Reading without speech sounds: VWFA and its connectivity in the congenitally deaf

Cerebral Cortex

Volumn 25, Issue 9, 2015, Pages 2416-2426

  Wang, Xiaosha ^a   Caramazza, Alfonso ^b,c   Peelen, Marius V ^c   Han, Zaizhu ^a   Bi, Yanchao ^a  

^a BEIJING NORMAL UNIVERSITY   (China)

^b HARVARD UNIVERSITY   (United States)

^c UNIVERSITY OF TRENTO   (Italy)

Author keywords

Auditory speech experience; Congenitally deaf; Functional connectivity; Resting state; Visual word form area

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; AUDITORY CORTEX; BRAIN REGION; CLINICAL ARTICLE; CONGENITAL DEAFNESS; CONNECTOME; CONTROLLED STUDY; EXPERIENCE; FEMALE; FRONTOPARIETAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEARING; HUMAN; LEFT HEMISPHERE; MALE; PHONEME; PRIORITY JOURNAL; READING; RESTING STATE NETWORK; SEMANTICS; SOUND; SPEECH; SPEECH SOUND; SUPERIOR TEMPORAL GYRUS; VISUAL WORD FORM AREA; ANALYSIS OF VARIANCE; BLOOD; BRAIN CORTEX; BRAIN MAPPING; HEARING IMPAIRMENT; HEMISPHERIC DOMINANCE; IMAGE PROCESSING; LANGUAGE; LINGUISTICS; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PHOTOSTIMULATION; REST; VASCULARIZATION; YOUNG ADULT;

OXYGEN;

ADOLESCENT; ANALYSIS OF VARIANCE; BRAIN MAPPING; CEREBRAL CORTEX; DEAFNESS; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LANGUAGE; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; OXYGEN; PHOTIC STIMULATION; READING; REST; SPEECH; VOCABULARY; YOUNG ADULT;

EID: 84973431917     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhu044     Document Type: Article

References (69)

