The relationship between phonological and auditory processing and brain organization in beginning readers

Brain and Language

Volumn 125, Issue 2, 2013, Pages 173-183

  Pugh, Kenneth R ^a,b,e   Landi, Nicole ^a,c   Preston, Jonathan L ^a,d   Mencl, W Einar ^a   Austin, Alison C ^a   Sibley, Daragh ^a   Fulbright, Robert K ^a,b   Seidenberg, Mark S ^a,f   Grigorenko, Elena L ^a,c   Constable, R Todd ^a,b   Molfese, Peter ^a   Frost, Stephen J ^a  

^a HASKINS LABORATORIES   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d SOUTHERN CONNECTICUT STATE UNIVERSITY   (United States)

^e UNIVERSITY OF CONNECTICUT   (United States)

^f UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Decoding; FMRI; Individual differences; Phonological awareness; Rapid auditory processing; Reading; Thalamus

Indexed keywords

ARTICLE; ATTENTION; CHILD; FEMALE; FRONTAL LOBE; HEARING; HUMAN; HUMAN EXPERIMENT; INFERIOR FRONTAL GYRUS; LEFT HEMISPHERE; MALE; NEUROPHYSIOLOGY; NORMAL HUMAN; OCCIPITAL LOBE; PARIETAL LOBE; PHONETICS; PRECUNEUS; PRESCHOOL CHILD; PRINTING; READING; SCHOOL CHILD; SPEECH; TASK PERFORMANCE; TEMPORAL LOBE; VISUAL CORTEX; WORD RECOGNITION;

AWARENESS; BRAIN; BRAIN MAPPING; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; MALE; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; READING; SPEECH; SPEECH PERCEPTION; VISUAL PERCEPTION;

EID: 84876494179     PISSN: 0093934X     EISSN: 10902155     Source Type: Journal    
DOI: 10.1016/j.bandl.2012.04.004     Document Type: Article

References (108)

