CoChat
Sign Up
Cited by 59Reading and Literacy DevelopmentNeurogenesis and neuroplasticity mechanismsLanguage Development and Disorders

The neuronal migration hypothesis of dyslexia: a critical evaluation 30 years on.

Open access
Guidi, Luiz G., Velayos‐Baeza, Antonio, Martinez‐Garay, Isabel, Monaco, Anthony P., Paracchini, Silvia, Bishop, Dorothy V. M., Molnár, Zoltán·2018·European Journal of Neuroscience
DOI 10.1111/ejn.14149PMC PMC6282621
Open this paper in CoChat — free accountOpen PDF

Abstract

The capacity for language is one of the key features underlying the complexity of human cognition and its evolution. However, little is known about the neurobiological mechanisms that mediate normal or impaired linguistic ability. For developmental dyslexia, early postmortem studies conducted in the 1980s linked the disorder to subtle defects in the migration of neurons in the developing neocortex. These early studies were reinforced by human genetic analyses that identified dyslexia susceptibility genes and subsequent evidence of their involvement in neuronal migration. In this review, we examine recent experimental evidence that does not support the link between dyslexia and neuronal migration. We critically evaluate gene function studies conducted in rodent models and draw attention to the lack of robust evidence from histopathological and imaging studies in humans. Our review suggests that the neuronal migration hypothesis of dyslexia should be reconsidered, and the neurobiological basis of dyslexia should be approached with a fresh start.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1111/ejn.14149

Cites

9 of 9 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Disruptions of neuronal migration and neurite outgrowth contribute importantly to the pathogenesis of dyslexia.

    “The molecular pathophysiology of dyslexia is less understood, but lines of evidence suggest that disruptions of neuronal migration and neurite outgrowth contribute importantly to the pathogenesis of the disease (Poelmans et al., 2011; Shao et al., 2016; Guidi et al., 2018).”

    From Two Autism/Dyslexia Linked Variations of DOCK4 Disrupt the Gene Function on Rac1/Rap1 Activation, Neurite Outgrowth, and Synapse Development (2020) · cites this paper as Guidi et al., 2018

    The Introduction describes why neuronal migration and axon growth became proposed explanations for dyslexia, but says the evidence for the migration hypothesis is not very robust and the link should be treated with caution. The Conclusion and Future Directions says further studies are needed to establish how far migration abnormalities cause dyslexia. Thus, the review does not support the attributed suggestion that these disruptions contribute importantly to its pathogenesis. (LLM, conf=0.83)

    Checked by a reasoning model — may be wrong.

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 195

  1. Adams, A. K., Smith, S. D., Truong, D. T., Willcutt, E. G., Olson, R. K., DeFries, J. C., … Gruen, J. R. (2017). Enrichment of putatively damaging rare variants in the DYX2 locus and the reading‐related genes CCDC136 and FLNC. Human Genetics, 136, 1395– 1405. 10.1007/s00439-017-1838-z 28866788 PMC5702371 · DOI
  2. Adler, W. T., Platt, M. P., Mehlhorn, A. J., Haight, J. L., Currier, T. A., Etchegaray, M. A., … Rosen, G. D. (2013). Position of neocortical neurons transfected at different gestational ages with shRNA targeted against candidate dyslexia susceptibility genes. PLoS One, 8, e65179 10.1371/journal.pone.0065179 23724130 PMC3665803 · DOI
