Investigating the contribution of ventral-lexical and dorsal-sublexical pathways during reading in bilinguals

Frontiers in Human Neuroscience

Volumn 8, Issue JULY, 2014, Pages

  Bakhtiari, Reyhaneh ^a   Boliek, Carol ^a   Cummine, Jacqueline ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Bilingualism; Dorsal sublexical; DTI; Reading; Tractography; Ventral lexical

Indexed keywords

ADULT; ARCUATE FASCICULUS; ARTICLE; BILINGUALISM; CHINESE; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; ENGLISH AS A SECOND LANGUAGE; FEMALE; HUMAN; HUMAN EXPERIMENT; INFERIOR LONGITUDINAL BUNDLE; LEFT HEMISPHERE; MALE; NERVE TRACT; NORMAL HUMAN; REACTION TIME; READING; RIGHT HEMISPHERE; SUPERIOR LONGITUDINAL BUNDLE; TASK PERFORMANCE; UNCINATE FASCICULUS; WHITE MATTER;

EID: 84904297897     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00507     Document Type: Article

References (66)

1. Abutalebi, J., Della Rosa, P. A., Gonzaga, A. K. C., Keim, R., Costa, A., and Perani, D. (2013). The role of the left putamen in multilingual language production. Brain Lang. 125, 307-315. doi: 10.1016/j.bandl.2012.03.009
2. Agosta, F., Henry, R. G., Migliaccio, R., Neuhaus, J., Miller, B. L., Dronkers, N. F., et al. (2010). Language networks in semantic dementia. Brain 133(pt 1), 286-299. doi: 10.1093/brain/awp233
3. Basser, P. J., and Jones, D. K. (2002). Diffusion-tensor MRI: theory, experimental design and data analysis - a technical review. NMR Biomed. 15, 456-467. doi: 10.1002/nbm.783
4. Basser, P. J., Pajevic, S., Pierpaoli, C., Duda, J., and Aldroubi, A. (2000). In vivo fiber tractography using DT-MRI data. Magn. Reson. Med. 44, 625-632. doi: 10.1002/1522-2594(200010)44:4<625::AID-MRM17>3.0.C0;2-0
5. Basser, P. J., and Pierpaoli, C. (1996). Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J. Magn. Reson. B 111, 209-219. doi: 10.1006/jmrb.1996.0086
6. Basser, P. J., and Pierpaoli, C. (2011). Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J. Magn. Reson. B 213, 560-570. doi: 10.1016/j.jmr.2011.09.022
7. Beaulieu, C. (2002). The basis of anisotropic water diffusion in the nervous system - a technical review. NMR Biomed. 15, 435-455. doi: 10.1002/nbm.782
8. Ben-Shachar, M., Dougherty, R. F., and Wandell, B. A. (2007). White matter pathways in reading. Curr. Opin. Neurobiol. 17, 258-270. doi: 10.1016/j.conb.2007.03.006
9. Binder, J. R., Desai, R. H., Graves, W. W., and Conant, L. L. (2009). Where is the semantic system? a critical review and meta-analysis of 120 functional neuroimaging studies. Cereb. Cortex 19, 2767-96. doi: 10.1093/cercor/bhp055
10. Borowsky, R., Cummine, J., Owen, W. J., Friesen, C. K., Shih, F., and Sarty, G. E. (2006). FMRI of ventral and dorsal processing streams in basic reading processes: insular sensitivity to phonology. Brain Topogr. 18, 233-239. doi: 10.1007/s10548-006-0001-2
