Advertisement

Neural and Genetic Mechanisms of Dyslexia

  • Tracy M. Centanni
Chapter
  • 66 Downloads
Part of the Contemporary Clinical Neuroscience book series (CCNE)

Abstract

Dyslexia is a common neurodevelopmental disorder and is marked by the failure to acquire reading in spite of normal nonverbal intelligence and adequate schooling. In spite of the plethora of interventions on the market, none claim 100% success and many individuals with dyslexia never achieve age-appropriate reading skills. This result is likely due to an increasingly accepted level of heterogeneity in this population, not just in the behavioral deficits present but in the core neural and genetic mechanisms as well. The differences in genetics, especially, have led to significant challenges for researchers to determine the biological mechanisms underlying dyslexia and optimize customized intervention options. Animal models are appealing for this type of research, because individual genes can be manipulated and the results studied in an ethical manner. This approach has led to new insights on the neurological and genetic causes of dyslexia but raises new questions about how well these models represent the biological underpinnings of this disorder in humans. In this chapter, I discuss the history of mechanism research in humans with dyslexia, recent approaches to tackling these questions in animal models, and the relationship between these findings and those in humans. I also discuss potential applications for this approach in the future as well as the limitations of this method.

Keywords

Dyslexia Rodent Animal model Intervention Reading Plasticity Genetics 

Abbreviations

A1

Primary auditory cortex

DYS

Dyslexia

PA

Phonological awareness

RAN

Rapid automatized naming

SES

Socioeconomic status

SNP

Single nucleotide polymorphism

TD

Typically developing

References

  1. Bates, T. C., Luciano, M., Medland, S. E., Montgomery, G. W., Wright, M. J., & Martin, N. G. (2011). Genetic variance in a component of the language acquisition device: ROBO1 polymorphisms associated with phonological buffer deficits. Behavior Genetics, 41(1), 50–57.PubMedCrossRefGoogle Scholar
  2. Boets, B., de Beeck, H., & Vandermosten, M. (2013). Intact but less accessible phonetic representations in adults with dyslexia. Science, 342(6163), 1251–1254.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Burbridge, T. J., Wang, Y., Volz, A. J., Peschansky, V. J., Lisann, L., Galaburda, A. M., … Rosen, G. D. (2008). Postnatal analysis of the effect of embryonic knockdown and overexpression of candidate dyslexia susceptibility gene homolog Dcdc2 in the rat. Neuroscience, 152(3), 723–733.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Cao, F., Bitan, T., Chou, T.-L., Burman, D. D., & Booth, J. R. (2006). Deficient orthographic and phonological representations in children with dyslexia revealed by brain activation patterns. Journal of Child Psychology and Psychiatry, 47(10), 1041–1050.  https://doi.org/10.1111/j.1469-7610.2006.01684.xCrossRefPubMedGoogle Scholar
  5. Centanni, T., Booker, A., Chen, F., Sloan, A., Carraway, R., Rennaker, R., … Kilgard, M. (2016). Knockdown of dyslexia-gene Dcdc2 interferes with speech sound discrimination in continuous streams. Journal of Neuroscience, 36(17), 4895–4906.PubMedCrossRefGoogle Scholar
  6. Centanni, T., Booker, A., Sloan, A., Chen, F., Maher, B. J., Carraway, R. S., … Kilgard, M. P. (2013). Knockdown of the dyslexia-associated gene Kiaa0319 impairs temporal responses to speech stimuli in rat primary auditory cortex. Cerebral Cortex, 24(7), 1753–1766.  https://doi.org/10.1093/cercor/bht028PubMedCrossRefGoogle Scholar
  7. Centanni, T., Chen, F., Booker, A., Engineer, C., Sloan, A., Rennaker, R., … Kilgard, M. (2014). Speech sound processing deficits and training-induced neural plasticity in rats with dyslexia gene knockdown. PLOS ONE, 9(5), e98439.  https://doi.org/10.1371/journal.pone.0098439CrossRefPubMedPubMedCentralGoogle Scholar