  3. Adorjan, I., Ahmed, B., Feher, V., Torso, M., Krug, K., Esiri, M., … Szele, F. G. (2017). Calretinin interneuron density in the caudate nucleus is lower in autism spectrum disorder. Brain, 140, 2028– 2040. 10.1093/brain/awx131 29177493 PMC6624365 · DOI
  4. Altarelli, I., Leroy, F., Monzalvo, K., Fluss, J., Billard, C., Dehaene‐Lambertz, G., … Ramus, F. (2014). Planum temporale asymmetry in developmental dyslexia: Revisiting an old question. Human Brain Mapping, 35, 5717– 5735. 10.1002/hbm.22579 25044828 PMC6869664 · DOI
  5. Altarelli, I., Monzalvo, K., Iannuzzi, S., Fluss, J., Billard, C., Ramus, F., & Dehaene‐Lambertz, G. (2013). A functionally guided approach to the morphometry of occipitotemporal regions in developmental dyslexia: Evidence for differential effects in boys and girls. Journal of Neuroscience, 33, 11296– 11301. 10.1523/JNEUROSCI.5854-12.2013 23825432 PMC6618608 · DOI
  6. Alvarez, V. A., Ridenour, D. A., & Sabatini, B. L. (2006). Retraction of synapses and dendritic spines induced by off‐target effects of RNA interference. Journal of Neuroscience, 26, 7820– 7825. 10.1523/JNEUROSCI.1957-06.2006 16870727 PMC6674211 · DOI
  7. Andrews, W., Liapi, A., Plachez, C., Camurri, L., Zhang, J., Mori, S., … Richards, L. J. (2006). Robo1 regulates the development of major axon tracts and interneuron migration in the forebrain. Development, 133, 2243– 2252. 10.1242/dev.02379 16690755 · DOI
  8. Baek, S. T., Kerjan, G., Bielas, S. L., Lee, J. E., Fenstermaker, A. G., Novarino, G., & Gleeson, J. G. (2014). Off‐target effect of doublecortin family shRNA on neuronal migration associated with endogenous microRNA dysregulation. Neuron, 82, 1255– 1262. 10.1016/j.neuron.2014.04.036 24945770 PMC4086250 · DOI
  9. Bai, J., Ramos, R. L., Ackman, J. B., Thomas, A. M., Lee, R. V., & LoTurco, J. J. (2003). RNAi reveals doublecortin is required for radial migration in rat neocortex. Nature Neuroscience, 6, 1277– 1283. 10.1038/nn1153 14625554 · DOI
  10. Beaton, A. A. (1997). The relation of planum temporale asymmetry and morphology of the corpus callosum to handedness, gender, and dyslexia: A review of the evidence. Brain and Language, 60, 255– 322. 10.1006/brln.1997.1825 9344480 · DOI
  11. Becker, J., Czamara, D., Scerri, T. S., Ramus, F., Csepe, V., Talcott, J. B., … Schumacher, J. (2014). Genetic analysis of dyslexia candidate genes in the European cross‐linguistic NeuroDys cohort. European Journal of Human Genetics, 22, 675– 680. 10.1038/ejhg.2013.199 24022301 PMC3992562 · DOI
  12. Begley, C. G., & Ioannidis, J. P. (2015). Reproducibility in science: Improving the standard for basic and preclinical research. Circulation Research, 116, 116– 126. 10.1161/CIRCRESAHA.114.303819 25552691 · DOI · Paper page
  13. Bishop, D. V. (2015). The interface between genetics and psychology: Lessons from developmental dyslexia. Proceedings of the Royal Society of London. Series B, Biological Sciences, 282, 20143139 10.1098/rspb.2014.3139 25854887 PMC4426619 · DOI
  14. Bloom, J. S., Garcia‐Barrera, M. A., Miller, C. J., Miller, S. R., & Hynd, G. W. (2013). Planum temporale morphology in children with developmental dyslexia. Neuropsychologia, 51, 1684– 1692. 10.1016/j.neuropsychologia.2013.05.012 23707683 PMC3799899 · DOI
