Cortical Signatures of Dyslexia and Remediation: An Intrinsic Functional Connectivity Approach

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Koyama, Maki S ^a,b   Di Martino, Adriana ^b   Kelly, Clare ^b   Jutagir, Devika R ^b   Sunshine, Jessica ^b   Schwartz, Susan J ^c   Castellanos, Francisco X ^b,d   Milham, Michael P ^c,d  

^a RUTGERS UNIVERSITY   (United States)

^b NEW YORK UNIVERSITY CHILD STUDY CENTER   (United States)

^c CHILD MIND INSTITUTE   (United States)

^d NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ARTICLE; BEHAVIOR; BEHAVIORAL REMEDIATION; BRAIN ASYMMETRY; BRAIN CORTEX; BRAIN FUNCTION; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DYSLEXIA; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM GYRUS; HUMAN; INTRAPARIETAL SULCUS; MALE; MIDDLE FRONTAL GYRUS; OBSERVATIONAL STUDY; OCCIPITAL GYRUS; READING; SCHOOL CHILD; SPELLING;

ADOLESCENT; CEREBRAL CORTEX; CHILD; DYSLEXIA; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE;

EID: 84873648123     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055454     Document Type: Article

References (112)

1. Bradley L, Bryant PE, (1978) Difficulties in auditory organisation as a possible cause of reading backwardness. Nature 271: 746-747.
2. Stanovich KE, (1988) Explaining the differences between the dyslexic and the garden-variety poor reader: the phonological-core variable-difference model. Journal of learning disabilities 21: 590-604.
3. Ramus F, Rosen S, Dakin SC, Day BL, Castellote JM, et al. (2003) Theories of developmental dyslexia: insights from a multiple case study of dyslexic adults. Brain: a journal of neurology 126: 841-865.
4. Pennington BF, Santerre-Lemmon L, Rosenberg J, MacDonald B, Boada R, et al. (2012) Individual prediction of dyslexia by single versus multiple deficit models. Journal of abnormal psychology 121: 212-224.
5. Georgiou GK, Papadopoulos TC, Zarouna E, Parrila R, (2012) Are auditory and visual processing deficits related to developmental dyslexia? Dyslexia 18: 110-129.
6. Valdois S, Bidet-Ildei C, Lassus-Sangosse D, Reilhac C, N'Guyen-Morel MA, et al. (2011) A visual processing but no phonological disorder in a child with mixed dyslexia. Cortex; a journal devoted to the study of the nervous system and behavior 47: 1197-1218.
7. Peyrin C, Lallier M, Demonet JF, Pernet C, Baciu M, et al. (2012) Neural dissociation of phonological and visual attention span disorders in developmental dyslexia: FMRI evidence from two case reports. Brain and Language 120: 381-394.
8. Stein J, (2001) The magnocellular theory of developmental dyslexia. Dyslexia 7: 12-36.
9. Goswami U, Thomson J, Richardson U, Stainthorp R, Hughes D, et al. (2002) Amplitude envelope onsets and developmental dyslexia: A new hypothesis. Proceedings of the National Academy of Sciences of the United States of America 99: 10911-10916.
10. Tallal P, (1980) Auditory temporal perception, phonics, and reading disabilities in children. Brain and Language 9: 182-198.
11. Hämäläinen JA, Salminen HK, Leppänen PHT (2012) Basic Auditory Processing Deficits in Dyslexia: Systematic Review of the Behavioral and Event-Related Potential/Field Evidence. Journal of Learning Disabilities.
12. Wolf M, Bowers PG, Biddle K, (2000) Naming-speed processes, timing, and reading: a conceptual review. Journal of learning disabilities 33: 387-407.
13. Bosse ML, Tainturier MJ, Valdois S, (2007) Developmental dyslexia: the visual attention span deficit hypothesis. Cognition 104: 198-230.
14. Vidyasagar TR, Pammer K, (2010) Dyslexia: a deficit in visuo-spatial attention, not in phonological processing. Trends in Cognitive Sciences 14: 57-63.
15. Facoetti A, Trussardi AN, Ruffino M, Lorusso ML, Cattaneo C, et al. (2010) Multisensory spatial attention deficits are predictive of phonological decoding skills in developmental dyslexia. Journal of cognitive neuroscience 22: 1011-1025.
16. Stoodley CJ, Stein JF, (2011) The cerebellum and dyslexia. Cortex; a journal devoted to the study of the nervous system and behavior 47: 101-116.
17. Nicolson RI, Fawcett AJ (2005) Developmental dyslexia, learning and the cerebellum. Journal of neural transmission Supplementum: 19-36.