11. Borowsky, R., Esopenko, C., Cummine, J., and Sarty, G.E. (2007).Neural representations of visual words and objects: a functional MRI study on the modularity of reading and object processing. Brain Topogr. 20, 89-96. doi: 10.1007/s10548- 007-0034-1
12. Catani, M., Howard, R. J., Pajevic, S., and Jones, D. K. (2002). Virtual in vivo interactive dissection of white matter fasciculi in the human brain. Neuroimage 17, 77-94. doi: 10.1006/nimg.2002.1136
13. Cohen, L., Dehaene, S., Vinckier, F., Jobert, A., and Montavont, A. (2008). Reading normal and degraded words: contribution of the dorsal and ven- tralvisual pathways. Neuroimage 40, 353-366. doi: 10.1016/j.neuroimage.2007.11.036
14. Conturo, T. E., Lori, N. F., Cull, T. S., Akbudak, E., Snyder, A. Z., Shimony, J. S., et al. (1999). Tracking neuronal fiber pathways in the living human brain. Proc. Natl. Acad. Sci. U.S.A. 96, 10422-10427. doi: 10.1073/pnas.96.18.10422
15. Cummine, J., and Boliek, C. A. (2013). Understanding white matter integrity stability for bilinguals on language status and reading performance. Brain Struct. Funct. 218, 595-601. doi: 10.1007/s00429-012-0466-6
16. Cummine, J., Dai, W., Borowsky, R., Gould, L., Rollans, C., and Boliek, C. (2013). Investigating the ventral-lexical, dorsal-sublexical model of basic reading processes using diffusion tensor imaging. Brain Struct. Funct. doi: 10.1007/s00429- 013-0666-8. [Epub ahead ofprint].
17. Friederici, A. D. (2009). Pathways to language: fiber tracts in the human brain. Trends Cogn. Sci. 13, 175-181. doi: 10.1016/j.tics.2009.01.001
18. Garcia-Penton, L., Perez Fernandez, A., Iturria-Medina, Y., Gillon-Dowens, M., and Carreiras, M. (2014). Anatomical connectivity changes in the bilingual brain. Neuroimage 84, 495-504. doi: 10.1016/j.neuroimage.2013.08.064
19. Gold, B. T., Johnson, N. F., and Powell, D. K. (2013). Lifelong bilingualism contributes to cognitive reserve against white matter integrity declines in aging. Neuropsychologia 51, 2841-2846. doi: 10.1016/j.neuropsychologia.2013.09.037
20. Grossman, M., McMillan, C., Moore, P., Ding, L., Glosser, G., Work, M., et al. (2004). What's in a name: voxel-based morphometric analyses of MRI and naming difficulty in Alzheimer's disease, frontotemporal dementia and corticobasal degeneration. Brain 127(pt 3), 628-649. doi: 10.1093/brain/awh075
21. Jobard, G., Crivello, F., and Tzourio-Mazoyer, N. (2003). Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies. Neuroimage 20, 693-712. doi: 10.1016/S1053-8119(03)00343-4
22. Jones, P. O., Green, D. W., Grogan, A., Pliatsikas, C., Filippopolitis, K., Ali, N., et al. (2012). Where, when andwhybrain activation differs for bilinguals and mono- linguals during picture naming and reading aloud. Cereb. Cortex 22, 892-902. doi: 10.1093/cercor/bhr161
23. Kovelman, I., Baker, S. A., and Petitto, L.-A. (2008a). Bilingual and monolingual brains compared: a functional magnetic resonance imaging investigation of syntactic processing and a possible "Neural Signature' of Bilingualism. J. Cogn. Neurosci. 20, 153-169. doi: 10.1162/jocn.2008.20.1.153