  8. Centanni, T. M., Sloan, A. M., Reed, A. C., Engineer, C. T., II, R, R., & Kilgard, M. P. (2013). Detection and identification of speech sounds using cortical activity patterns. Neuroscience, 258, 292–306.PubMedPubMedCentralCrossRefGoogle Scholar
  9. Centanni, T., Pantazis, D., Truong, D., Gruen, J., Gabrieli, J., & Hogan, T. (2018). Increased variability of stimulus-driven cortical responses is associated with genetic variability in children with and without dyslexia. Developmental Cognitive Neuroscience.  https://doi.org/10.1016/j.dcn.2018.05.008PubMedPubMedCentralCrossRefGoogle Scholar
  10. Centanni, T., Sanmann, J., Green, J., Iuzzini-Seigel, J., Bartlett, C., Sanger, W., & Hogan, T. (2015). The role of candidate-gene CNTNAP2 in childhood apraxia of speech and specific language impairment. American Journal of Medical Genetics, Part B, 168(7), 536–543.CrossRefGoogle Scholar
  11. Che, A., Girgenti, M. J., & LoTurco, J. (2014). The dyslexia-associated gene Dcdc2 is required for spike-timing precision in mouse neocortex. Biological Psychiatry, 76(5), 387–396.  https://doi.org/10.1016/j.biopsych.2013.08.018CrossRefPubMedGoogle Scholar
  12. Che, A., Truong, D., Fitch, R., & LoTurco, J. (2016). Mutation of the dyslexia-associated gene Dcdc2 enhances glutamatergic synaptic transmission between layer 4 neurons in mouse neocortex. Cerebral Cortex, 26(9), 3705–3718.PubMedCrossRefGoogle Scholar
  13. Choudhry, Z., Rikani, A. A., Choudhry, A. M., Tariq, S., Zakaria, F., Asghar, M. W., … Mobassarah, N. J. (2014). Sonic hedgehog signalling pathway: A complex network. Annals of Neurosciences, 21(1), 28–31.  https://doi.org/10.5214/ans.0972.7531.210109CrossRefPubMedPubMedCentralGoogle Scholar
  14. Ciani, L., & Salinas, P. C. (2005). WNTS in the vertebrate nervous system: From patterning to neuronal connectivity. Nature Reviews Neuroscience, 6(5), 351–362.  https://doi.org/10.1038/nrn1665CrossRefPubMedGoogle Scholar
  15. Cicchini, G. M., Marino, C., Mascheretti, S., Perani, D., & Morrone, M. C. (2015). Strong motion deficits in dyslexia associated with DCDC2 gene alteration. Journal of Neuroscience, 35(21), 8059–8064.  https://doi.org/10.1523/JNEUROSCI.5077-14.2015CrossRefPubMedGoogle Scholar
  16. Condro, M. C., & White, S. a. (2014). Recent advances in the genetics of vocal learning. Comparative Cognition & Behavior Reviews, 9, 75–98.  https://doi.org/10.3819/ccbr.2014.90003CrossRefGoogle Scholar
  17. Currier, T. A., Etchegaray, M. A., Haight, J. L., Galaburda, A. M., & Rosen, G. D. (2011). The effects of embryonic knockdown of the candidate dyslexia susceptibility gene homologue Dyx1c1 on the distribution of GABAergic neurons in the cerebral cortex. Neuroscience, 172, 535–546.PubMedCrossRefGoogle Scholar
  18. Darki, F., & Peyrard-Janvid, M. (2014). DCDC2 polymorphism is associated with left temporoparietal gray and white matter structures during development. Journal of Neuroscience, 34(43), 14455–14462.PubMedCrossRefGoogle Scholar
  19. Darki, F., Peyrard-Janvid, M., Matsson, H., Kere, J., & Klingberg, T. (2012). Three dyslexia susceptibility genes, DYX1C1, DCDC2, and KIAA0319, affect temporo-parietal white matter structure. Biological Psychiatry, 72(8), 671–676.PubMedCrossRefGoogle Scholar
  20. Denckla, M., & Rudel, R. (1976). Rapid ’automatized’naming (RAN): Dyslexia differentiated from other learning disabilities. Neuropsychologia, 14(4), 471–479.PubMedCrossRefGoogle Scholar
  21. Dennis, M. Y., Paracchini, S., Scerri, T. S., Prokunina-Olsson, L., Knight, J. C., Wade-Martins, R., … Monaco, A. P. (2009). A common variant associated with dyslexia reduces expression of the KIAA0319 gene. PLoS Genetics, 5(3), e1000436.PubMedPubMedCentralCrossRefGoogle Scholar