18. Demb JB, Boynton GM, Heeger DJ, (1998) Functional magnetic resonance imaging of early visual pathways in dyslexia. The Journal of neuroscience: the official journal of the Society for Neuroscience 18: 6939-6951.
19. Eden GF, VanMeter JW, Rumsey JM, Zeffiro TA, (1996) The visual deficit theory of developmental dyslexia. NeuroImage 4: S108-117.
20. Peyrin C, Demonet JF, N'Guyen-Morel MA, Le Bas JF, Valdois S, (2011) Superior parietal lobule dysfunction in a homogeneous group of dyslexic children with a visual attention span disorder. Brain and Language 118: 128-138.
21. Duff FJ, Clarke PJ, (2011) Practitioner Review: Reading disorders: what are the effective interventions and how should they be implemented and evaluated? Journal of Child Psychology and Psychiatry 52: 3-12.
22. Sarkari S, Simos PG, Fletcher JM, Castillo EM, Breier JI, et al. (2002) Contributions of magnetic source imaging to the understanding of dyslexia. Semin Pediatr Neurol 9: 229-238.
23. Simos PG, Fletcher JM, Sarkari S, Billingsley RL, Denton C, et al. (2007) Altering the brain circuits for reading through intervention: a magnetic source imaging study. Neuropsychology 21: 485-496.
24. Gaab N, Gabrieli JD, Deutsch GK, Tallal P, Temple E, (2007) Neural correlates of rapid auditory processing are disrupted in children with developmental dyslexia and ameliorated with training: an fMRI study. Restor Neurol Neurosci 25: 295-310.
25. Shaywitz BA, Shaywitz SE, Blachman BA, Pugh KR, Fulbright RK, et al. (2004) Development of left occipitotemporal systems for skilled reading in children after a phonologically- based intervention. Biol Psychiatry 55: 926-933.
26. Eden GF, Jones KM, Cappell K, Gareau L, Wood FB, et al. (2004) Neural Changes following Remediation in Adult Developmental Dyslexia. Neuron 44: 411-422.
27. Davis N, Barquero L, Compton DL, Fuchs LS, Fuchs D, et al. (2011) Functional correlates of children's responsiveness to intervention. Developmental neuropsychology 36: 288-301.
28. Torgesen JK, Alexander AW, Wagner RK, Rashotte CA, Voeller KK, et al. (2001) Intensive remedial instruction for children with severe reading disabilities: immediate and long-term outcomes from two instructional approaches. Journal of learning disabilities 34: 33-58, 78.
29. Kelly C, Biswal BB, Craddock RC, Castellanos FX, Milham MP, (2012) Characterizing variation in the functional connectome: promise and pitfalls. Trends in Cognitive Sciences 16: 181-188.
30. Biswal B, Yetkin FZ, Haughton VM, Hyde JS, (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magnetic resonance in medicine: official journal of the Society of Magnetic Resonance in Medicine/Society of Magnetic Resonance in Medicine 34: 537-541.
31. Fox MD, Corbetta M, Snyder AZ, Vincent JL, Raichle ME, (2006) Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. Proceedings of the National Academy of Sciences 103: 10046-10051.
32. Cordes D, Haughton VM, Arfanakis K, Wendt GJ, Turski PA, et al. (2000) Mapping Functionally Related Regions of Brain with Functional Connectivity MR Imaging. American Journal of Neuroradiology 21: 1636-1644.
33. Greicius MD, Krasnow B, Reiss AL, Menon V, (2003) Functional connectivity in the resting brain: A network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences 100: 253-258.
34. Margulies DS, Kelly AMC, Uddin LQ, Biswal BB, Castellanos FX, et al. (2007) Mapping the functional connectivity of anterior cingulate cortex. NeuroImage 37: 579-588.
35. Di Martino A, Scheres A, Margulies DS, Kelly AMC, Uddin LQ, et al. (2008) Functional Connectivity of Human Striatum: A Resting State fMRI Study. Cerebral Cortex 18: 2735-2747.
36. Krienen FM, Buckner RL, (2009) Segregated Fronto-Cerebellar Circuits Revealed by Intrinsic Functional Connectivity. Cerebral Cortex 19: 2485-2497.
37. Hampson M, Tokoglu F, Sun Z, Schafer RJ, Skudlarski P, et al. (2006) Connectivity'Äìbehavior analysis reveals that functional connectivity between left BA39 and Broca's area varies with reading ability. NeuroImage 31: 513-519.
38. Koyama MS, Kelly C, Shehzad Z, Penesetti D, Castellanos FX, et al. (2010) Reading Networks at Rest. Cerebral Cortex 20: 2549-2559.
39. Koyama MS, Di Martino A, Zuo X-N, Kelly C, Mennes M, et al. (2011) Resting-State Functional Connectivity Indexes Reading Competence in Children and Adults. The Journal of Neuroscience 31: 8617-8624.