24. Kovelman, I., Shalinsky, M. H., Berens, M. S., and Petitto, L.-A. (2008b). Shining new light on the brain's "bilingual signature": a functional Near Infrared Spectroscopy investigation of semantic processing. Neuroimage 39, 1457-1471. doi: 10.1016/j.neuroimage.2007.10.017
25. Le Bihan, D., Mangin, J. F., Poupon, C., Clark, C. A., Pappata, S., Molko, N., et al. (2001). Diffusion tensor imaging: concepts and applications. J. Magn. Reson. Imaging 13, 534-46. doi: 10.1002/jmri.1076
26. Levy, J., Pernet, C., Treserras, S., Boulanouar, K., Aubry, F., Demonet, J.-F., et al. (2009). Testing for the dual-route cascade reading model in the brain: an fMRI effective connectivity account of an efficient reading style. PLoS ONE 4:e6675. doi: 10.1371/journal.pone.0006675
27. Lopez-Barroso, D., de Diego-Balaguer, R., Cunillera, T., Camara, E., Munte, T. F., and Rodriguez-Fornells, A. (2011). Language learning under working memory constraints correlates with microstructural differences in the ventral language pathway. Cereb. Cortex 21, 2742-2750. doi: 10.1093/cercor/bhr064
28. Luk, G., Bialystok, E., Craik, F. I. M., and Grady, C. L. (2011). Lifelong bilingualism maintains white matter integrity in older adults. J. Neurosci. 31, 16808-16813. doi: 10.1523/JNEUROSCI.4563-11.2011
29. Lupker, S. J., Brown, P., and Colombo, L. (1997). Strategic control in anaming task: changing routes or changing deadlines? J. Exp. Psychol. Learn. Mem. Cogn. 23, 570-590. doi: 10.1037/0278-7393.23.3.570
30. Marchina, S., Zhu, L. L., Norton, A., Zipse, L., Wan, C. Y., and Schlaug, G. (2011). Impairment of speech production predicted by lesion load of the left arcuate fasciculus. Stroke 42, 2251-2256. doi: 10.1161/STR0KEAHA.110.606103
31. Mechelli, A., Crinion, J. T., Long, S., Friston, K. J., Lambon Ralph, M. A., Patterson, K., et al. (2005). Dissociating reading processes on the basis of neuronal interactions. J. Cogn. Neurosci. 17, 1753-1765. doi: 10.1162/089892905774589190
32. Mechelli, A., Crinion, J. T., Noppeney, U., O'Doherty, J., Ashburner, J., Frackowiak, R. S., et al. (2004). Neurolinguistics: structural plasticity in the bilingual brain. Nature 431, 757. doi: 10.1038/431757a
33. Mohades, S. G., Struys, E., Van Schuerbeek, P., Mondt, K., Van De Craen, P., and Luypaert, R. (2012). DTI reveals structural differences in white matter tracts between bilingual and monolingual children. Brain Res. 1435, 72-80. doi: 10.1016/j.brainres.2011.12.005
34. Monsell, S., Patterson, K. E., Graham, A., Hughes, C. H., and Milroy, R. (1992). Lexical and sublexical translation of spelling to sound: strategic anticipation of lexical status. J. Exp. Psychol. Learn. Mem. Cogn. 18, 452-467. doi: 10.1037/02787393.18.3.452
35. Mori, M., Crain, B. J., Chacko, V. P., and Van Zijl, P. C. M. (1999). Threedimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann. Neurol. 45, 265-269.