  22. Farquharson, K., Centanni, T. M., Franzluebbers, C. E., & Hogan, T. P. (2014). Phonological and lexical influences on phonological awareness in children with specific language impairment and dyslexia. Frontiers in Psychology, 5(838).  https://doi.org/10.3389/fpsyg.2014.00838
  23. Fisher, S. E., & DeFries, J. C. (2002). Developmental dyslexia: Genetic dissection of a complex cognitive trait. Nature Reviews Neuroscience, 3(10), 767–780.PubMedCrossRefGoogle Scholar
  24. Francks, C., Paracchini, S., Smith, S. D., Richardson, A. J., Scerri, T. S., Cardon, L. R., … Pennington, B. F. (2004). A 77-kilobase region of chromosome 6p22. 2 is associated with dyslexia in families from the United Kingdom and from the United States. The American Journal of Human Genetics, 75(6), 1046–1058.PubMedCrossRefGoogle Scholar
  25. Furnes, B., & Samuelsson, S. (2010). Predicting reading and spelling difficulties in transparent and opaque orthographies: A comparison between Scandinavian and US/Australian children. Dyslexia, 16(2), 119–142.  https://doi.org/10.1002/dys.401CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gabel, L., Marin, I., LoTurco, J., Che, A., Murphy, C., Manglani, M., & Kass, S. (2011). Mutation of the dyslexia-associated gene Dcdc2 impairs LTM and visuo-spatial performance in mice. Genes, Brain, and Behavior, 10(8), 868–875.PubMedPubMedCentralCrossRefGoogle Scholar
  27. Galaburda, A. M., & Kemper, T. L. (1979). Cytoarchitectonic abnormalities in developmental dyslexia: A case study. Annals of Neurology, 6(2), 94–100.PubMedCrossRefGoogle Scholar
  28. Galaburda, A. M., LoTurco, J., Ramus, F., Fitch, R. H., & Rosen, G. D. (2006). From genes to behavior in developmental dyslexia. Nature Neuroscience, 9(10), 1213–1217.PubMedCrossRefGoogle Scholar
  29. Galaburda, A. M., Sherman, G. F., Rosen, G. D., Aboitiz, F., & Geschwind, N. (1985). Developmental dyslexia: Four consecutive patients with cortical anomalies. Annals of Neurology, 18(2), 222–233.PubMedCrossRefGoogle Scholar
  30. Georgiou, G. K., Parrila, R., & Liao, C.-H. (2008). Rapid naming speed and reading across languages that vary in orthographic consistency. Reading and Writing, 21(9), 885–903.  https://doi.org/10.1007/s11145-007-9096-4CrossRefGoogle Scholar
  31. Gillon, G. T. (2005). Phonological awareness. Language Speech and Hearing Services in Schools, 36(4), 281.  https://doi.org/10.1044/0161-1461(2005/028)CrossRefGoogle Scholar
  32. Gori, S., Mascheretti, S., & Giora, E. (2014). The DCDC2 intron 2 deletion impairs illusory motion perception unveiling the selective role of magnocellular-dorsal stream in reading (dis)ability. Cerebral Cortex, 25(6), 1685–1695.PubMedCrossRefGoogle Scholar
  33. Groszer, M., Keays, D., Deacon, R. M. J., de Bono, J. P., Prasad-Mulcare, S., Gaub, S., … Fisher, S. E. (2008). Impaired synaptic plasticity and motor learning in mice with a point mutation implicated in human speech deficits. Current Biology, 18(5), 354–362.  https://doi.org/10.1016/j.cub.2008.01.060CrossRefPubMedPubMedCentralGoogle Scholar
  34. Guidi, L. G., Mattley, J., Martinez-Garay, I., Monaco, A. P., Linden, J. F., Velayos-Baeza, A., & Molnár, Z. (2017). Knockout mice for dyslexia susceptibility gene homologs KIAA0319 and KIAA0319L have unaffected neuronal migration but display abnormal auditory processing. Cerebral Cortex, 27(12), 5831–5845.  https://doi.org/10.1093/cercor/bhx269CrossRefPubMedGoogle Scholar
  35. Haesler, S., Rochefort, C., Georgi, B., Licznerski, P., Osten, P., & Scharff, C. (2007). Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus area X. PLoS Biology, 5(12), e321.  https://doi.org/10.1371/journal.pbio.0050321CrossRefPubMedPubMedCentralGoogle Scholar
  36. Heim, S., Pape-Neumann, J., van Ermingen-Marbach, M., Brinkhaus, M., & Grande, M. (2014). Shared vs. specific brain activation changes in dyslexia after training of phonology, attention, or reading. Brain Structure & Function (Snowling 2000).  https://doi.org/10.1007/s00429-014-0784-yPubMedCrossRefGoogle Scholar