1. Ahissar M., Hochstein S. The reverse hierarchy theory of visual perceptual learning. Trends in Cognitive Sciences 2004, 8:457-464.
2. Ball E.W., Blachman B.A. Does phoneme awareness training in kindergarten make a difference in early word recognition and developmental spelling?. Reading Research Quarterly 1991, 26:49-66.
3. Baleydier C., Morel A. Segregated thalamocortical pathways to inferior parietal and inferotemporal cortex in macaque monkey. Visual Neuroscience 1992, 8:391-405.
4. Beaulieu C., Plewes C., Paulson L.A., Roy D., Snook L., Concha L., et al. Imaging brain connectivity in children with diverse reading ability. Neuroimage 2005, 25(4):1266-1271.
5. Ben-Shachar M., Dougherty R.F., Deutsch G.K., Wandell B.A. The development of cortical sensitivity to visual word forms. Journal of Cognitive Neuroscience 2011, 23(9):2387-2399.
6. Binder J.R., Medler D.A., Desai R., Conant L.L., Liebenthal E. Some neurophysiological constraints on models of word naming. Neuroimage 2005, 27:677-693.
7. Blau V., Reithler J., van Atteveldt N., Seitz J., Gerretsen P., Goebel R., et al. Deviant processing of letters and speech sounds as proximate cause of reading failure: A functional magnetic resonance imaging study of dyslexic children. Brain 2010, 133:868-879.
8. Brambati S.M., Termine C., Ruffino M., Stella G., Fazio F., Cappa S.F., et al. Regional reductions of gray matter volume in familial dyslexia. Neurology 2004, 63:742-745.
9. Brem, S., Bach, S., Kucian. K., Guttorm, T. K., Martin, E., Lyytinen, H., et al. (2010). Brain sensitivity to print emerges when children learn letter-speech sound correspondences. Proceedings of the National Academy of Sciences, 107, 7939-7944.
10. Breier J.I., Fletcher J.M., Foorman B.R., Klass P., Gray L.C. Auditory temporal processing in children with specific reading disability with and without attention deficit/hyperactivity disorder. Journal of Speech, Language, and Hearing Research 2003, 46:31-42.
11. Brown J.K., O'Regan M.E. The neurology of speech and language disorders in children. Part I: Disorders of comprehension and inner language. Clinics in Developmental Medicine 2001, 156:1-32.
12. Brunswick N., McCrory E., Price C., Frith C.D., Frith U. Explicit and implicit processing of words and pseudowords by adult developmental dyslexics: A search for Wernicke's Wortschatz?. Brain 1999, 122:1901-1917.
13. Byrne B., Coventry W.L., Olson R.K., Hulslander J., Wadsworth S., DeFries J.C., et al. A behavior-genetic analysis of orthographic learning, spelling, and decoding. Journal of Research in Reading 2008, 31:8-21.
14. Casanova C. The visual functions of the pulvinar. The Visual Neurosciences 2004, 592-608. The MIT Press, Cambridge, USA. L.M. Chalupa, J.S. Werner (Eds.).
15. Castles A., Coltheart M. Is there a causal link from phonological awareness to success in learning to read?. Cognition 2004, 91:77-111.
16. Castles A., McLean G.M.T., McArthur G. Dyslexia (neuropsychological). WIREs Cognitive Science 2010, 1:426-432.
17. Castro-Caldas A., Petersson K.M., Reis A., Stone-Elander S., Ingvar M. The illiterate brain. Learning to read and write during childhood influences the functional organization of the adult brain. Brain 1998, 121:1053-1063.
18. Cavanna A.E., Trimble M.R. The precuneus: A review of its functional anatomy and behavioural correlates. Brain 2006, 129:564-583.
19. Crosson B. Subcortical mechanisms in language: Lexical-semantic mechanisms and the thalamus. Brain and Cognition 1999, 40:414-438.
20. Dehaene S., Cohen L. The unique role of the visual word form area in reading. Trends in Cognitive Sciences 2011, 15(6):254-262.
21. Demb J.B., Boynton G.M., Best M., Heeger D.J. Psychophysical evidence for a magnocellular pathway deficit in dyslexia. Vision Research 1998, 38:1555-1559.
22. Desimone R., Wessinger M., Thomas L., Schneider W. Attentional control of visual perception: Cortical and subcortical mechanisms. Cold Spring Harbor Symposia on Quantitative Biology 1990, 55:963-971.
