI tractography of the human brain's language pathways. Cerebral Cortex (New York, N.Y.: 1991) 2008, 18(11):2471-2482. 10.1093/cercor/bhn011.
24. Gu F., Zhang C., Hu A., Zhao G. Left hemisphere lateralization for lexical and acoustic pitch processing in Cantonese speakers as revealed by mismatch negativity. NeuroImage 2013, 83:637-645.
25. Halligan P.W., Fink G.R., Marshall J.C., Vallar G. Spatial cognition: evidence from visual neglect. Trends in Cognitive Sciences 2003, 7(3):125-133. 10.1016/S1364-6613(03)00032-9.
26. Hickok G., Poeppel D. Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language. Cognition 2004, 92(1-2):67-99. 10.1016/j.cognition.2003.10.011.
27. Hickok G., Poeppel D. The cortical organization of speech processing. Nature Reviews Neuroscience 2007, 8(May):393-402.
28. Hosoda C., Tanaka K., Nariai T., Honda M., Hanakawa T. Dynamic neural network reorganization associated with second language vocabulary acquisition: a multimodal imaging study. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience 2013, 33(34):13663-13672. 10.1523/JNEUROSCI.0410-13.2013.
29. Hsieh L., Gandour J., Wong D., Hutchins G.D. Functional heterogeneity of inferior frontal gyrus is shaped by linguistic experience. Brain and Language 2001, 76(3):227-252. 10.1006/brln.2000.2382.
30. Hull R., Vaid J. Bilingual language lateralization: a meta-analytic tale of two hemispheres. Neuropsychologia 2007, 45(9):1987-2008. 10.1016/j.neuropsychologia.2007.03.002.
31. Johnson J.S., Newport E.L. Critical period effects in second language learning: the influence of maturational state on the acquisition of English as a second language. Cognitive Psychology 1989, 21(1):60-99.
32. Jones D.K., Knösche T.R., Turner R. White matter integrity, fiber count, and other fallacies: the do's and don'ts of diffusion MRI. NeuroImage 2012, 10.1016/j.neuroimage.2012.06.081.
33. Kaufman A.S., Kaufman N.L. Kaufman brief intelligence test 2004, Pearson. 2nd ed.
34. Klein D., Zatorre R.J., Milner B., Zhao V. Across-linguistic PET study of tone perception in Mandarin Chinese and English speakers. NeuroImage 2001, 13(4):646-653. 10.1006/nimg.2000.0738.
35. Kuhl P.K. Early language acquisition: cracking the speech code. Nature Reviews Neuroscience 2004, 5(11):831-843. 10.1038/nrn1533.
36. Kunimatsu A., Aoki S., Masutani Y., Abe O., Hayashi N., Mori H., et al. The optimal trackability threshold of fractional anisotropy for diffusion tensor tractography of the corticospinal tract. Magnetic Resonance in Medical Sciences 2004, 3:11-17.
37. Lane L., Groisman M., Ferreira V. Don't talk about Pink Elephants!: speakers' control over leaking private information during language production. Psychological Science 2006, 17(4):273-277.
38. Leonard M.K., Brown T.T., Travis K.E., Gharapetian L., Hagler D.J., Dale A.M., et al. Spatiotemporal dynamics of bilingual word processing. NeuroImage 2010, 49(4):3286-3294. 10.1016/j.neuroimage.2009.12.009.
39. Li P., Legault J., Litcofsky K.A. Neuroplasticity as a function of second language learning: anatomical changes in the human brain. Cortex 2014, 58:301-324. 10.1016/j.cortex.2014.05.001.
40. Linck J.a., Hughes M.M., Campbell S.G., Silbert N.H., Tare M., Jackson S.R., et al. Hi-LAB: a new measure of aptitude for high-level language proficiency. Language Learning 2013, 63(3):530-566. 10.1111/lang.12011.
41. Liu L., Peng D., Ding G., Jin Z., Zhang L., Li K., et al. Dissociation in the neural basis underlying Chinese tone and vowel production. NeuroImage 2006, 29(2):515-523. 10.1016/j.neuroimage.2005.07.046.