1. Aparicio M, Gounot D, Demont E, Metz-Lutz MN. 2007. Phonological processing in relation to reading: an fMRI study in deaf readers. Neuroimage. 35:1303-1316.
2. Ben-Shachar M, Dougherty RF, Deutsch GK, Wandell BA. 2011. The development of cortical sensitivity to visual word forms. J Cogn Neurosci. 23:2387-2399.
3. Binder JR, Desai RH, Graves WW, Conant LL. 2009. Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb Cortex. 19:2767-2796.
4. Bolger DJ, Perfetti CA, Schneider W. 2005. Cross-cultural effect on the brain revisited: universal structures plus writing system variation. Hum Brain Mapp. 25:92-104.
5. Brem S, Bach S, Kucian K, Guttorm TK, Martin E, Lyytinen H, Brandeis D, Richardson U. 2010. Brain sensitivity to print emerges when children learn letter-speech sound correspondences. Proc Natl Acad Sci USA. 107:7939-7944.
6. Buchel C, Price C, Friston K. 1998. A multimodal language region in the ventral visual pathway. Nature. 394:274-277.
7. Cohen L, Dehaene S, Naccache L, Lehericy S, Dehaene-Lambertz G, Henaff MA, Michel F. 2000. The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. Brain. 123(Pt 2): 291-307.
8. Cohen L, Jobert A, Le Bihan D, Dehaene S. 2004. Distinct unimodal and multimodal regions for word processing in the left temporal cortex. Neuroimage. 23:1256-1270.
9. Cohen L, Lehericy S, Chochon F, Lemer C, Rivaud S, Dehaene S. 2002. Language-specific tuning of visual cortex? Functional properties of the visual word form area. Brain. 125:1054-1069.
10. Cohen L, Martinaud O, Lemer C, Lehericy S, Samson Y, Obadia M, Slachevsky A, Dehaene S. 2003. Visual word recognition in the left and right hemispheres: anatomical and functional correlates of peripheral alexias. Cereb Cortex. 13:1313-1333.
11. Coltheart M, Rastle K, Perry C, Langdon R, Ziegler J. 2001. DRC: a dual route cascaded model of visual word recognition and reading aloud. Psychol Rev. 108:204-256.
12. Corbetta M, Shulman GL. 2002. Control of goal-directed and stimulusdriven attention in the brain. Nat Rev Neurosci. 3:201-215.
13. Craddock RC, Jbabdi S, Yan CG, Vogelstein JT, Castellanos FX, Di Martino A, Kelly C, Heberlein K, Colcombe S, Milham MP. 2013. Imaging human connectomes at the macroscale. Nat Methods. 10:524-539.
14. Dehaene S, Cohen L. 2011. The unique role of the visual word form area in reading. Trends Cogn Sci. 15:254-262.
15. Dehaene S, Le Clec HG, Poline JB, Le Bihan D, Cohen L. 2002. The visual word form area: a prelexical representation of visual words in the fusiform gyrus. Neuroreport. 13:321-325.
16. Dehaene S, Pegado F, Braga LW, Ventura P, Nunes Filho G, Jobert A, Dehaene-Lambertz G, Kolinsky R, Morais J, Cohen L. 2010. How learning to read changes the cortical networks for vision and language. Science. 330:1359-1364.
17. DeWitt I, Rauschecker JP. 2012. Phoneme and word recognition in the auditory ventral stream. Proc Natl Acad Sci USA. 109:E505-E514.
18. Duncan KJ, Pattamadilok C, Knierim I, Devlin JT. 2009. Consistency and variability in functional localisers. Neuroimage. 46:1018-1026.
19. Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT. 2009. Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp. 30: 2907-2926.
20. Emmorey K, Allen JS, Bruss J, Schenker N, Damasio H. 2003. A morphometric analysis of auditory brain regions in congenitally deaf adults. Proc Natl Acad Sci USA. 100:10049-10054.
21. Emmorey K, Weisberg J, McCullough S, Petrich JA. 2013. Mapping the reading circuitry for skilled deaf readers: an fMRI study of semantic and phonological processing. Brain Lang. 126:169-180.
22. Fox MD, Zhang D, Snyder AZ, Raichle ME. 2009. The global signal and observed anticorrelated resting state brain networks. J Neurophysiol. 101:3270-3283.
23. Glezer LS, Jiang X, Riesenhuber M. 2009. Evidence for highly selective neuronal tuning to whole words in the "visual word form area". Neuron. 62:199-204.
24. Goldin-Meadow S, Mayberry R. 2001. How do profoundly deaf children learn to read?. Learn Disabil Res Pract. 16:222-229.