  37. Hoeft, F., McCandliss, B. D., Black, J. M., Gantman, A., Zakerani, N., Hulme, C., … Gabrieli, J. D. E. (2011). Neural systems predicting long-term outcome in dyslexia. Proceedings of the National Academy of Sciences, 108(1), 361–366.  https://doi.org/10.1073/pnas.1008950108CrossRefGoogle Scholar
  38. Hornickel, J., & Kraus, N. (2013). Unstable representation of sound: A biological marker of dyslexia. Journal of Neuroscience, 33(8), 3500–3504.PubMedCrossRefGoogle Scholar
  39. Humphreys, P., Kaufmann, W. E., & Galaburda, A. M. (1990). Developmental dyslexia in women: Neuropathological findings in three patients. Annals of Neurology, 28(6), 727–738.PubMedCrossRefGoogle Scholar
  40. Kato, M., Okanoya, K., Koike, T., Sasaki, E., Okano, H., Watanabe, S., & Iriki, A. (2014). Human speech-and reading-related genes display partially overlapping expression patterns in the marmoset brain. Brain and Language, 133, 26–38.PubMedCrossRefGoogle Scholar
  41. Kidd, T., Brose, K., Mitchell, K., Fetter, R., Tessier-Lavigne, M., Goodman, C., & Tear, G. (1998). Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell, 92(2), 205–215.PubMedCrossRefGoogle Scholar
  42. Korhonen, T. (1995). The persistence of rapid naming problems in children with reading disabilities a nine-year follow-up. Journal of Learning Disabilities, 28(4), 232–239.PubMedCrossRefGoogle Scholar
  43. Lai, C. S., Fisher, S. E., Hurst, J. A., Vargha-Khadem, F., & Monaco, A. P. (2001). A forkhead-domain gene is mutated in a severe speech and language disorder. Nature, 413(6855), 519–523.  https://doi.org/10.1038/35097076CrossRefPubMedGoogle Scholar
  44. Lamminmäki, S., Massinen, S., Nopola-Hemmi, J., Kere, J., & Hari, R. (2012). Human ROBO1 regulates interaural interaction in auditory pathways. Journal of Neuroscience, 32(3), 966–971.PubMedCrossRefGoogle Scholar
  45. Landerl, K., Ramus, F., Moll, K., Lyytinen, H., Leppänen, P. H. T., Lohvansuu, K., … Schulte-Körne, G. (2013). Predictors of developmental dyslexia in European orthographies with varying complexity. Journal of Child Psychology and Psychiatry, 54(6), 686–694.  https://doi.org/10.1111/jcpp.12029CrossRefPubMedGoogle Scholar
  46. Landerl, K., Wimmer, H., & Frith, U. (1997). The impact of orthographic consistency on dyslexia: A German-English comparison. Cognition, 63(3), 315–334.  https://doi.org/10.1016/S0010-0277(97)00005-XCrossRefPubMedGoogle Scholar
  47. Lehongre, K., Ramus, F., Villiermet, N., Schwartz, D., & Giraud, A. L. (2011). Altered low-gamma sampling in auditory cortex accounts for the three main facets of dyslexia. Neuron, 72(6), 1080–1090.PubMedCrossRefGoogle Scholar
  48. Lervåg, A., & Hulme, C. (2009). Rapid automatized naming (RAN) taps a mechanism that places constraints on the development of early reading fluency. Psychological Science, 20(8), 1040–1048.  https://doi.org/10.1111/j.1467-9280.2009.02405.xCrossRefPubMedGoogle Scholar
  49. Lind, P. A., Luciano, M., Wright, M. J., Montgomery, G. W., Martin, N. G., & Bates, T. C. (2010). Dyslexia and DCDC2: Normal variation in reading and spelling is associated with DCDC2 polymorphisms in an Australian population sample. European Journal of Human Genetics, 18(6), 668–673.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Lovett, M. W. (1984). The search for subtypes of specific reading disability: Reflections from a cognitive perspective. Annals of Dyslexia, 34(1), 153–178.  https://doi.org/10.1007/BF02663618CrossRefPubMedGoogle Scholar
  51. Marino, C., Giorda, R., Lorusso, M. L., Vanzin, L., Salandi, N., Nobile, M., … Battaglia, M. (2005). A family-based association study does not support DYX1C1 on 15q21.3 as a candidate gene in developmental dyslexia. European Journal of Human Genetics, 13(4), 491–499.PubMedCrossRefGoogle Scholar