  15. Bloomfield, T. C., Gentner, T. Q., & Margoliash, D. (2011). What birds have to say about language. Nature Neuroscience, 14, 947– 948. 10.1038/nn.2884 21792190 PMC3718307 · DOI
  16. Bourgeron, T. (2015). From the genetic architecture to synaptic plasticity in autism spectrum disorder. Nature Reviews Neuroscience, 16, 551– 563. 10.1038/nrn3992 26289574 · DOI · Paper page
  17. Brandler, W. M., & Paracchini, S. (2014). The genetic relationship between handedness and neurodevelopmental disorders. Trends in Molecular Medicine, 20, 83– 90. 10.1016/j.molmed.2013.10.008 24275328 PMC3969300 · DOI
  18. 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, 723– 733. 10.1016/j.neuroscience.2008.01.020 18313856 PMC2424111 · DOI
  19. Bustin, S. A. (2014). The reproducibility of biomedical research: Sleepers awake!. Biomolecular Detection and Quantification, 2, 35– 42. 10.1016/j.bdq.2015.01.002 27896142 PMC5121206 · DOI
  20. Caffrey, D. R., Zhao, J., Song, Z., Schaffer, M. E., Haney, S. A., Subramanian, R. R., … Hughes, J. D. (2011). siRNA off‐target effects can be reduced at concentrations that match their individual potency. PLoS One, 6, e21503 10.1371/journal.pone.0021503 21750714 PMC3130022 · DOI
  21. Carreiras, M., Armstrong, B. C., Perea, M., & Frost, R. (2014). The what, when, where, and how of visual word recognition. Trends in Cognitive Sciences, 18, 90– 98. 10.1016/j.tics.2013.11.005 24373885 · DOI
  22. Carrion‐Castillo, A., Franke, B., & Fisher, S. E. (2013). Molecular genetics of dyslexia: An overview. Dyslexia, 19, 214– 240. 10.1002/dys.1464 24133036 · DOI
  23. Carrion‐Castillo, A., Maassen, B., Franke, B., Heister, A., Naber, M., van der Leij, A., … Fisher, S. E. (2017). Association analysis of dyslexia candidate genes in a Dutch longitudinal sample. European Journal of Human Genetics, 25, 452– 460. 10.1038/ejhg.2016.194 28074887 PMC5386414 · DOI
  24. Centanni, T. M., Booker, A. B., Chen, F., Sloan, A. M., Carraway, R. S., Rennaker, R. L., … Kilgard, M. P. (2016). Knockdown of dyslexia‐gene Dcdc2 interferes with speech sound discrimination in continuous streams. Journal of Neuroscience, 36, 4895– 4906. 10.1523/JNEUROSCI.4202-15.2016 27122044 PMC4846679 · DOI
  25. Centanni, T. M., Booker, A. B., Sloan, A. M., Chen, F., Maher, B. J., Carraway, R. S., … Kilgard, M. P. (2014). Knockdown of the dyslexia‐associated gene Kiaa0319 impairs temporal responses to speech stimuli in rat primary auditory cortex. Cerebral Cortex, 24, 1753– 1766. 10.1093/cercor/bht028 23395846 PMC4051891 · DOI
  26. Chandrasekar, G., Vesterlund, L., Hultenby, K., Tapia‐Paez, I., & Kere, J. (2013). The zebrafish orthologue of the dyslexia candidate gene DYX1C1 is essential for cilia growth and function. PLoS One, 8, e63123 10.1371/journal.pone.0063123 23650548 PMC3641089 · DOI
  27. Chang, B. S., Katzir, T., Liu, T., Corriveau, K., Barzillai, M., Apse, K. A., … Walsh, C. A. (2007). A structural basis for reading fluency: White matter defects in a genetic brain malformation. Neurology, 69, 2146– 2154. 10.1212/01.wnl.0000286365.41070.54 18056578 · DOI
  28. Chang, B. S., Ly, J., Appignani, B., Bodell, A., Apse, K. A., Ravenscroft, R. S., … Walsh, C. A. (2005). Reading impairment in the neuronal migration disorder of periventricular nodular heterotopia. Neurology, 64, 799– 803. 10.1212/01.WNL.0000152874.57180.AF 15753412 · DOI