40. Di Martino A, Kelly C, Grzadzinski R, Zuo X-N, Mennes M, et al. (2011) Aberrant Striatal Functional Connectivity in Children with Autism. Biological psychiatry 69: 847-856.
41. Cherkassky VL, Kana RK, Keller TA, Just MA, (2006) Functional connectivity in a baseline resting-state network in autism. NeuroReport 17: 1687-1690.
42. Kennedy DP, Courchesne E, (2008) The intrinsic functional organization of the brain is altered in autism. NeuroImage 39: 1877-1885.
43. von dem Hagen EA, Stoyanova RS, Baron-Cohen S, Calder AJ (2012) Reduced functional connectivity within and between 'social' resting state networks in Autism Spectrum Conditions. Social cognitive and affective neuroscience.
44. Cao X, Cao Q, Long X, Sun L, Sui M, et al. (2009) Abnormal resting-state functional connectivity patterns of the putamen in medication-naïve children with attention deficit hyperactivity disorder. Brain Research 1303: 195-206.
45. Fair DA, Posner J, Nagel BJ, Bathula D, Dias TGC, et al. (2010) Atypical Default Network Connectivity in Youth with Attention-Deficit/Hyperactivity Disorder. Biological psychiatry 68: 1084-1091.
46. Castellanos FX, Margulies DS, Kelly C, Uddin LQ, Ghaffari M, et al. (2008) Cingulate-Precuneus Interactions: A New Locus of Dysfunction in Adult Attention-Deficit/Hyperactivity Disorder. Biological psychiatry 63: 332-337.
47. Chabernaud C, Mennes M, Kelly C, Nooner K, Di Martino A, et al. (2012) Dimensional brain-behavior relationships in children with attention-deficit/hyperactivity disorder. Biological psychiatry 71: 434-442.
48. Church JA, Fair DA, Dosenbach NU, Cohen AL, Miezin FM, et al. (2009) Control networks in paediatric Tourette syndrome show immature and anomalous patterns of functional connectivity. Brain: a journal of neurology 132: 225-238.
49. Farris EA, Odegard TN, Miller HL, Ring J, Allen G, et al. (2011) Functional connectivity between the left and right inferior frontal lobes in a small sample of children with and without reading difficulties. Neurocase: 1-15.
50. Bolger DJ, Perfetti CA, Schneider W, (2005) Cross-cultural effect on the brain revisited: universal structures plus writing system variation. Human Brain Mapping 25: 92-104.
51. Houde O, Rossi S, Lubin A, Joliot M, (2010) Mapping numerical processing, reading, and executive functions in the developing brain: an fMRI meta-analysis of 52 studies including 842 children. Developmental Science 13: 876-885.
52. Richlan F, Kronbichler M, Wimmer H, (2011) Meta-analyzing brain dysfunctions in dyslexic children and adults. NeuroImage 56: 1735-1742.
53. Wechsler D (2001) Wechsler Individual Achievement Test-Second Edition (WIAT-II) San Antonio: The Psychological Corporation.
54. Snowling M, (1998) Dyslexia as a Phonological Deficit: Evidence and Implications. Child and Adolescent Mental Health 3: 4-11.
55. Kaufman J, Birmaher B, Brent D, Rao U, Ryan N (1996) The schedule for affective disorders and schizophrenia for school-age children Pittsburgh: University of Pittsburgh Medical Center.
56. Wechsler D (1999) Wechsler Abbreviated Scale of Intelligence (WASI). San Antonio: The Psychological Corporatio.
57. Torgesen J, Wagner R, Rashotte C (1999) Test of Word Reading Efficiency (TOWRE). Austin, TX: Pro-ED Inc.
58. Wagner RK, Torgesen JK, Rashotte CA (1999) CTOPP, Comprehensive Test of Phonological Processing. Austin, Tex.: PRO-ED. 1 case. p.
59. Willcutt EG, Pennington BF, Olson RK, DeFries JC, (2007) Understanding comorbidity: a twin study of reading disability and attention-deficit/hyperactivity disorder. American journal of medical genetics Part B, Neuropsychiatric genetics: the official publication of the International Society of Psychiatric Genetics 144B: 709-714.
60. Willcutt EG, Pennington BF, (2000) Comorbidity of Reading Disability and Attention-Deficit/Hyperactivity Disorder. Journal of learning disabilities 33: 179-191.
61. Conners CK (1997) Conners' Rating Scales-Revised: Technical manual. North Tonawanda, NY:: Multi-Health Systems.
62. Cox RW, (1996) AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and biomedical research, an international journal 29: 162-173.