42. Liu X. New practical Chinese reader 2010, Vol. 1. Beijing Language Culture University Press. 2nd ed.
43. López-Barroso D., Catani M., Ripollés P., Dell'acqua F., Rodríguez-Fornells A., de Diego-Balaguer R. Word learning is mediated by the left arcuate fasciculus. Proceedings of the National Academy of Sciences of the United States of America 2013, 10.1073/pnas.1301696110.
44. Lorenz M.W., Thoelen N., Loesel N., Lienerth C., Gonzalez M., Humpich M., et al. Assessment of cerebral autoregulation with transcranial Doppler sonography in poor bone windows using constant infusion of an ultrasound contrast agent. Ultrasound in Medicine & Biology 2008, 34(3):345-353. 10.1016/j.ultrasmedbio.2007.09.001.
45. Loui P., Alsop D., Schlaug G. Tone deafness: a new disconnection syndrome?. The Journal of Neuroscience[U+202F]: The Official Journal of the Society for Neuroscience 2009, 29(33):10215-10220. 10.1523/JNEUROSCI.1701-09.2009.
46. Loui P., Li H.C., Schlaug G. White matter integrity in right hemisphere predicts pitch-related grammar learning. NeuroImage 2011, 55(2):500-507. 10.1016/j.neuroimage.2010.12.022.
47. Luk G., Bialystok E., Craik F.I.M., Grady C.L. Lifelong bilingualism maintains white matter integrity in older adults. The Journal of Neuroscience[U+202F]: The Official Journal of the Society for Neuroscience 2011, 31(46):16808-16813. 10.1523/JNEUROSCI.4563-11.2011.
48. Luk G., Green D. Cognitive control for language switching in bilinguals: a quantitative meta-analysis of functional neuroimaging studies. Language and Cognitive Processes 2011, 27(10):1479-1488. 10.1080/01690965.2011.613209.Cognitive.
49. Makris N., Kennedy D.N., McInerney S., Sorensen A.G., Wang R., Caviness V.S., et al. Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, invivo, DT-MRI study. Cerebral Cortex (New York, N.Y.[U+202F]: 1991) 2005, 15(6):854-869. 10.1093/cercor/bhh186.
50. Mårtensson J., Eriksson J., Bodammer N.C., Lindgren M., Johansson M., Nyberg L., et al. Growth of language-related brain areas after foreign language learning. NeuroImage 2012, 63(1):240-244. 10.1016/j.neuroimage.2012.06.043.
51. Meyer M., Alter K., Friederici A.D., Lohmann G., von Cramon D.Y. FMRI reveals brain regions mediating slow prosodic modulations in spoken sentences. Human Brain Mapping 2002, 17(2):73-88. 10.1002/hbm.10042.
52. Mohades S.G., Struys E., Van Schuerbeek P., Mondt K., Van Den Craen P., Luypaert R. DTI reveals structural differences in white matter tracts between bilingual and monolingual children. Brain Research 2012, 1435:72-80.
53. Mosidze V.M., Mkheidze R.A., Makashvili M.A. Disorders of visuo-spatial attention in patients with unilateral brain damage. Behavioural Brain Research 1994, 65(1):121-122. 10.1016/0166-4328(94)90081-7.
54. Nelson J.R., Liu Y., Fiez J., Perfetti C.A. Assimilation and accommodation patterns in ventral occipitotemporal cortex in learning a second writing system. Human Brain Mapping 2009, 30(3):810-820. 10.1002/hbm.20551.
55. Oguz I., Farzinfar M., Matsui J., Budin F., Liu Z., Gerig G., et al. DTIPrep: quality control of diffusion-weighted images. Frontiers in Neuroinformatics 2014, 8:4. 10.3389/fninf.2014.00004.
56. Pell M.D. Recognition of prosody following unilateral brain lesion: influence of functional and structural attributes of prosodic contours. Neuropsychologia 1998, 36(8):701-715. 10.1016/S0028-3932(98)00008-6.
57. Perani D., Paulesu E., Galles N.S., Dupoux E., Dehaene S., Bettinardi V., et al. The bilingual brain proficiency and age of acquisition of the second language 1998, 1841-1852.
58. Perfetti C.A., Liu Y., Tan L.H. The lexical constituency model: some implications of research on Chinese for general theories of reading. Psychological Review 2005, 112(1):43-59.