  29. 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, 387– 396. 10.1016/j.biopsych.2013.08.018 24094509 PMC4025976 · DOI
  30. Che, A., Truong, D. T., Fitch, R. H., & LoTurco, J. J. (2016). Mutation of the dyslexia‐associated gene Dcdc2 enhances glutamatergic synaptic transmission between layer 4 neurons in mouse neocortex. Cerebral Cortex, 26, 3705– 3718. 10.1093/cercor/bhv168 26250775 PMC5004750 · DOI
  31. Cohen, M., Campbell, R., & Yaghmai, F. (1989). Neuropathological abnormalities in developmental dysphasia. Annals of Neurology, 25, 567– 570. 10.1002/ana.410250607 2472772 · DOI
  32. Corbo, J. C., Deuel, T. A., Long, J. M., LaPorte, P., Tsai, E., Wynshaw‐Boris, A., & Walsh, C. A. (2002). Doublecortin is required in mice for lamination of the hippocampus but not the neocortex. Journal of Neuroscience, 22, 7548– 7557. 10.1523/JNEUROSCI.22-17-07548.2002 12196578 PMC6757990 · DOI
  33. Couto, J. M., Gomez, L., Wigg, K., Cate‐Carter, T., Archibald, J., Anderson, B., … Barr, C. L. (2008). The KIAA0319‐like (KIAA0319L) gene on chromosome 1p34 as a candidate for reading disabilities. Journal of Neurogenetics, 22, 295– 313. 10.1080/01677060802354328 19085271 PMC5381963 · DOI
  34. 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. 10.1016/j.neuroscience.2010.11.002 21070838 PMC3010415 · DOI
  35. Davidson, B. L., & Boudreau, R. L. (2007). RNA interference: A tool for querying nervous system function and an emerging therapy. Neuron, 53, 781– 788. 10.1016/j.neuron.2007.02.020 17359914 · DOI
  36. Davies, G., Lam, M., Harris, S. E., Trampush, J., Luciano, M., Hill, W. D., … Deary, I. J. (2017). Ninety‐nine independent genetic loci influencing general cognitive function include genes associated with brain health and structure (N = 280,360). bioRxiv, 176511.
  37. Davis, O. S., Band, G., Pirinen, M., Haworth, C. M., Meaburn, E. L., Kovas, Y., … Spencer, C. C. (2014). The correlation between reading and mathematics ability at age twelve has a substantial genetic component. Nature Communications, 5, 4204 10.1038/ncomms5204 PMC4102107 25003214 · DOI
  38. de Nijs, L., Leon, C., Nguyen, L., Loturco, J. J., Delgado‐Escueta, A. V., Grisar, T., & Lakaye, B. (2009). EFHC1 interacts with microtubules to regulate cell division and cortical development. Nature Neuroscience, 12, 1266– 1274. 10.1038/nn.2390 19734894 · DOI
  39. Dehaene, S. (2009). Reading in the brain: The new science of how we read. New York, NY: Penguin Publishing Group.
  40. Dehaene, S., & Cohen, L. (2011). The unique role of the visual word form area in reading. Trends in Cognitive Sciences, 15, 254– 262. 10.1016/j.tics.2011.04.003 21592844 · DOI
  41. Deuel, T. A., Liu, J. S., Corbo, J. C., Yoo, S. Y., Rorke‐Adams, L. B., & Walsh, C. A. (2006). Genetic interactions between doublecortin and doublecortin‐like kinase in neuronal migration and axon outgrowth. Neuron, 49, 41– 53. 10.1016/j.neuron.2005.10.038 16387638 · DOI
  42. Diaz, B., Hintz, F., Kiebel, S. J., & von Kriegstein, K. (2012). Dysfunction of the auditory thalamus in developmental dyslexia. Proceedings of the National Academy of Sciences of the United States of America, 109, 13841– 13846. 10.1073/pnas.1119828109 22869724 PMC3427071 · DOI
  43. Drake, W. E. (1968). Clinical and pathological findings in a child with a developmental learning disability. Journal of Learning Disabilities, 1, 486– 502. 10.1177/002221946800100901 · DOI