25. Grainger J, Dufau S, Montant M, Ziegler JC, Fagot J. 2012. Orthographic processing in baboons (Papio papio). Science. 336: 245-248.
26. Hashimoto R, Sakai KL. 2004. Learning letters in adulthood: direct visualization of cortical plasticity for forming a new link between orthography and phonology. Neuron. 42:311-322.
27. Hickok G, Poeppel D. 2007. The cortical organization of speech processing. Nat Rev Neurosci. 8:393-402.
28. Hu Z, Wang W, Liu H, Peng D, Yang Y, Li K, Zhang JX, Ding G. 2011. Brain activations associated with sign production using word and picture inputs in deaf signers. Brain Lang. 116:64-70.
29. Koyama MS, Kelly C, Shehzad Z, Penesetti D, Castellanos FX, Milham MP. 2010. Reading networks at rest. Cereb Cortex. 20:2549-2559.
30. Kronschnabel J, Schmid R, Maurer U, Brandeis D. 2013. Visual print tuning deficits in dyslexic adolescents under minimized phonological demands. Neuroimage. 74:58-69.
31. Liang X, Zou Q, He Y, Yang Y. 2013. Coupling of functional connectivity and regional cerebral blood flow reveals a physiological basis for network hubs of the human brain. Proc Natl Acad Sci USA. 110:1929-1934.
32. Liu C, Zhang WT, Tang YY, Mai XQ, Chen HC, Tardif T, Luo YJ. 2008. The visual word form area: evidence from an fMRI study of implicit processing of Chinese characters. Neuroimage. 40: 1350-1361.
33. Lohmann G, Hoehl S, Brauer J, Danielmeier C, Bornkessel-Schlesewsky I, Bahlmann J, Turner R, Friederici A. 2010. Setting the frame: the human brain activates a basic low-frequency network for language processing. Cereb Cortex. 20:1286-1292.
34. MacSweeney M, Brammer MJ, Waters D, Goswami U. 2009. Enhanced activation of the left inferior frontal gyrus in deaf and dyslexic adults during rhyming. Brain. 132:1928-1940.
35. MacSweeney M, Waters D, Brammer MJ, Woll B, Goswami U. 2008. Phonological processing in deaf signers and the impact of age of first language acquisition. Neuroimage. 40:1369-1379.
36. Mano QR, Humphries C, Desai RH, Seidenberg MS, Osmon DC, Stengel BC, Binder JR. 2013. The role of left occipitotemporal cortex in reading: reconciling stimulus, task, and lexicality effects. Cereb Cortex. 23:988-1001.
37. McCandliss BD, Cohen L, Dehaene S. 2003. The visual word form area: expertise for reading in the fusiform gyrus. Trends Cogn Sci. 7:293-299.
38. Murphy K, Birn RM, Handwerker DA, Jones TB, Bandettini PA. 2009. The impact of global signal regression on resting state correlations: are anti-correlated networks introduced?. Neuroimage. 44: 893-905.
39. Nakamura K, Kuo WJ, Pegado F, Cohen L, Tzeng OJ, Dehaene S. 2012. Universal brain systems for recognizing word shapes and handwriting gestures during reading. Proc Natl Acad Sci USA. 109: 20762-20767.
40. Neville HJ, Bavelier D, Corina D, Rauschecker J, Karni A, Lalwani A, Braun A, Clark V, Jezzard P, Turner R. 1998. Cerebral organization for language in deaf and hearing subjects: biological constraints and effects of experience. Proc Natl Acad Sci USA. 95:922-929.
41. Peelen MV, Bracci S, Lu X, He C, Caramazza A, Bi Y. 2013. Tool selectivity in left occipitotemporal cortex develops without vision. J Cogn Neurosci. 25:1225-1234.
42. Petitto LA, Zatorre RJ, Gauna K, Nikelski EJ, Dostie D, Evans AC. 2000. Speech-like cerebral activity in profoundly deaf people processing signed languages: implications for the neural basis of human language. Proc Natl Acad Sci USA. 97:13961-13966.
43. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE. 2012. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage. 59: 2142-2154.
44. Price CJ, Devlin JT. 2011. The interactive account of ventral occipitotemporal contributions to reading. Trends Cogn Sci. 15:246-253.
45. Rauschecker AM, Bowen RF, Perry LM, Kevan AM, Dougherty RF, Wandell BA. 2011. Visual feature-tolerance in the reading network. Neuron. 71:941-953.
