Testing for the dual-route cascade reading model in the brain: An fMRI effective connectivity account of an efficient reading style

PLoS ONE

Volumn 4, Issue 8, 2009, Pages

  Levy, Jonathan ^a,b,d,e   Pernet, Cyril ^c   Treserras, Sébastien ^a,b   Boulanouar, Kader ^a,b   Aubry, Florent ^a,b   Démonet, Jean François ^a,b   Celsis, Pierre ^a,b  

^a CHU PURPAN   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c WESTERN GENERAL HOSPITAL   (United Kingdom)

^d RADBOUD UNIVERSITY   (Netherlands)

^e RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BRAIN DEPTH STIMULATION; BRAIN REGION; CHILD; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; LANGUAGE ABILITY; MALE; MENTAL FUNCTION; NERVE CELL NETWORK; NEUROPSYCHOLOGICAL TEST; READING; SCHOOL CHILD; STIMULUS RESPONSE; TASK PERFORMANCE; WORD READING; BIOLOGICAL MODEL; BRAIN; METHODOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY;

BRAIN; HUMANS; MAGNETIC RESONANCE IMAGING; MODELS, BIOLOGICAL; NEUROPSYCHOLOGICAL TESTS; READING;

EID: 68949207158     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006675     Document Type: Article

References (70)