59. Pisella L., Alahyane N., Blangero A., Thery F., Blanc S., Pelisson D. Right-hemispheric dominance for visual remapping in humans. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 2011, 366(1564):572-585. 10.1098/rstb.2010.0258.
60. Pugh K.R., Mencl W.E., Jenner A.R., Katz L., Frost S.J., Lee J.R., et al. Neurobiological studies of reading and reading disability. Journal of Communication Disorders 2001, 34(6):479-492.
61. Rauschecker A.M., Deutsch G.K., Ben-Shachar M., Schwartzman A., Perry L.M., Dougherty R.F. Reading impairment in a patient with missing arcuate fasciculus. Neuropsychologia 2009, 47(1):180-194. 10.1016/j.neuropsychologia.2008.08.011.
62. Sakai K.L. Language acquisition and brain development. Science (New York, N.Y.) 2005, 310(5749):815-819. 10.1126/science.1113530.
63. Saur D., Kreher B.W., Schnell S., Kümmerer D., Kellmeyer P., Vry M.-S., et al. Ventral and dorsal pathways for language. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(46):18035-18040. 10.1073/pnas.0805234105.
64. Saur D., Schelter B., Schnell S., Kratochvil D., Küpper H., Kellmeyer P., et al. Combining functional and anatomical connectivity reveals brain networks for auditory language comprehension. NeuroImage 2010, 49(4):3187-3197. 10.1016/j.neuroimage.2009.11.009.
65. Saygin Z.M., Norton E.S., Osher D.E., Beach S.D., Cyr A.B., Ozernov-Palchik O., et al. Tracking the roots of reading ability: white matter volume and integrity correlate with phonological awareness in prereading and early-reading kindergarten children. The Journal of Neuroscience[U+202F]: The Official Journal of the Society for Neuroscience 2013, 33(33):13251-13258. 10.1523/JNEUROSCI.4383-12.2013.
66. Schlegel A.a., Rudelson J.J., Tse P.U. White matter structure changes as adults learn a second language. Journal of Cognitive Neuroscience 2012, 24(8):1664-1670. 10.1162/jocn_a_00240.
67. Song S.K., Sun S.W., Ramsbottom M.J., Chang C., Russell J., Cross A.H. Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. NeuroImage 2002, 17:1429-1436.
68. Sun Y., Yang Y., Desroches A.S., Liu L., Peng D. The role of the ventral and dorsal pathways in reading Chinese characters and English words. Brain and Language 2011, 119(2):80-88. 10.1016/j.bandl.2011.03.012.
69. Takahashi M., Hackney D.B., Zhang G.X., Wehrli S.L., Wright A.C., O'Brien W.T. Magnetic resonance microimaging of intraaxonal water diffusion in live excised lamprey spinal cord. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:16192-16196.
70. Tan L.H., Laird A.R., Li K., Fox P.T. Neuroanatomical correlates of phonological processing of Chinese characters and alphabetic words: a meta-analysis. Human Brain Mapping 2005, 25(1):83-91. 10.1002/hbm.20134.
71. Tan L.H., Hoosain R., Peng D. Role of early Presemantic phonological code in Chinese character identification. Journal of Experimental Psychology: Learning, Memory, and Cognition 1995, 21(1):43-54.
72. Tan L.H., Chen L., Yip V., Chan A.H.D., Yang J., Gao J.H., et al. Activity levels in the left hemisphere caudate-fusiform circuit predict how well a second language will be learned. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(6):2540-2544. 10.1073/pnas.0909623108.
73. Tong Y., Gandour J., Talavage T., Wong D., Dzemidzic M., Xu Y., et al. Neural circuitry underlying sentence-level linguistic prosody. NeuroImage 2005, 28(2):417-428. 10.1016/j.neuroimage.2005.06.002.
74. Tracy D.K., Ho D.K., O'Daly O., Michalopoulou P., Lloyd L.C., Dimond E., et al. It's not what you say but the way that you say it: an fMRI study of differential lexical and non-lexical prosodic pitch processing. BMC Neuroscience 2011, 12:128.
75. Vandermosten M., Boets B., Poelmans H., Sunaert S., Wouters J., Ghesquière P. Atractography study in dyslexia: neuroanatomic correlates of orthographic, phonological and speech processing. Brain[U+202F]: A Journal of Neurology 2012, 135(Pt 3):935-948. 10.1093/brain/awr363.