36. Mukherjee, P., Berman, J. I., Chung, S. W., Hess, C. P., and Henry, R. G. (2008). Diffusion tensor MR imaging and fiber tractography: theoretic underpinnings. Am. J. Neuroradiol. 29, 632-641. doi: 10.3174/ajnr.A1051
37. Norris, D. G. (2001). The effects of microscopic tissue parameters on the diffusion weighted magnetic resonance imaging experiment. NMR Biomed. 14, 77-93. doi: 10.1002/nbm.682
38. Papagno, C., Miracapillo, C., Casarotti, A., Romero Lauro, L. J., Castellano, A., Falini, A., et al. (2011). What is the role of the uncinate fasciculus? Surgical removal and proper name retrieval. Brain 134(pt 2), 405-414. doi: 10.1093/brain/awq283
39. Pierpaoli, C., Barnett, A., Pajevic, S., Chen, R., Penix, L. R., Virta, A., et al. (2001). Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage 13(6 pt 1), 1174-1185. doi: 10.1006/nimg.2001.0765
40. Price, C. J. (2010). The anatomy of language: a review of 100 fMRI studies published in 2009. Ann. N.Y. Acad. Sci. 1191, 62-88. doi: 10.1111/j.1749- 6632.2010.05444.x
41. Pugh, K. R., Mencl, W. E., Jenner, A. R., Katz, L., Frost, S. J., Lee, J. R., et al. (2000). Functional neuroimaging studies of reading and reading disability (developmental dyslexia). Ment. Retard. Dev. Disabil. Res. Rev. 6, 207-213. doi: 10.1002/1098-2779(2000)6:3 <207::AID-MRDD8>3.0.C0;2-P
42. Pugh, K. R., Mencl, W. E., Jenner, A. R., Katz, L., Frost, S. J., Lee, J. R., et al. (2001). Neurobiological studies of reading and reading disability. J. Commun. Disord. 34, 479-92. doi: 10.1016/S0021-9924(01)00060-0
43. Raboyeau, G., Marie, N., Balduyck, S., Gros, H., Demonet, J.-F., and Cardebat, D. (2004). Lexical learning of the English language: a PET study in healthy French subjects. Neuroimage 22, 1808-1818. doi: 10.1016/j.neuroimage.2004.05.011
44. Rauschecker, A. M., Deutsch, G. K., Ben-Shachar, M., Schwartzman, A., Perry, L. M., and Dougherty, R. F. (2009). Reading impairment in a patient with missing arcuate fasciculus. Neuropsychologia 47, 180-194. doi: 10.1016/j.neuropsychologia.2008.08.011
45. Rodriguez-Fornells, A., Rotte, M., Heinze, H.-J., Nosselt, T., and Munte, T. F. (2002). Brain potential and functional MRI evidence for how to handle two languages with one brain. Nature 415, 1026-1029. doi: 10.1038/4151026a
46. Rodriguez-Fornells, A., van der Lugt, A., Rotte, M., Britti, B., Heinze, H.-J., and Munte, T. F. (2005). Second language interferes with word production in fluent bilinguals: brain potential and functional imaging evidence. J. Cogn. Neurosci. 17, 422-433. doi: 10.1162/0898929053279559
47. Rolheiser, T., Stamatakis, E. A., and Tyler, L. K. (2011). Dynamic processing in the human language system: synergy between the arcuate fascicle and extreme capsule. J. Neurosci. 31, 16949-16957. doi: 10.1523/JNEUROSCI.2725- 11.2011
48. Saur, D., Kreher, B. W., Schnell, S., Kummerer, D., Kellmeyer, P., Vry, M.-S., et al. (2008). Ventral and dorsal pathways for language. Proc. Natl. Acad. Sci. U.S.A. 105, 18035-18040. doi: 10.1073/pnas.0805234105
49. Saur, D., Schelter, B., Schnell, S., Kratochvil, D., Kupper, H., Kellmeyer, P., et al. (2010). Combining functional and anatomical connectivity reveals brain networks for auditory language comprehension. Neuroimage 49, 3187-3197. doi: 10.1016/j.neuroimage.2009.11.009
50. Saygin, Z. M., Norton, E. S., Osher, D. E., Beach, S. D., Cyr, A. B., Ozernov-Palchik, O., et al. (2013). Tracking the roots of reading ability: white matter volume and integrity correlate with phonological awareness in prereading and early-reading kindergarten children. J. Neurosci. 33, 13251-13258. doi: 10.1523/JNEUROSCI.4383-12.2013