  52. Martinez-Garay, I., Guidi, L. G., Holloway, Z. G., Bailey, M. A. G., Lyngholm, D., Schneider, T., … Monaco, A. P. (2016). Normal radial migration and lamination are maintained in dyslexia-susceptibility candidate gene homolog Kiaa0319 knockout mice. Brain Structure & Function, 1–18.  https://doi.org/10.1007/s00429-016-1282-1PubMedCrossRefGoogle Scholar
  53. Massinen, S., Hokkanen, M.-E., Matsson, H., Tammimies, K., Tapia-Páez, I., Dahlström-Heuser, V., … Kere, J. (2011). Increased expression of the dyslexia candidate gene DCDC2 affects length and signaling of primary cilia in neurons. PLOS ONE, 6(6), e20580.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Meng, H., Powers, N. R., Tang, L., Cope, N. A., Zhang, P.-X., Fuleihan, R., … Gruen, J. R. (2011). A dyslexia-associated variant in DCDC2 changes gene expression. Behavior Genetics, 41(1), 58–66.  https://doi.org/10.1007/s10519-010-9408-3CrossRefPubMedGoogle Scholar
  55. Meyer, M. S., Wood, F. B., Hart, L. A., & Felton, R. H. (1998). Selective predictive value of RAN in poor readers. Journal of Learning Disabilities, 31(2), 106–117.PubMedCrossRefGoogle Scholar
  56. Meyler, A., Keller, T. A., Cherkassky, V. L., Gabrieli, J. D. E., & Just, M. A. (2008). Modifying the brain activation of poor readers during sentence comprehension with extended remedial instruction: A longitudinal study of neuroplasticity. Neuropsychologia, 46(10), 2580–2592.  https://doi.org/10.1016/j.neuropsychologia.2008.03.012CrossRefPubMedPubMedCentralGoogle Scholar
  57. Monzalvo, K., Fluss, J., Billard, C., & Dehaene, S. (2012). Cortical networks for vision and language in dyslexic and normal children of variable socio-economic status. Neuroimage, 61(1), 258–274.PubMedCrossRefGoogle Scholar
  58. Neef, N. E., Müller, B., Liebig, J., Schaadt, G., Grigutsch, M., Gunter, T. C., … Friederici, A. D. (2017). Dyslexia risk gene relates to representation of sound in the auditory brainstem. Developmental Cognitive Neuroscience.  https://doi.org/10.1016/j.dcn.2017.01.008PubMedPubMedCentralCrossRefGoogle Scholar
  59. Neef, N. E., Schaadt, G., & Friederici, A. D. (2016). Auditory brainstem responses to stop consonants predict literacy. Clinical Neurophysiology, 128(3), 484–494.  https://doi.org/10.1016/j.clinph.2016.12.007CrossRefPubMedGoogle Scholar
  60. Norton, E. S., Black, J. M., Stanley, L. M., Tanaka, H., Gabrieli, J. D. E., Sawyer, C., & Hoeft, F. (2014). Functional neuroanatomical evidence for the double-deficit hypothesis of developmental dyslexia. Neuropsychologia, 61(1), 235–246.  https://doi.org/10.1016/j.neuropsychologia.2014.06.015CrossRefPubMedPubMedCentralGoogle Scholar
  61. Norton, E., & Wolf, M. (2012). Rapid automatized naming (RAN) and reading fluency: Implications for understanding and treatment of reading disabilities. Annual Review of Psychology, 63, 427–452.PubMedCrossRefGoogle Scholar
  62. Paracchini, S., Steer, C., Buckingham, L.-L., Morris, A., Ring, S., Scerri, T., … Golding, J. (2008). Association of the KIAA0319 dyslexia susceptibility gene with reading skills in the general population. American Journal of Psychiatry, 165(12), 1576–1584.PubMedCrossRefGoogle Scholar
  63. Paracchini, S., Thomas, A., Castro, S., Lai, C., Paramasivam, M., Wang, Y., … Monaco, A. (2006). The chromosome 6p22 haplotype associated with dyslexia reduces the expression of KIAA0319, a novel gene involved in neuronal migration. Human Molecular Genetics, 15(10), 1659–1666.PubMedCrossRefGoogle Scholar
  64. Paulesu, E., Frith, U., Snowling, M., Gallagher, A., Morton, J., Frackowiak, R. S. J., & Frith, C. D. (1996). Is developmental dyslexia a disconnection syndrome? Evidence from PET scanning. Brain, 119(1), 143–157.PubMedCrossRefGoogle Scholar
  65. Pennington, B. F., Gilger, J. W., Pauls, D., Smith, S. A., Smith, S. D., & DeFries, J. C. (1991). Evidence for major gene transmission of developmental dyslexia. JAMA, 266(11), 1527–1534.Google Scholar