76. Ventura-Campos N., Sanjuán A., González J., Palomar-García M.-Á., Rodríguez-Pujadas A., Sebastián-Gallés N., et al. Spontaneous brain activity predicts learning ability of foreign sounds. The Journal of Neuroscience 2013, 33(22):9295-9305. 10.1523/JNEUROSCI.4655-12.2013.
77. Vernooij M.W., Smits M., Wielopolski P.A., Houston G.C., Krestin G.P., van der Lugt A. Fiber density asymmetry of the arcuate fasciculus in relation to functional hemispheric language lateralization in both right- and left-handed healthy subjects: a combined fMRI and DTI study. Neuroimage 2007, 35(3):1064-1076.
78. Wahl M., Li Y.-O., Ng J., Lahue S.C., Cooper S.R., Sherr E.H., et al. Microstructural correlations of white matter tracts in the human brain. NeuroImage 2010, 51(2):531-541. 10.1016/j.neuroimage.2010.02.072.
79. Wakana S., Caprihan A., Panzenboeck M.M., Fallon J.H., Perry M., Gollub R.L., et al. Reproducibility of quantitative tractography meth- ods applied to cerebralwhite matter. Neuroimage 2007, 36:630-644.
80. Wang X.D., Wang M., Chen L. Hemispheric lateralization for early auditory processing of lexical tones: dependence on pitch level and pitch contour. Neuropsychologia 2013, 51(11):2238-2244.
81. Warrier C.M., Zatorre R.J. Right temporal cortex is critical for utilization of melodic contextual cues in a pitch constancy task. Brain[U+202F]: A Journal of Neurology 2004, 127(Pt 7):1616-1625. 10.1093/brain/awh183.
82. Wildgruber D., Pihan H., Ackermann H., Erb M., Grodd W. Dynamic brain activation during processing of emotional intonation: influence of acoustic parameters, emotional valence, and sex. NeuroImage 2002, 15(4):856-869. 10.1006/nimg.2001.0998.
83. Wong F.C.K., Chandrasekaran B., Garibaldi K., Wong P.C.M. White matter anisotropy in the ventral language pathway predicts sound-to-word learning success. The Journal of Neuroscience 2011, 31(24):8780-8785. 10.1523/JNEUROSCI.0999-11.2011.
84. Wong P.C.M. Hemispheric specialization of linguistic pitch patterns. Brain Research Bulletin 2002, 59(2):83-95. 10.1016/S0361-9230(02)00860-2.
85. Wong P.C.M., Perrachione T.K., Parrish T.B. Neural characteristics of successful and less successful speech and word learning in adults. Human Brain Mapping 2007, 28(10):995-1006. 10.1002/hbm.20330.
86. Xu Y., Gandour J., Talavage T., Wong D., Dzemidzic M., Tong Y., et al. Activation of the left planum temporale in pitch processing is shaped by language experience. Human Brain Mapping 2006, 27(2):173-183. 10.1002/hbm.20176.
87. Yeatman J.D., Dougherty R.F., Ben-Shachar M., Wandell B.A. Development of white matter and reading skills. Proceedings of the National Academy of Sciences of the United States of America 2012, 109(44):E3045-E3053. 10.1073/pnas.1206792109.
88. Yeatman J.D., Dougherty R.F., Rykhlevskaia E., Sherbondy A.J., Deutsch G.K., Wandell B.A., et al. Anatomical properties of the arcuate fasciculus predict phonological and reading skills in children. Journal of Cognitive Neuroscience 2011, 23(11):3304-3317. 10.1162/jocn_a_00061.
89. Yendiki A., Panneck P., Srinivasan P., Stevens A., Zöllei L., Augustinack J., et al. Automated probabilistic reconstruction of white-matter pathways in health and disease using an atlas of the underlying anatomy. Frontiers in Neuroinformatics 2011, 5:23. 10.3389/fninf.2011.00023.
90. Zatorre R.J., Gandour J.T. Neural specializations for speech and pitch: moving beyond the dichotomies. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 2008, 363(1493):1087-1104. 10.1098/rstb.2007.2161.