46. Reich L, Szwed M, Cohen L, Amedi A. 2011. A ventral visual stream reading center independent of visual experience. Curr Biol. 21:363-368.
47. Richlan F, Kronbichler M, Wimmer H. 2009. Functional abnormalities in the dyslexic brain: a quantitative meta-analysis of neuroimaging studies. Hum Brain Mapp. 30:3299-3308.
48. Seidenberg MS, McClelland JL. 1989. A distributed, developmental model of word recognition and naming. Psychol Rev. 96:523-568.
49. Shibata DK 2007. Differences in brain structure in deaf persons on MR imaging studied with voxel-based morphometry. AJNR Am J Neuroradiol. 28:243-249.
50. Song XW, Dong ZY, Long XY, Li SF, Zuo XN, Zhu CZ, He Y, Yan CG, Zang YF. 2011. REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS ONE. 6:e25031.
51. Srihasam K, Mandeville JB, Morocz IA, Sullivan KJ, Livingstone MS. 2012. Behavioral and anatomical consequences of early versus late symbol training in macaques. Neuron. 73:608-619.
52. Striem-Amit E, Cohen L, Dehaene S, Amedi A. 2012. Reading with sounds: sensory substitution selectively activates the visual word form area in the blind. Neuron. 76:640-652.
53. Sun HL, Huang JP, Sun DJ, Li DJ, Xing HB, editors. 1997. Introduction to language corpus system of modern Chinese study. Beijing: Peking University Publisher.
54. Szwed M, Vinckier F, Cohen L, Dehaene S. 2012. Towards a universal neurobiological architecture for learning to read. Behav Brain Sci. 35:308-309.
55. Tan LH, Laird AR, Li K, Fox PT. 2005. Neuroanatomical correlates of phonological processing of Chinese characters and alphabetic words: a meta-analysis. Hum Brain Mapp. 25:83-91.
56. Twomey T, Kawabata Duncan KJ, Price CJ, Devlin JT. 2011. Top-down modulation of ventral occipito-temporal responses during visual word recognition. Neuroimage. 55:1242-1251.
57. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M. 2002. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 15:273-289.
58. Van der Haegen L, Cai Q, Brysbaert M. 2012. Colateralization of Broca's area and the visual word form area in left-handers: fMRI evidence. Brain Lang. 122:171-178.
59. van der Mark S, Klaver P, Bucher K, Maurer U, Schulz E, Brem S, Martin E, Brandeis D. 2011. The left occipitotemporal system in reading: disruption of focal fMRI connectivity to left inferior frontal and inferior parietal language areas in children with dyslexia. Neuroimage. 54:2426-2436.
60. Van Dijk KR, Sabuncu MR, Buckner RL. 2012. The influence of head motion on intrinsic functional connectivity MRI. Neuroimage. 59:431-438.
61. Vigneau M, Beaucousin V, Herve PY, Duffau H, Crivello F, Houde O, Mazoyer B, Tzourio-Mazoyer N. 2006. Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. Neuroimage. 30:1414-1432.
62. Vogel AC, Miezin FM, Petersen SE, Schlaggar BL. 2012. The putative visual word form area is functionally connected to the dorsal attention network. Cereb Cortex. 22:537-549.
63. Wandell BA, Rauschecker AM, Yeatman JD. 2012. Learning to see words. Annu Rev Psychol. 63:31-53.
64. Waters D, Campbell R, Capek CM, Woll B, David AS, McGuire PK, Brammer MJ, MacSweeney M. 2007. Fingerspelling, signed language, text and picture processing in deaf native signers: the role of the mid-fusiform gyrus. Neuroimage. 35:1287-1302.
65. Xia M, Wang J, He Y. 2013. Brain Net Viewer: a network visualization tool for human brain connectomics. PLoS ONE. 8:e68910.
66. Xue G, Chen C, Jin Z, Dong Q. 2006. Language experience shapes fusiform activation when processing a logographic artificial language: an fMRI training study. Neuroimage. 31:1315-1326.
67. Yeatman JD, Rauschecker AM, Wandell BA. 2013. Anatomy of the visual word form area: adjacent cortical circuits and long-range white matter connections. Brain Lang. 125:146-155.
68. Zhang D, Raichle ME. 2010. Disease and the brain's dark energy. Nat Rev Neurol. 6:15-28.
69. Zhao J, Liu J, Li J, Liang J, Feng L, Ai L, Lee K, Tian J. 2011. Intrinsically organized network for word processing during the resting state. Neurosci Lett. 487:27-31.