63. Biswal BB, Mennes M, Zuo XN, Gohel S, Kelly C, et al. (2010) Toward discovery science of human brain function. Proceedings of the National Academy of Sciences of the United States of America 107: 4734-4739.
64. Andersson J, Jenkinson M, Smith S (2007) Non-linear registration, aka spatial normalisation. Oxford, UK: FMRIB.
65. Jenkinson M, Bannister P, Brady M, Smith S, (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17: 825-841.
66. Jenkinson M, Smith S, (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5: 143-156.
67. Bianciardi M, Fukunaga M, van Gelderen P, Horovitz SG, de Zwart JA, et al. (2009) Sources of functional magnetic resonance imaging signal fluctuations in the human brain at rest: a 7 T study. Magn Reson Imaging 27: 1019-1029.
68. Shmueli K, van Gelderen P, de Zwart JA, Horovitz SG, Fukunaga M, et al. (2007) Low-frequency fluctuations in the cardiac rate as a source of variance in the resting-state fMRI BOLD signal. NeuroImage 38: 306-320.
69. Schölvinck ML, Maier A, Ye FQ, Duyn JH, Leopold DA, (2010) Neural basis of global resting-state fMRI activity. Proceedings of the National Academy of Sciences 107: 10238-10243.
70. Margulies DS, Kelly AM, Uddin LQ, Biswal BB, Castellanos FX, et al. (2007) Mapping the functional connectivity of anterior cingulate cortex. NeuroImage 37: 579-588.
71. Castellanos FX, Margulies DS, Kelly C, Uddin LQ, Ghaffari M, et al. (2008) Cingulate-precuneus interactions: a new locus of dysfunction in adult attention-deficit/hyperactivity disorder. Biol Psychiatry 63: 332-337.
72. Di Martino A, Shehzad Z, Kelly C, Roy AK, Gee DG, et al. (2009) Relationship between cingulo-insular functional connectivity and autistic traits in neurotypical adults. Am J Psychiatry 166: 891-899.
73. 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.
74. Van Dijk KR, Sabuncu MR, Buckner RL, (2012) The influence of head motion on intrinsic functional connectivity MRI. NeuroImage 59: 431-438.
75. Satterthwaite TD, Wolf DH, Loughead J, Ruparel K, Elliott MA, et al. (2012) Impact of in-scanner head motion on multiple measures of functional connectivity: relevance for studies of neurodevelopment in youth. NeuroImage 60: 623-632.
76. Carp J (2011) Optimizing the order of operations for movement scrubbing: Comment on Poweret al. NeuroImage.
77. 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.
78. Saad ZS, Gotts SJ, Murphy K, Chen G, Jo HJ, et al. (2012) Trouble at rest: how correlation patterns and group differences become distorted after global signal regression. Brain connectivity 2: 25-32.
79. Moats LC, (1996) Phonological spelling errors in the writing of dyslexic adolescents. Reading and Writing 8: 105-119.
80. Willcutt EG, Pennington BF, (2000) Comorbidity of reading disability and attention-deficit/hyperactivity disorder: differences by gender and subtype. J Learn Disabil 33: 179-191.
81. Shaywitz SE, Shaywitz BA, (2008) Paying attention to reading: the neurobiology of reading and dyslexia. Development and psychopathology 20: 1329-1349.
82. Amodio DM, Frith CD, (2006) Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci 7: 268-277.
83. Corbetta M, Shulman GL, (2002) Control of goal-directed and stimulus-driven attention in the brain. Nature reviews Neuroscience 3: 201-215.
84. Hoeft F, Hernandez A, McMillon G, Taylor-Hill H, Martindale JL, et al. (2006) Neural Basis of Dyslexia: A Comparison between Dyslexic and Nondyslexic Children Equated for Reading Ability. The Journal of Neuroscience 26: 10700-10708.
85. Pugh KR, Mencl WE, Shaywitz BA, Shaywitz SE, Fulbright RK, et al. (2000) The angular gyrus in developmental dyslexia: task-specific differences in functional connectivity within posterior cortex. Psychological science 11: 51-56.
86. Shaywitz BA, Shaywitz SE, Pugh KR, Mencl WE, Fulbright RK, et al. (2002) Disruption of posterior brain systems for reading in children with developmental dyslexia. Biological psychiatry 52: 101-110.
87. Corbetta M, (1998) Frontoparietal cortical networks for directing attention and the eye to visual locations: Identical, independent, or overlapping neural'Äâsystems? Proceedings of the National Academy of Sciences 95: 831-838.
88. Pessoa L, Rossi A, Japee S, Desimone R, Ungerleider LG, (2009) Attentional control during the transient updating of cue information. Brain Research 1247: 149-158.