51. Scantlebury, N., Cunningham, T., Dockstader, C., Laughlin, S., Gaetz, W., Rockel, C., et al. (2014). Relations between white matter maturation and reaction time in childhood. J. Int. Neuropsychol. Soc. JINS 20, 99-112. doi: 10.1017/S1355617713001148
52. Schmahmann, J. D., Pandya, D. N., Wang, R., Dai, G., D'Arceuil, H. E., de Crespigny, A. J., et al. (2007). Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 130(pt 3), 630-653. doi: 10.1093/brain/awl359
53. Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T.E., Mackay C. E., et al. (2006). Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31, 1487-1505. doi: 10.1016/j.neuroimage.2006.02.024
54. Song, S.-K., Yoshino, J., Le, T. Q., Lin, S.-J., Sun, S.-W., Cross, A. H., et al. (2005). Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26, 132-140. doi: 10.1016/j.neuroimage.2005.01.028
55. Steinbrink, C., Vogt, K., Kastrup, A., Muller, H.-P., Juengling, F. D., Kassubek, J., et al. (2008). The contribution of white and gray matter differences to developmental dyslexia: insights from DTI and VBM at 3.0 T. Neuropsychologia 46, 3170-3178. doi: 10.1016/j.neuropsychologia.2008.07.015
56. Tan, L. H., Spinks, J. A., Feng, C. M., Siok, W. T., Perfetti, C. A., Xiong, J., et al. (2003). Neural systems of second language reading are shaped by native language. Hum. Brain Mapp. 18, 158-166. doi: 10.1002/hbm.10089
57. Vandermosten, M., Boets, B., Poelmans, H., Sunaert, S., Wouters, J., and Ghesquiere, P. (2012a). A tractography study in dyslexia: neuroanatomic correlates of orthographic, phonological and speech processing. Brain 135(pt 3), 935-948. doi: 10.1093/brain/awr363
58. Vandermosten, M., Boets, B., Wouters, J., and Ghesquiere, P. (2012b). A qualitative and quantitative review of diffusion tensor imaging studies in reading and dyslexia. Neurosci. Biobehav. Rev. 36, 1532-1552. doi: 10.1016/j.neubiorev.2012.04.002
59. Wakana, S., Caprihan, A., Panzenboeck, M. M., Fallon, J. H., Perry, M., Gollub, R. L., et al. (2007). Reproducibility of quantitative tractography methods applied to cerebral white matter. Neuroimage 36, 630-644. doi: 10.1016/j.neuroimage.2007.02.049
60. Wakana, S., Jiang, H., Nagae-Poetscher, L. M., van Zijl, P. C. M., and Mori, S. (2004). Fiber tract-based atlas of human white matter anatomy. Radiology 230, 77-87. doi: 10.1148/radiol.2301021640
61. Wilson, S. M., Galantucci, S., Tartaglia, M. C., Rising, K., Patterson, D. K., Henry, M. L., et al. (2011). Syntactic processing depends on dorsal language tracts. Neuron 72, 397-403. doi: 10.1016/j.neuron.2011.09.014
62. Yeatman, J. D., Dougherty, R. F., Rykhlevskaia, E., Sherbondy, A. J., Deutsch, G. K., Wandell, B. A., et al. (2011). Anatomical properties of the arcuate fasciculus predict phonological and reading skills in children. J. Cogn. Neurosci. 23, 3304-3317. doi: 10.1162/jocn_a_00061
63. Zisner, A., and Phillips, O. (2009a). Identifying the Arcuate Fasciculus (AF) in DTIStudio Using a Multiple ROI Approach. Available online at: http://www.loni.ucla.edu/~narr/protocol.php?q=dti_af (Accessed January 06, 2014).
64. Zisner, A., and Phillips, O. (2009b). Identifying the Inferior Longitudinal Fasciculus in DTIStudio Using a Multiple ROI Approach. Available online at: http://www.loni.ucla.edu/~narr/protocol.php?q=dti_ilf (Accessed January06, 2014).
65. Zisner, A., and Phillips, O. (2009c). Identifying the Uncinate Fasciculus (UF) in DTIStudio Using a Multiple ROI Approach. Available online at: http://www.loni.ucla.edu/~narr/protocol.php?q=dti_uf (Accessed January06, 2014).
66. Zou, L., Ding, G., Abutalebi, J., Shu, H., and Peng, D. (2012). Structural plasticity of the left caudate in bimodal bilinguals. Cortex 48, 1197-1206. doi: 10.1016/j.cortex.2011.05.022