23. Dunn L., Dunn L. Peabody Picture Vocabulary Test 1997, American Guidance Service, Circle Pines, MN. 3rd Ed.
24. Elbro C. Early linguistic abilities and reading development: A review and hypothesis. Reading and Writing 1996, 8(6):453-485.
25. Fischer J., Whitney D. Attention narrows position tuning of population responses in V1. Current Biology 2009, 19(16):1356-1361.
26. Fletcher J.M., Lyon G.R., Fuchs L.S., Barnes M.A. Learning disabilities: From identification to intervention 2007, Guilford, New York.
27. Fletcher J. Dyslexia: The evolution of a scientific concept. Journal of the International Neuropsychological Society 2009, 15:501-508.
28. Foorman B.R., Francis D., Fletcher J.K., Schatschneider C., Mehta P. The role of instruction in learning to reading: Preventing reading failure in at-risk children. Journal of Educational Psychology 1998, 90:37-55.
29. Fowler, A. E. (1991). How early phonological development might set the stage for phoneme awareness. In S. Brady & D. P. Shankweiler (Eds.), Phonological processes in literacy: A tribute to Isabelle Y. Liberman (pp. 97-118). Hillsdale, NJ: Erlbaum.
30. Friston K.J., Holmes A.P., Poline J.B., Price C.J., Frith C.D. Detecting activations in PET and fMRI: Levels of inference and power. NeuroImage 1995, 4:223-235.
31. Frost S.J., Landi N., Mencl W.E., Sandak R., Fulbright R.K., Tejada E.T., et al. Phonological awareness predicts activation patterns for print and speech. Annals of Dyslexia 2009, 59:78-97.
32. Gaab N., Gabrieli J.D.E., Deutsch G.K., Tallal P., Temple E. Neural correlates of rapid auditory processing are disrupted in children with developmental dyslexia and ameliorated with training: An fMRI study. Restorative Neurology and Neuroscience 2007, 25:295-310.
33. Galaburda A.M., LoTurco J., Ramus F., Fitch R.H., Rosen G.D. From genes to behavior in developmental dyslexia. Nature Neuroscience 2006, 9(10):1213-1217.
34. Galaburda A.M., Sherman G.F., Rosen G.D., Aboitiz F., Geschwind N. Developmental dyslexia: four consecutive patients with cortical anomalies. Annals of Neurology 1985, 18:222-233.
35. Genovese C.R., Lazar N.A., Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 2002, 15:870-878.
36. Goldman-Rakic P.S. Topography of cognition: Paralleled distribution networks in primate association cortex. Annual Review of Neuroscience 1988, 11:137-156.
37. Goswami U., Fosker T., Huss M., Mead N., Szucs D. Rise time and formant transition duration in the discrimination of speech sounds: The Ba-Wa distinction in developmental dyslexia. Developmental Science 2010, 14:34-43.
38. Goswami U., Ziegler J.C. A developmental perspective on the neural code for written words. Trends in Cognitive Sciences 2006, 10:142-143.
39. Hampson M., Olson I.R., Leung H.C., Skudlarski P., Gore J.C. Changes in functional connectivity of human MT/V5 with visual motion input. NeuroReport 2004, 15:1315-1319.
40. Harm M.W., Seidenberg M.S. Computing the meanings of words in reading: Cooperative division of labor between visual and phonological processes. Psychological Review 1999, 106:491-528.
41. Horwitz, B., Rumsey, J. M., & Donohue, B. C. (1998). Functional connectivity of the angular gyrus in normal reading and dyslexia. Proceedings of the National Academy Sciences, 95, 8939-8944.
42. Johnson E.P., Pennington B.F., Lee N.R., Boada R. Directional effects between rapid auditory processing and phonological awareness in children. Journal of Child Psychology and Psychiatry 2009, 50:902-910.
43. Jorm A.F., Share D.L., Maclean R., Matthews R. Cognitive factors at school entry predictive of specific reading retardation and general reading backwardness: A research note. Journal of Child Psychology and Psychiatry 1986, 27:45-54.
44. Katusic S.K., Colligan R.C., Barbaresi W.J., Schaid D.J., Jacobsen S.J. Incidence of reading disability in a population-based birth cohort, 1976-1982, Rochester, Minn. Mayo Clinic Proceedings 2001, 76:1081-1092.