  44. Dubeau, F., Tampieri, D., Lee, N., Andermann, E., Carpenter, S., Leblanc, R., … Andermann, F. (1995). Periventricular and subcortical nodular heterotopia. A study of 33 patients. Brain, 118, 1273– 1287. 10.1093/brain/118.5.1273 7496786 · DOI
  45. Eckert, M. (2004). Neuroanatomical markers for dyslexia: A review of dyslexia structural imaging studies. Neuroscientist, 10, 362– 371. 10.1177/1073858404263596 15271263 · DOI
  46. Edelman, G. M., & Gally, J. A. (2001). Degeneracy and complexity in biological systems. Proceedings of the National Academy of Sciences of the United States of America, 98, 13763– 13768. 10.1073/pnas.231499798 11698650 PMC61115 · DOI · Paper page
  47. Eicher, J. D., Powers, N. R., Miller, L. L., Akshoomoff, N., Amaral, D. G., Bloss, C. S., … Gruen, J. R. (2013). Genome‐wide association study of shared components of reading disability and language impairment. Genes, Brain, and Behavior, 12, 792– 801. 10.1111/gbb.12085 PMC3904347 24024963 · DOI
  48. Eicher, J. D., Stein, C. M., Deng, F., Ciesla, A. A., Powers, N. R., Boada, R., … Gruen, J. R. (2015). The DYX2 locus and neurochemical signaling genes contribute to speech sound disorder and related neurocognitive domains. Genes, Brain, and Behavior, 14, 377– 385. 10.1111/gbb.12214 PMC4492462 25778907 · DOI
  49. Einarsdottir, E., Peyrard‐Janvid, M., Darki, F., Tuulari, J. J., Merisaari, H., Karlsson, L., … Kere, J. (2017). Identification of NCAN as a candidate gene for developmental dyslexia. Scientific Reports, 7, 9294 10.1038/s41598-017-10175-7 28839234 PMC5570950 · DOI
  50. Einarsdottir, E., Svensson, I., Darki, F., Peyrard‐Janvid, M., Lindvall, J. M., Ameur, A., … Matsson, H. (2015). Mutation in CEP63 co‐segregating with developmental dyslexia in a Swedish family. Human Genetics, 134, 1239– 1248. 10.1007/s00439-015-1602-1 26400686 PMC4628622 · DOI
  51. Felker, M. V., Walker, L. M., Sokol, D. K., Edwards‐Brown, M., & Chang, B. S. (2011). Early cognitive and behavioral problems in children with nodular heterotopia. Epilepsy & Behavior, 22, 523– 526. 10.1016/j.yebeh.2011.08.010 21908237 PMC3206142 · DOI
  52. Field, L. L., Shumansky, K., Ryan, J., Truong, D., Swiergala, E., & Kaplan, B. J. (2013). Dense‐map genome scan for dyslexia supports loci at 4q13, 16p12, 17q22; Suggests novel locus at 7q36. Genes, Brain, and Behavior, 12, 56– 69. 10.1111/gbb.12003 23190410 · DOI
  53. Fisher, S. E., & Francks, C. (2006). Genes, cognition and dyslexia: Learning to read the genome. Trends in Cognitive Sciences, 10, 250– 257. 10.1016/j.tics.2006.04.003 16675285 · DOI
  54. Fisher, S. E., & Scharff, C. (2009). FOXP2 as a molecular window into speech and language. Trends in Genetics, 25, 166– 177. 10.1016/j.tig.2009.03.002 19304338 · DOI
  55. Fitch, W. T. (2017). Empirical approaches to the study of language evolution. Psychonomic Bulletin & Review, 24, 3– 33. 10.3758/s13423-017-1236-5 28150125 · DOI
  56. Franquinho, F., Nogueira‐Rodrigues, J., Duarte, J. M., Esteves, S. S., Carter‐Su, C., Monaco, A. P., … Sousa, M. M. (2017). The dyslexia‐susceptibility protein KIAA0319 inhibits axon growth through Smad2 signaling. Cerebral Cortex, 27, 1732– 1747. 10.1093/cercor/bhx023 28334068 PMC5905272 · DOI
  57. Friederici, A. D., & Gierhan, S. M. (2013). The language network. Current Opinion in Neurobiology, 23, 250– 254. 10.1016/j.conb.2012.10.002 23146876 · DOI