  66. Penolazzi, B., Spironelli, C., Vio, C., & Angrilli, A. (2010). Brain plasticity in developmental dyslexia after phonological treatment: A beta EEG band study. Behavioural Brain Research, 209(1), 179–182.PubMedCrossRefGoogle Scholar
  67. Perrachione, T. K., Del Tufo, S., Winter, R., Murtagh, J., Cyr, A., Chang, P., … Gabrieli, J. (2016). Dysfunction of rapid neural adaptation in dyslexia. Neuron, 92(6), 1383–1397.PubMedPubMedCentralCrossRefGoogle Scholar
  68. Peter, B., Raskind, W. H., Matsushita, M., Lisowski, M., Vu, T., Berninger, V. W., … Brkanac, Z. (2011). Replication of CNTNAP2 association with nonword repetition and support for FOXP2 association with timed reading and motor activities in a dyslexia family sample. Journal of Neurodevelopmental Disorders, 3(1), 39–49.  https://doi.org/10.1007/s11689-010-9065-0CrossRefPubMedGoogle Scholar
  69. Peterson, R. L., & Pennington, B. F. (2012). Developmental dyslexia. The Lancet, 379(9830), 1997–2007.CrossRefGoogle Scholar
  70. Petrin, A. L., Giacheti, C. M., Maximino, L. P., Abramides, D. V. M., Zanchetta, S., Rossi, N. F., … Murray, J. C. (2010). Identification of a microdeletion at the 7q33-q35 disrupting the CNTNAP2 gene in a Brazilian stuttering case. American Journal of Medical Genetics Part A, 152A(12), 3164–3172.  https://doi.org/10.1002/ajmg.a.33749CrossRefPubMedPubMedCentralGoogle Scholar
  71. Pinel, P., Fauchereau, F., Moreno, A., Barbot, A., Lathrop, M., Zelenika, D., … Dehaene, S. (2012). Genetic variants of FOXP2 and KIAA0319/TTRAP/THEM2 locus are associated with altered brain activation in distinct language-related regions. Journal of Neuroscience, 32(3), 817–825.  https://doi.org/10.1523/JNEUROSCI.5996-10.2012CrossRefPubMedGoogle Scholar
  72. Poliak, S., & Gollan, L. (2001). Localization of Caspr2 in myelinated nerves depends on axon–glia interactions and the generation of barriers along the axon. Journal of Neuroscience, 21(19), 7568–7575.PubMedCrossRefGoogle Scholar
  73. Powers, N. R., Eicher, J. D., Miller, L. L., Kong, Y., Smith, S. D., Pennington, B. F., … Gruen, J. R. (2016). The regulatory element READ1 epistatically influences reading and language, with both deleterious and protective alleles. Journal of Medical Genetics, 53(3), 163–171.  https://doi.org/10.1136/jmedgenet-2015-103418CrossRefPubMedGoogle Scholar
  74. Raca, G., Baas, B. S., Kirmani, S., Laffin, J. J., Jackson, C., Strand, E., … Shriberg, L. D. (2013). Childhood apraxia of speech (CAS) in two patients with 16p11.2 microdeletion syndrome. European Journal of Human Genetics: EJHG, 21(4), 455–459.  https://doi.org/10.1038/ejhg.2012.165CrossRefPubMedGoogle Scholar
  75. Ramus, F., & Szenkovits, G. (2008). What phonological deficit? The Quarterly Journal of Experimental Psychology, 61(1), 129–141.PubMedCrossRefGoogle Scholar
  76. Ranasinghe, K. G., Vrana, W. A., Matney, C. J., & Kilgard, M. P. (2012). Neural mechanisms supporting robust discrimination of spectrally and temporally degraded speech. JARO Journal of the Association for Research in Otolaryngology, 13(4), 527–542.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Rasband, M. (2004). It’s “juxta” potassium channel. Journal of Neuroscience Research.  https://doi.org/10.1002/jnr.20073/full
  78. Richards, T. L., & Berninger, V. W. (2008). Abnormal fMRI connectivity in children with dyslexia during a phoneme task: Before but not after treatment. Journal of Neurolinguistics, 21(4), 294–304.  https://doi.org/10.1016/j.jneuroling.2007.07.002CrossRefPubMedPubMedCentralGoogle Scholar
  79. Romeo, R. R., Christodoulou, J. A., Halverson, K. K., Murtagh, J., Cyr, A. B., Schimmel, C., … Gabrieli, J. D. E. (2017). Socioeconomic status and reading disability: Neuroanatomy and plasticity in response to intervention. Cerebral Cortex, 1–16.  https://doi.org/10.1093/cercor/bhx131CrossRefGoogle Scholar