45. Katzir T., Misra M., Poldrack R.A. Imaging phonology without print: Assessing the neural correlates of phonemic awareness using fMRI. NeuroImage 2005, 27:106-115.
46. Klingberg T., Hedehus M., Temple E., Salz T., Gabrieli J.D.E., Moseley M.E., et al. Microstructure of temporo-parietal white matter as a basis for reading ability: Evidence from diffusion tensor magnetic resonance imaging. Neuron 2000, 25(2):493-500.
47. Kronbichler M., Wimmer H., Staffen W., Hutzler F., Mair A., Ladurner G. Developmental dyslexia: Gray matter abnormalities in the occipitotemporal cortex. Human Brain Mapping 2008, 29:613-625.
48. LaBerge D., Buchsbaum M.S. Positron emission tomographic measurements of pulvinar activity during an attention task. Journal of Neuroscience 1990, 10:613-619.
49. Landerl K., Willburger E. Temporal processing, attention, and learning disorders. Learning and Individual Differences 2010, 20:393-401.
50. Liberman I.Y., Shankweiler D. Phonology and the problems of learning to read and write. Remedial and Special Education 1985, 6:8-17.
51. Liberman I.Y., Shankweiler D., Fischer W., Carter B. Explicit syllable and phoneme segmentation in the young child. Journal of Child Psychology 1974, 18:201-212.
52. Lockwood A.H., Murphy B.W., Khalak H. Attentional systems and the allocation of cerebral resources in reading and grammatical tasks. International Journal of Neuroscience 1997, 91:241-252.
53. Lyon G.R., Shaywitz S.E., Shaywitz B.A. A definition of dyslexia. Annals of Dyslexia 2003, 53:1-14.
54. McCandliss B.D., Cohen L., Dehaene S. The visual word form area: expertise for reading in the fusiform gyrus. Trends in Cognitive Sciences 2003, 7(7):293-299.
55. Meyler A., Keller T.A., Cherkassky V.L., Lee D., Hoeft F., Whitfield-Gabrieli S., et al. Brain activation during sentence comprehension among good and poor readers. Cerebral Cortex 2007, 10(17):2780-2787.
56. Miezin F.M., Maccotta L., Ollinger J.M., Petersen S.E., Buckner R.L. Characterizing the hemodynamic response: Effects of presentation rate, sampling procedure, and the possibility of ordering brain activity based on relative timing. Neuroimage 2000, 11:735-759.
57. Nicolson R.I., Fawcett A.J., Dean P. Developmental dyslexia: The cerebellar deficit hypothesis. Trends in Neurosciences 2001, 24:508-511.
58. Niogi S.N., McCandliss B.D. Left lateralized white matter microstructure accounts for individual differences in reading ability and disability. Neuropsychologia 2006, 44:2178-2188.
59. Perfetti C.A., Hart L. The lexical basis of comprehension skill. The consequences of meaning selection 2001, 67-86. American Psychological Association, Washington, DC. D. Gorfein (Ed.).
60. Peschke C., Ziegler W., Eisenberger J., Baumgaertner A. Phonological manipulation between speech perception and production activates a parieto-frontal circuit. Neuroimage 2012, 59(1):788-799.
61. Plomin R., Kovas Y. Generalist genes and learning disabilities. Psychological Bulletin 2005, 131:592-617.
62. Posner M.I., Raichle M.E. Precis of images of mind. Behavioral and Brain Sciences 1995, 18:327-383.
63. Preston J.L., Frost S.J., Mencl W.E., Fulbright R.K., Landi N., Grigorenko E., et al. Early and late talkers: School-age language, literacy and neurolinguistic differences. Brain 2010, 133:2185-2195.
64. Price C.J., Devlin J.T. The interactive account of ventral occipitotemporal contributions to reading. Trends in Cognitive Sciences 2011, 15(6):246-253.
65. Psychological Corporation (1999). Wechsler abbreviated scale of intelligence. San Antonio, TX: The Psychological Corporation.
66. Pugh K.R., Frost S.J., Sandak R., Landi N., Moore D., Della Porta G., et al. The neural basis of reading. Mapping the word reading circuitry in skilled and disabled readers 2010, 281-305. Oxford University Press, New York. P.L. Cornelissen, P.C. Hansen, M.L. Kringelbach, R. Salmelin (Eds.).