  58. Gabel, L. A., Gibson, C. J., Gruen, J. R., & LoTurco, J. J. (2010). Progress towards a cellular neurobiology of reading disability. Neurobiology of Diseases, 38, 173– 180. 10.1016/j.nbd.2009.06.019 PMC2854314 19616627 · DOI
  59. Gabel, L. A., Marin, I., LoTurco, J. 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, 868– 875. 10.1111/j.1601-183X.2011.00727.x PMC3212622 21883923 · DOI
  60. Galaburda, A. M. (1985). Developmental dyslexia: A review of biological interactions. Ann Dyslexia, 35, 19– 33. 10.1007/BF02659178 24243407 · DOI
  61. Galaburda, A. M. (1989). Ordinary and extraordinary brain development: Anatomical variation in developmental dyslexia. Annals of Dyslexia, 39, 65– 80. 10.1007/BF02656901 24233472 · DOI
  62. Galaburda, A. M. (1992). Dyslexia. The New England Journal of Medicine, 327, 279; author reply 280‐281. 10.1056/nejm199207233270413 1614472 · DOI
  63. Galaburda, A. M. (1993). Neurology of developmental dyslexia. Current Opinion in Neurobiology, 3, 237– 242. 10.1016/0959-4388(93)90216-L 8513237 · DOI
  64. Galaburda, A. M., & Kemper, T. L. (1979). Cytoarchitectonic abnormalities in developmental dyslexia: A case study. Annals of Neurology, 6, 94– 100. 10.1002/ana.410060203 496415 · DOI
  65. Galaburda, A. M., LoTurco, J., Ramus, F., Fitch, R. H., & Rosen, G. D. (2006). From genes to behavior in developmental dyslexia. Nature Neuroscience, 9, 1213– 1217. 10.1038/nn1772 17001339 · DOI
  66. 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, 222– 233. 10.1002/ana.410180210 4037763 · DOI
  67. Gialluisi, A., Newbury, D. F., Wilcutt, E. G., Olson, R. K., DeFries, J. C., Brandler, W. M., … Fisher, S. E. (2014). Genome‐wide screening for DNA variants associated with reading and language traits. Genes, Brain, and Behavior, 13, 686– 701. 10.1111/gbb.12158 PMC4165772 25065397 · DOI
  68. Gilger, J. W. (1992). Using self‐report and parental‐ report survey data to assess past and present academic achievement of adults and children. Journal of Applied Developmental Psychology, 13, 235– 256. 10.1016/0193-3973(92)90031-C · DOI
  69. Giraud, A. L., & Ramus, F. (2013). Neurogenetics and auditory processing in developmental dyslexia. Current Opinion in Neurobiology, 23, 37– 42. 10.1016/j.conb.2012.09.003 23040541 · DOI
  70. Gleeson, J. G., Allen, K. M., Fox, J. W., Lamperti, E. D., Berkovic, S., Scheffer, I., … Walsh, C. A. (1998). Doublecortin, a brain‐specific gene mutated in human X‐linked lissencephaly and double cortex syndrome, encodes a putative signaling protein. Cell, 92, 63– 72. 10.1016/S0092-8674(00)80899-5 9489700 · DOI
  71. Gonda, Y., Andrews, W. D., Tabata, H., Namba, T., Parnavelas, J. G., Nakajima, K., … Uchino, S. (2013). Robo1 regulates the migration and laminar distribution of upper‐layer pyramidal neurons of the cerebral cortex. Cerebral Cortex, 267617 10.1093/cercor/bhs141 PMC3643720 22661412 · DOI
  72. Gostic, M., Martinelli, A., Tucker, C., Yang, Z., Gasparoli, F., Dholakia, K., … Paracchini, S. (2018). The dyslexia susceptibility KIAA0319 gene shows a highly specific expression pattern during zebrafish development supporting a role beyond neuronal migration. bioRxiv, 267617. 10.1101/267617 PMC6767054 30950042 · DOI
  73. Goswami, U. (2015). Sensory theories of developmental dyslexia: Three challenges for research. Nature Reviews Neuroscience, 16, 43– 54. 10.1038/nrn3836 25370786 · DOI