  80. Sasaki, E., Suemizu, H., Shimada, A., Hanazawa, K., Oiwa, R., Kamioka, M., … Nomura, T. (2009). Generation of transgenic non-human primates with germline transmission. Nature, 459(7246), 523–527.  https://doi.org/10.1038/nature08090CrossRefPubMedGoogle Scholar
  81. Scarborough, H. S. (1998). Predicting the future achievement of second graders with reading disabilities: Contributions of phonemic awareness, verbal memory, rapid naming, and IQ. Annals of Dyslexia, 48(1), 115–136.  https://doi.org/10.1007/s11881-998-0006-5CrossRefGoogle Scholar
  82. Scerri, T. S., Morris, A. P., Buckingham, L. L., Newbury, D. F., Miller, L. L., Monaco, A. P., … Paracchini, S. (2011). DCDC2, KIAA0319 and CMIP are associated with reading-related traits. Biological Psychiatry, 70(3), 237–245.PubMedPubMedCentralCrossRefGoogle Scholar
  83. Scerri, T., & Schulte-Körne, G. (2010). Genetics of developmental dyslexia. European Child & Adolescent Psychiatry.  https://doi.org/10.1007/s00787-009-0081-0CrossRefGoogle Scholar
  84. Schulte-Körne, G., Deimel, W., Bartling, J., & Remschmidt, H. (2001). Speech perception deficit in dyslexic adults as measured by mismatch negativity (MMN). International Journal of Psychophysiology, 40(1), 77–87.PubMedCrossRefGoogle Scholar
  85. Serrano, F., & Defior, S. (2008). Dyslexia speed problems in a transparent orthography. Annals of Dyslexia, 58(1), 81.PubMedCrossRefGoogle Scholar
  86. Shetake, J. A., Wolf, J. T., Cheung, R. J., Engineer, C. T., Ram, S. K., & Kilgard, M. P. (2011). Cortical activity patterns predict robust speech discrimination ability in noise. European Journal of Neuroscience, 34(11), 1823–1838.PubMedCrossRefGoogle Scholar
  87. Swan, D., & Goswami, U. (1997). Phonological awareness deficits in developmental dyslexia and the phonological representations hypothesis. Journal of Experimental Child Psychology, 66(1), 18–41.PubMedCrossRefGoogle Scholar
  88. Szalkowski, C. E., Fiondella, C. F., Truong, D. T., Rosen, G. D., LoTurco, J. J., & Fitch, R. H. (2012). The effects of Kiaa0319 knockdown on cortical and subcortical anatomy in male rats. International Journal of Developmental Neuroscience, 31(2), 116–122.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Szalkowski, C. E., Fiondella, C. G., Galaburda, A. M., Rosen, G. D., LoTurco, J. J., & Fitch, R. H. (2012). Neocortical disruption and behavioral impairments in rats following in utero RNAi of candidate dyslexia risk gene Kiaa0319. International Journal of Developmental Neuroscience, 30(4), 293–302.PubMedPubMedCentralCrossRefGoogle Scholar
  90. Temple, E., Deutsch, G. K., Poldrack, R. A., Miller, S. L., Tallal, P., Merzenich, M. M., & Gabrieli, J. D. E. (2003). Neural deficits in children with dyslexia ameliorated by behavioral remediation: Evidence from functional MRI. Proceedings of the National Academy of Sciences, 100(5), 2860.CrossRefGoogle Scholar
  91. Threlkeld, S. W., McClure, M. M., Bai, J., Wang, Y., LoTurco, J. J., Rosen, G. D., & Fitch, R. H. (2007). Developmental disruptions and behavioral impairments in rats following in utero RNAi of Dyx1c1. Brain Research Bulletin, 71(5), 508–514.PubMedCrossRefGoogle Scholar
  92. Truong, D. T., Che, A., Rendall, A. R., Szalkowski, C. E., LoTurco, J. J., Galaburda, A. M., & Holly Fitch, R. (2014). Mutation of Dcdc2 in mice leads to impairments in auditory processing and memory ability. Genes, Brain, and Behavior, 13(8), 802–811.  https://doi.org/10.1111/gbb.12170CrossRefPubMedPubMedCentralGoogle Scholar
  93. Tsui, D., Vessey, J. P., Tomita, H., Kaplan, D. R., & Miller, F. D. (2013). FoxP2 regulates neurogenesis during embryonic cortical development. Journal of Neuroscience, 33(1), 244–258.  https://doi.org/10.1523/JNEUROSCI.1665-12.2013PubMedCrossRefGoogle Scholar
  94. Vernes, S. C., Newbury, D. F., Abrahams, B. S., Winchester, L., Nicod, J., Groszer, M., … Fisher, S. E. (Eds.). (2008). A functional genetic link between distinct developmental language disorders. The New England Journal of Medicine, 359(22), 2337–2345.  https://doi.org/10.1056/NEJMoa0802828PubMedCrossRefGoogle Scholar