1. Castles A, Bates TC, Coltheart M (2006) John Marshall and the developmental Dyslexias. Aphasiology 20: 871-892.
2. Coltheart M, Rastle K, Perry C, Langdon R, Ziegler J (2001) DRC: A dual route cascaded model of visual word recognition and reading aloud. Psychological Review 108: 204-256.
3. Coltheart M (2006) The genetics of learning to read. Journal of Research in Reading 29: 124-132.
4. McCarthy R, Warrington EK (1986) Phonological reading: Phenomena and paradoxes. Cortex 22: 359-380.
5. Patterson K, Hodges JR (1992) Deterioration of word meaning: implications for reading. Neuropsychologia 30: 1025-1040.
6. Hodges JR, Patterson K (2007) Semantic dementia: a unique clinicopathological syndrome. Lancet Neurol 6: 1004-1014.
7. Funnell E (1983) Phonological processes in reading: New evidence from acquired dyslexia. British Journal of Psychology 74: 159-180.
8. Jobard G, Crivello F, Tzourio-Mazoyer N (2003) Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies. Neuroimage 20: 693-712.
9. Mechelli A, Gorno-Tempini ML, Price CJ (2003) Neuroimaging studies of word and pseudoword reading: consistencies, inconsistencies, and limitations. J Cogn Neurosci 15: 260-271.
10. Price CJ, Winterburn D, Giraud AL, Moore CJ, Noppeney U (2003) Cortical localization of the visual and auditory word form areas: a reconsideration of the evidence. Brain Lang 86: 272-286.
11. Wilson TW, Leuthold AC, Lewis SM, Georgopoulos AP, Pardo PJ (2005) Cognitive dimensions of orthographic stimuli affect occipitotemporal dynamics. Exp Brain Res 167: 141-147.
12. Levy J, Pernet C, Treserras S, Boulanouar K, Berry I, et al. (2008) Piecemeal recruitment of left-lateralized brain areas during reading: a spatio-functional account. Neuroimage 43: 581-591.
13. Pernet C, Schyns PG, Demonet JF (2007) Specific, selective or preferential: comments on category specificity in neuroimaging. Neuroimage 35: 991-997.
14. Price CJ, Mechelli A (2005) Reading and reading disturbance. Curr Opin Neurobiol 15: 231-238.
15. Booth JR, Burman DD, Meyer JR, Gitelman DR, Parrish TR, et al. (2002) Functional anatomy of intra- and cross-modal lexical tasks. NeuroImage 16: 7-22.
16. Mechelli A, Crinion JT, Long S, Friston KJ, Lambon Ralph MA, et al. (2005) Dissociating reading processes on the basis of neuronal interactions. J Cogn Neurosci 17: 1753-1765.
17. Dietz NA, Jones KM, Gareau L, Zeffiro TA, Eden GF (2005) Phonological decoding involves left posterior fusiform gyrus. Hum Brain Mapp 26: 81-93.
18. Binder JR, Medler DA, Desai R, Conant LL, Liebenthal E (2005) Some neurophysiological constraints on models of word naming. Neuroimage 27: 677-693.
19. Binder JR, Medler DA, Westbury CF, Liebenthal E, Buchanan L (2006) Tuning of the human left fusiform gyrus to sublexical orthographic structure. Neuroimage 33: 739-748.
20. Vinckier F, Dehaene S, Jobert A, Dubus JP, Sigman M, et al. (2007) Hierarchical coding of letter strings in the ventral stream: dissecting the inner organization of the visual word-form system. Neuron 55: 143-156.
21. Moore CJ, Price CJ (1999) Three distinct ventral occipitotemporal regions for reading and object naming. Neuroimage 10: 181-192.
22. James KH, James TW, Jobard G, Wong ACN, Gauthier I (2005) Letter processing in the visual system: different activation patterns for single letters and strings. Cogn Affect Behav Neurosci 5: 452-456.
23. Vigneau M, Beaucousin V, Herve PY, Duffau H, Crivello F, et al. (2006) Meta-analyzing left hemisphere language areas: phonology, semantics, and sentence processing. Neuroimage 30: 1414-1432.
24. Seghier ML, Lee HL, Schofield T, Ellis CL, Price CJ (2008) Inter-subject variability in the use of two different neuronal networks for reading aloud familiar words. Neuroimage 42: 1226-1236.
25. Zevin JD, Balota DA (2000) Priming and attentional control of lexical and sublexical pathways during naming. J Exp Psychol Learn Mem Cogn 26: 121-135.
26. Bitan T, Booth JR, Choy J, Burman DD, Gitelman DR, et al. (2005) Shifts of effective connectivity within a language network during rhyming and spelling. J Neurosci 25: 5397-5403.
27. Nakamura K, Hara N, Kouider S, Takayama Y, Hanajima R, et al. (2006) Task-guided selection of the dual neural pathways for reading. Neuron 52: 557-564.
28. Nakamura K, Dehaene S, Jobert A, Le Bihan D, Kouider S (2007) Task-specific change of unconscious neural priming in the cerebral language network. Proc Natl Acad Sci USA 104: 19643-19648.
29. Cao F, Bitan T, Booth JR (2008) Effective brain connectivity in children with reading difficulties during phonological processing. Brain Lang 107: 91-101.
30. Paulesu E, Demonet JF, Fazio F, McCrory E, Chanoine V, et al. (2001) Dyslexia: cultural diversity and biological unity. Science 291: 2165-2167.
31. Lefavrais P (2006) Alouette R: test d'analyse de la vitesse de lecture à partir d'un texte. [Translation into English: « Alouette R: test of analysis of text reading-speed » J.L.] Les éditions du centre de psychologie appliquée, Paris.
32. Rapcsak SZ, Beeson PM (2004) The role of left posterior inferior temporal cortex in spelling. Neurology 62: 2221-2229.
33. Henry ML, Beeson PM, Stark AJ, Rapcsak SZ (2007) The role of left perisylvian cortical regions in spelling. Brain Lang 100: 44-52.
34. Price CJ (2000) The anatomy of language: contributions from functional neuroimaging. J Anat 197: 335-359.
35. Demonet JF, Thierry G, Cardebat D (2005) Renewal of the neurophysiology of language: Functional neuroimaging. Physiol Rev 85: 49-95.
36. Salmelin R (2007) Clinical neurophysiology of language: The MEG approach. Clin Neurophysiol 118: 237-254.