67. Pugh K.R., Frost S.J., Sandak R., Landi N., Rueckl J.G., Constable R.T., et al. Effects of stimulus difficulty and repetition on printed word identification: An fMRI comparison of nonimpaired and reading-disabled adolescent cohorts. Journal of Cognitive Neuroscience 2008, 20:1146-1160.
68. Pugh K.R., Mencl W.E., Jenner A.R., Katz L., Frost S.J., Lee J.R., et al. Functional neuroimaging studies of reading and reading disability (developmental dyslexia). Mental Retardation & Developmental Disabilities Research Reviews 2000, 6:207-213.
69. Pugh K.R., Mencl W.E., Shaywitz B.A., Shaywitz S.E., Fulbright R.K., Skudlarski P., et al. The angular gyrus in developmental dyslexia: Task-specific differences in functional connectivity in posterior cortex. Psychological Science 2000, 11:51-56.
70. Pugh, K. R., Shaywitz, B. A., Shaywitz, S. E., Shankweiler, D. P., Katz, L., Fletcher, J. M., & Gore, J. C. (1997). Predicting reading performance from neuroimaging profiles: The cerebral basis of phonological effects in printed word identification. Journal of Experimental Psychology: Human Perception and Performance, 23, 299-318.
71. Ramus F. Developmental dyslexia: Specific phonological deficit or general sensorimotor dysfunction. Current Opinion in Neurobiology 2003, 13:212-218.
72. Ramus F., White S., Frith U. Weighing the evidence between competing theories of dyslexia. Developmental Science 2006, 9:265-269.
73. Raschle N.M., Chang M., Gaab N. Structural brain alterations associated with dyslexia predate reading onset. Neuroimage 2011, 57(3):742-749.
74. Rumsey J.M., Nace K., Donohue B., Wise D., Maisog J.M., Andreason P. A positron emission tomographic study of impaired word recognition and phonological processing in dyslexic men. Archives of Neurology 1997, 54:562-573.
75. Salmelin R., Service E., Kiesila P., Uutela K., Salonen O. Impaired visual word processing in dyslexia revealed with magnetoencephalography. Annals of Neurology 1996, 40:157-162.
76. Sarkari S., Simos P.G., Fletcher J.M., Castillo E.M., Breier J.I., Papanicolaou A.C. The emergence and treatment of developmental reading disability: Contributions of functional brain imaging. Seminars in Pediatric Neurology 2002, 9:227-236.
77. Seghier M.L., Price C.J. Reading aloud boosts connectivity through the putamen. Cerebral Cortex 2010, 20:570-582.
78. Serences J.T., Yantis S. Selective visual attention and perceptual coherence. Trends in Cognitive Sciences 2006, 10(1):38-45.
79. Shankweiler D., Mencl W.E., Braze D., Tabor W., Pugh K.R., Fulbright R.K. Reading differences and brain: cortical integration of speech and print in sentence processing varies with reader skill. Developmental Neuropsychology 2008, 33:745-775.
80. Shaywitz S.E., Escobar M.D., Shaywitz B.A., Fletcher J.M., Makuch R.W. Evidence that dyslexia may represent the lower tail of a normal distribution of reading ability. New England Journal of Medicine 1992, 326:145-150.
81. Shaywitz, S. E., Shaywitz, B. A., Pugh, K. R., Fulbright, R. K., Constable, R. T., Mencl, W. E., et al. (1998). Functional disruption in the organization of the brain for reading in dyslexia. Proceedings of the National Academy of Sciences, 95, 2636-2641.
82. Shaywitz B.A., Shaywitz S.E., Pugh K.R., Mencl W.E., Fullbright R.K., Skudlarski P., et al. Disruption of posterior brain systems for reading in children with developmental dyslexia. Biological Psychiatry 2002, 52:101-110.
83. Shaywitz S.E., Shaywitz B.A. The science of reading and dyslexia. Journal of AAPOS 2003, 7(3):158-166.
84. Silani G., Frith U., Demonet J.F., Fazio F., Perani D., Price C., et al. Brain abnormalities underlying altered activation in dyslexia: A voxel based morphometry study. Brain 2005, 128(10):2453-2461.
85. Simos P.G., Fletcher J.M., Bergman E., Breier J.I., Foorman B.R., Castillo E.M., et al. Dyslexia-specific brain activation profile becomes normal following successful remedial training. Neurology 2002, 58:1203-1213.
86. Snowling M.J., Hulme C. Annual Research Review: The nature and classification of reading disorders: A commentary on proposals for DSM-5. Journal of Child Psychology and Psychiatry 2012, 53(5):593-607.