  95. Wagner, R., Torgesen, J., & Pearson, N. (2013). Comprehensive test of phonological processing (2nd ed.). Austin, TX: Pro-Ed.Google Scholar
  96. Wang, Y., Yin, X., Rosen, G., Gabel, L., Guadiana, S. M., Sarkisian, M. R., … LoTurco, J. J. (2011). Dcdc2 knockout mice display exacerbated developmental disruptions following knockdown of Dcx. Neuroscience, 190, 398–408.PubMedPubMedCentralCrossRefGoogle Scholar
  97. Whalley, H. C., O’Connell, G., Sussmann, J. E., Peel, A., Stanfield, A. C., Hayiou-Thomas, M. E., … Hall, J. (2011). Genetic variation in CNTNAP2 alters brain function during linguistic processing in healthy individuals. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 156(8), 941–948.  https://doi.org/10.1002/ajmg.b.31241CrossRefGoogle Scholar
  98. Wilcke, A., Ligges, C., Burkhardt, J., Alexander, M., Wolf, C., Quente, E., … Kirsten, H. (2012). Imaging genetics of FOXP2 in dyslexia. European Journal of Human Genetics, 20(2), 224–229.  https://doi.org/10.1038/ejhg.2011.160CrossRefPubMedGoogle Scholar
  99. Wolf, M., Barzillai, M., Gottwald, S., Miller, L., Spencer, K., Norton, E., … Morris, R. (2009). The RAVE-O intervention: Connecting neuroscience to the classroom. Mind, Brain, and Education, 3(2), 84–93.  https://doi.org/10.1111/j.1751-228X.2009.01058.xCrossRefGoogle Scholar
  100. Wolf, M., & Bowers, P. (1999). The double-deficit hypothesis for the developmental dyslexias. Journal of Educational Psychology, 91(3), 415.CrossRefGoogle Scholar
  101. Wolf, M., Miller, L., & Donnelly, K. (2000). Retrieval, automaticity, vocabulary elaboration, orthography (RAVE-O). Journal of Learning Disabilities, 33(4), 375–386.  https://doi.org/10.1177/002221940003300408CrossRefPubMedGoogle Scholar
  102. Ypsilanti, A., Zagar, Y., & Chedotal, C. (2010). Moving away from the midline: New developments for Slit and Robo. Development, 137(12), 1939–1952.PubMedCrossRefGoogle Scholar
  103. Žarić, G., Fraga González, G., Tijms, J., van der Molen, M. W., Blomert, L., & Bonte, M. (2014). Reduced neural integration of letters and speech sounds in dyslexic children scales with individual differences in reading fluency. PLOS ONE, 9(10), e110337.  https://doi.org/10.1371/journal.pone.0110337CrossRefPubMedPubMedCentralGoogle Scholar
  104. Zhang, Y., Li, J., Song, S., Tardif, T., Burmeister, M., Villafuerte, S. M., … Shu, H. (2016). Association of DCDC2 polymorphisms with normal variations in reading abilities in a Chinese population. PLOS ONE, 11(4), e0153603.  https://doi.org/10.1371/journal.pone.0153603CrossRefPubMedPubMedCentralGoogle Scholar
  105. Ziegler, J. C., Bertrand, D., Tóth, D., Csépe, V., Reis, A., Faísca, L., … Blomert, L. (2010). Orthographic depth and its impact on universal predictors of reading. Psychological Science, 21(4), 551–559.  https://doi.org/10.1177/0956797610363406CrossRefPubMedGoogle Scholar
  106. Ziegler, J. C., Pech-Georgel, C., George, F., & Lorenzi, C. (2009). Speech-perception-in-noise deficits in dyslexia. Developmental Science, 12(5), 732–745.PubMedCrossRefGoogle Scholar
  107. Zou, L., Chen, W., Shao, S., Sun, Z., Zhong, R., Shi, J., … Song, R. (2012). Genetic variant in KIAA0319, but not in DYX1C1, is associated with risk of dyslexia: An integrated meta-analysis. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 159(8), 970–976.CrossRefGoogle Scholar
  108. Zoubrinetzky, R., Bielle, F., & Valdois, S. (2014). New insights on developmental dyslexia subtypes: Heterogeneity of mixed reading profiles. PLOS ONE, 9(6), e99337.  https://doi.org/10.1371/journal.pone.0099337CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Tracy M. Centanni
    • 1
  1. 1.Psychology DepartmentTexas Christian UniversityFort WorthUSA

Personalised recommendations