37. Pugh KR, Mencl WE, Jenner AR, Katz L, Frost SJ, et al. (2000) Functional neuroimaging studies of reading and reading disability (developmental dyslexia). Ment Retard Dev Disabil Res Rev 6: 207-213.
38. Cohen L, Lehéricy S, Chochon F, Lemer C, Rivaud S, et al. (2002) Language-specific tuning of visual cortex? Functional properties of the Visual Word Form Area. Brain 125: 1054-1069.
39. Ratcliff R, McKoon G, Gomez P (2004) A diffusion model account of the lexical decision task. Psychol Rev 111: 159-182.
40. Booth JR, Mehdiratta N, Burman DD, Bitan T (2008) Developmental increases in effective connectivity to brain regions involved in phonological processing during tasks with orthographic demands. Brain Res 1189: 78-89.
41. Price CJ, Wise RJ, Frackowiak RS (1996) Demonstrating the implicit processing of visually presented words and pseudowords. Cereb Cortex 6: 62-70.
42. Puce A, Allison T, Asgari M, Gore JC, McCarthy G (1996) Differential sensitivity of human visual cortex to faces, letterstrings, and textures: a functional magnetic resonance imaging study. J Neurosci 16: 5205-5215.
43. Longcamp M, Anton J, Roth M, Velay J (2003) Visual presentation of single letters activates a premotor area involved in writing. NeuroImage 19: 1492-1500.
44. Pernet C, Franceries X, Basan S, Cassol E, Demonet JF, et al. (2004) Anatomy and time course of discrimination and categorization processes in vision: an fMRI study. NeuroImage 22: 1563-1577.
45. Kuo WJ, Yeh TC, Lee JR, Chen LF, Lee PL, et al. (2004) Orthographic and phonological processing of Chinese characters: an fMRI study. Neuroimage 21: 1721-1731.
46. Kronbichler M, Bergmann J, Hutzler F, Staffen W, Mair A, et al. (2007) Taxi vs. taksi: on orthographic word recognition in the left ventral occipitotemporal cortex. J Cogn Neurosci 19: 1584-1594.
47. Starrfelt R, Gerlach C (2007) The Visual What For Area: Words and pictures in the left fusiform gyrus. Neuroimage 35: 334-342.
48. Bar M, Tootell RB, Schacter DL, Greve DN, Fischl B, et al. (2001) Cortical mechanisms specific to explicit visual object recognition. Neuron 29: 529-535.
49. Joseph JE, Gathers AD (2003) Effects of structural similarity on neural substrates for object recognition. Cogn Affect Behav Neurosci 3: 1-16.
50. Joseph JE, Gathers AD, Piper GA (2003) Shared and dissociated cortical regions for object and letter processing. Brain Res Cogn Brain Res 17: 56-67.
51. Joseph JE, Cerullo MA, Farley AB, Steinmetz NA, Mier CR (2006) fMRI correlates of cortical specialization and generalization for letter processing. Neuroimage 15: 806-820.
52. Seidenberg MS, McClelland JL (1989) A distributed, developmental model of word recognition and naming. Psychol Rev 96: 523-568.
53. Wilson TW, Leuthold AC, Moran JE, Pardo PJ, Lewis SM, et al. (2007) Reading in a deep orthography: neuromagnetic evidence for dual-mechanisms. Exp Brain Res 180: 247-262.
54. Reinke K, Fernandes M, Schwindt G, O'Craven K, Grady CL (2008) Functional specificity of the visual word form area: general activation for words and symbols but specific network activation for words. Brain Lang 104: 180-189.
55. Bruno JL, Zumberge A, Manis FR, Lu ZL, Goldman JG (2008) Sensitivity to orthographic familiarity in the occipito-temporal region. Neuroimage 39: 1988-2001.
56. Pernet C, Andersson J, Paulesu E, Demonet JF (2009) When all hypotheses are right: A multifocal account of dyslexia. Hum Brain Mapp, In Press.
57. Baron J, Strawson C (1976) Use of orthographic and word-specific knowledge in reading words aloud. Journal of Experimental Psychology: Human Perception and Performance 2: 386-393.
58. 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.
59. Ziegler JC, Castel C, Pech-Georgel C, George F, Alario FX, et al. (2008) Developmental dyslexia and the dual route model of reading: simulating individual differences and subtypes. Cognition 107: 151-178.
60. Treiman R (1984) Individual differences among children in spelling and reading styles. J Exp Child Psychol 37: 463-477.
61. Connor CM, Morrison FJ, Fishman BJ, Schatschneider C, Underwood P (2007) The early years Algorithm-guided individualized reading instruction. Science 315: 464-465.
62. Dufor O, Serniclaes W, Sprenger-Charolles L, Démonet JF (2007) Top-down processes during auditory phoneme categorization in dyslexia: a PET study. Neuroimage 34: 1692-1707.
63. Dufor O, Serniclaes W, Sprenger-Charolles L, Démonet JF (2009) Left premotor cortex and allophonic speech perception in dyslexia: a PET study. Neuroimage 15: 241-248.
64. Mechelli A, Friston KJ, Price CJ (2000) The effects of presentation rate during word and pseudoword reading: a comparison of PET and fMRI. J Cogn Neurosci 12: 145-156.
65. Price CJ, Veltman DJ, Ashburner J, Josephs O, Friston KJ (1999) The critical relationship between the timing of stimulus presentation and data acquisition in blocked designs with fMRI. Neuroimage 10: 36-44.
66. Van Essen DC, Drury HA, Dickson J, Harwell J, Hanlon D, et al. (2001) An integrated software suite for surface-based analyses of cerebral cortex. J Am Med Inform Assoc 8: 443-459.
67. Jöreskog KG, Sörbom D (1996) LISREL 8 User's Reference Guide. Scientific Software International, Chicago.
68. de Marco G, Vrignaud P, Destrieux C, de Marco D, Testelin S, et al. (2009) Principle of structural equation modeling for exploring functional interactivity within a putative network of interconnected brain areas. Magn Reson Imaging 27: 1-12.
69. Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J Roy Stat Soc 57: 289-300.
70. Meyler A, Keller TA, Cherkassky VL, Lee D, Hoeft F, et al. (2007) Brain Activation during Sentence Comprehension among Good and Poor Readers. Cereb Cortex 17: 2780-2787.