87. Specht K., Hugdahl K., Ofte S., Nygard M., Bjornerud A., Plante E., et al. Brain activation on pre-reading tasks reveals at-risk status for dyslexia in 6-yearold children. Scandanavian Journal of Psychology 2009, 50(1):79-91.
88. Sperling A.J., Lu Z.L., Manis F.R., Seidenberg M.S. Deficits in perceptual noise exclusion in developmental dyslexia. Nature Neuroscience 2005, 8:862-863.
89. Sperling A.J., Lu Z.L., Manis F.R., Seidenberg M.S. Motion-perception deficits and reading impairment: It's the noise, not the motion. Psychological Science 2006, 17:1047-1053.
90. Stein J., Walsh V. To see but not to read: The magnocellular theory of dyslexia. Trends in Neurosciences 1997, 20:147-151.
91. Stevenson J. Which aspects of reading disability show a "hump" in their distribution?. Applied Cognitive Psychology 1988, 2:77-85.
92. Tallal P. Auditory temporal perception, phonics, and reading disabilities in children. Brain & Language 1980, 9:182-198.
93. Tallal P., Gaab N. Dynamic auditory processing, musical experience and language development. Trends in Neurosciences 2006, 29(7):382-390.
94. Temple, E., Deutsch, G. K., Poldrack, R. A., Miller, S. L., Tallal, P., Merzenich, M. M., et al. (2003). Neural deficits in children with dyslexia ameliorated by behavioral remediation: Evidence from functional MRI. Proceedings of the National Academy of Sciences, 100, 2860-2865.
95. Temple, E., Poldrack, R. A., Protopapas, A., Nagarajan, S., Salz, T., Tallal, P., et al. (2000). Disruption of the neural response to rapid acoustic stimuli in dyslexia: evidence from functional MRI. Proceedings of the National Academy of Sciences, 97, 13907-13912.
96. Torgesen J.K., Morgan S.T., Davis C. Effects of two types of phonological awareness training on word learning in kindergarten children. Journal of Educational Psychology 1992, 84:364-370.
97. Torgesen J. K., Wagner R. K., & Rashotte C. A. (1999). Test of word reading efficiency. Austin, TX: Pro-Ed.
98. Torgesen J.K., Wagner R.K., Rashotte C.A., Rose E., Lindamood P., Conway T., et al. Preventing reading failure in young children with phonological processing disabilities: Group and individual responses to instruction. Journal of Educational Psychology 1999, 91(4):579-593.
99. Turkeltaub P., Eden G., Jones K., Zeffiro T. Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. Neuroimage 2002, 16:765-780.
100. Turkeltaub P.E., Gareau L., Flowers D.L., Zeffiro T.A., Eden G.F. Development of neural mechanisms for reading. Nature Neuroscience 2003, 6:767-773.
101. Ullman M.T., Pierpont E.I. Specific language impairment is not specific to language: The procedural deficit hypothesis. Cortex 2005, 41:399-433.
102. Vellutino F.R., Fletcher J.M., Snowling M.J., Scanlon D.M. Specific reading disability (dyslexia): What have we learned in the past four decades?. Journal of Child Psychology and Psychiatry 2004, 45:2-40.
103. Wagner, R. K., Torgesen, J. K., & Rashotte, C. A. (1999). Comprehensive Test of Phonological Processing. Austin, TX: Pro-Ed.
104. Ward R., Jackson S.R. Visual attention in blindsight: Sensitivity in the blind field increased by targets in the sighted field. NeuroReport 2002, 13:301-304.
105. Woodcock R.W., McGrew K.S., Mather N. Woodcock-Johnson III tests of cognitive abilities 2001, Riverside Publishing, Itasca, IL.
106. Yamada Y., Stevens C., Dow M., Harn B.A., Chard D.J., Neville H.J. Emergence of the neural network for reading in five-year-old beginning readers of different levels of pre-literacy abilities: An fMRI study. Neuroimage 2011, 57(3):704-713.
107. Zatorre R.J., Meyer E., Gjedde A., Evans A.C. PET studies of phonetic processing of speech: review, replication, and reanalysis. Cerebral Corex 1996, 6(1):21-30.
108. Ziegler J.C., Pech-Georgel C., George F., Lorenzi C. Speech-perception-in-noise deficits in dyslexia. Developmental Science 2009, 12:732-745.