89. Zorzi M, Barbiero C, Facoetti A, Lonciari I, Carrozzi M, et al. (2012) Extra-large letter spacing improves reading in dyslexia. Proceedings of the National Academy of Sciences of the United States of America.
90. Franceschini S, Gori S, Ruffino M, Pedrolli K, Facoetti A, (2012) A Causal Link between Visual Spatial Attention and Reading Acquisition. Current biology: CB 22: 814-819.
91. Gaab N, Gabrieli JD, Deutsch GK, Tallal P, Temple E, (2007) Neural correlates of rapid auditory processing are disrupted in children with developmental dyslexia and ameliorated with training: an fMRI study. Restorative neurology and neuroscience 25: 295-310.
92. Eden GF, Jones KM, Cappell K, Gareau L, Wood FB, et al. (2004) Neural changes following remediation in adult developmental dyslexia. Neuron 44: 411-422.
93. Shaywitz SE, Shaywitz BA, Fulbright RK, Skudlarski P, Mencl WE, et al. (2003) Neural systems for compensation and persistence: young adult outcome of childhood reading disability. Biological psychiatry 54: 25-33.
94. Temple E, Deutsch GK, Poldrack RA, Miller SL, Tallal P, 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. Dehaene S, Le Clec'H G, Poline J-B, 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.
96. Dehaene S, Cohen L, (2011) The unique role of the visual word form area in reading. Trends in Cognitive Sciences 15: 254-262.
97. Blau V, Reithler J, van Atteveldt N, Seitz J, Gerretsen P, et al. (2010) Deviant processing of letters and speech sounds as proximate cause of reading failure: a functional magnetic resonance imaging study of dyslexic children. Brain: a journal of neurology 133: 868-879.
98. van der Mark S, Bucher K, Maurer U, Schulz E, Brem S, et al. (2009) Children with dyslexia lack multiple specializations along the visual word-form (VWF) system. NeuroImage 47: 1940-1949.
99. van der Mark S, Klaver P, Bucher K, Maurer U, Schulz E, et al. (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.
100. Horwitz B, Rumsey JM, Donohue BC, (1998) Functional connectivity of the angular gyrus in normal reading and dyslexia. Proceedings of the National Academy of Sciences of the United States of America 95: 8939-8944.
101. Wandell BA, Dumoulin SO, Brewer AA, (2007) Visual field maps in human cortex. Neuron 56: 366-383.
102. Renier LA, Anurova I, De Volder AG, Carlson S, VanMeter J, et al. (2010) Preserved functional specialization for spatial processing in the middle occipital gyrus of the early blind. Neuron 68: 138-148.
103. Andrews-Hanna JR, Reidler JS, Sepulcre J, Poulin R, Buckner RL, (2010) Functional-Anatomic Fractionation of the Brain's Default Network. Neuron 65: 550-562.
104. Buckner RL, Andrews-Hanna JR, Schacter DL, (2008) The brain's default network: anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences 1124: 1-38.
105. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, et al. (2001) A default mode of brain function. Proceedings of the National Academy of Sciences 98: 676-682.
106. McCloskey M, Rapp B, (2000) Attention-referenced visual representations: evidence from impaired visual localization. Journal of experimental psychology Human perception and performance 26: 917-933.
107. Kelly AM, Uddin LQ, Biswal BB, Castellanos FX, Milham MP, (2008) Competition between functional brain networks mediates behavioral variability. NeuroImage 39: 527-537.
108. Fox MD, Zhang D, Snyder AZ, Raichle ME, (2009) The global signal and observed anticorrelated resting state brain networks. Journal of Neurophysiology 101: 3270-3283.
109. Kraemer HC, (1991) To increase power in randomized clinical trials without increasing sample size. Psychopharmacology bulletin 27: 217-224.
110. Odegard T, Ring J, Smith S, Biggan J, Black J, (2008) Differentiating the neural response to intervention in children with developmental dyslexia. Annals of Dyslexia 58: 1-14.
111. Ferrer E, Shaywitz BA, Holahan JM, Marchione K, Shaywitz SE, (2010) Uncoupling of reading and IQ over time: empirical evidence for a definition of dyslexia. Psychol Sci 21: 93-101.
112. Tanaka H, Black JM, Hulme C, Stanley LM, Kesler SR, et al. (2011) The brain basis of the phonological deficit in dyslexia is independent of IQ. Psychol Sci 22: 1442-1451.