  74. Graham, S. A., & Fisher, S. E. (2015). Understanding language from a genomic perspective. Annual Review of Genetics, 49, 131– 160. 10.1146/annurev-genet-120213-092236 26442845 · DOI
  75. Grati, M., Chakchouk, I., Ma, Q., Bensaid, M., Desmidt, A., Turki, N., … Masmoudi, S. (2015). A missense mutation in DCDC2 causes human recessive deafness DFNB66, likely by interfering with sensory hair cell and supporting cell cilia length regulation. Human Molecular Genetics, 24, 2482– 2491. 10.1093/hmg/ddv009 25601850 PMC4383862 · DOI
  76. Grimm, D., Streetz, K. L., Jopling, C. L., Storm, T. A., Pandey, K., Davis, C. R., … Kay, M. A. (2006). Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature, 441, 537– 541. 10.1038/nature04791 16724069 · DOI · Paper page
  77. Guadalupe, T., Zwiers, M. P., Wittfeld, K., Teumer, A., Vasquez, A. A., Hoogman, M., … Francks, C. (2015). Asymmetry within and around the human planum temporale is sexually dimorphic and influenced by genes involved in steroid hormone receptor activity. Cortex, 62, 41– 55. 10.1016/j.cortex.2014.07.015 25239853 · DOI
  78. Guerreiro, M. M., Hage, S. R., Guimaraes, C. A., Abramides, D. V., Fernandes, W., Pacheco, P. S., … Cendes, F. (2002). Developmental language disorder associated with polymicrogyria. Neurology, 59, 245– 250. 10.1212/WNL.59.2.245 12136065 · DOI
  79. Guerrero‐Cazares, H., Lavell, E., Chen, L., Schiapparelli, P., Lara‐Velazquez, M., Capilla‐Gonzalez, V., … Quinones‐Hinojosa, A. (2017). Brief report: Robo1 regulates the migration of human subventricular zone neural progenitor cells during development. Stem Cells, 35, 1860– 1865. 10.1002/stem.2628 28406573 PMC5484745 · DOI
  80. Guidi, L. G., Mattley, J., Martinez‐Garay, I., Monaco, A. P., Linden, J. F., Velayos‐Baeza, A., & Molnar, Z. (2017). Knockout mice for dyslexia susceptibility gene homologs KIAA0319 and KIAA0319L have unaffected neuronal migration but display abnormal auditory processing. Cerebral Cortex, 27, 5831– 5845. 10.1093/cercor/bhx269 29045729 PMC5939205 · DOI
  81. Habib, M. (2000). The neurological basis of developmental dyslexia: An overview and working hypothesis. Brain, 123, 2373– 2399. 10.1093/brain/123.12.2373 11099442 · DOI
  82. Hage, S. R., Joaquim, R. S., Carvalho, K. G., Padovani, C. R., & Guerreiro, M. M. (2004). [Diagnosis of children with specific language impairment using a developmental scale]. Arquivos de Neuro‐Psiquiatria, 62, 649– 653. https://doi.org//s0004-282x2004000400015 15334224
  83. Hage, S. R., & Nieder, A. (2016). Dual neural network model for the evolution of speech and language. Trends in Neurosciences, 39, 813– 829. 10.1016/j.tins.2016.10.006 27884462 · DOI
  84. Hagoort, P. (2014). Nodes and networks in the neural architecture for language: Broca's region and beyond. Current Opinion in Neurobiology, 28, 136– 141. 10.1016/j.conb.2014.07.013 25062474 · DOI
  85. Hannula‐Jouppi, K., Kaminen‐Ahola, N., Taipale, M., Eklund, R., Nopola‐Hemmi, J., Kaariainen, H., & Kere, J. (2005). The axon guidance receptor gene ROBO1 is a candidate gene for developmental dyslexia. PLoS Genetics, 1, e50 10.1371/journal.pgen.0010050 16254601 PMC1270007 · DOI
  86. Hong, S. J., Kim, H., Schrader, D., Bernasconi, N., Bernhardt, B. C., & Bernasconi, A. (2014). Automated detection of cortical dysplasia type II in MRI‐negative epilepsy. Neurology, 83, 48– 55. 10.1212/WNL.0000000000000543 24898923 PMC4114179 · DOI
  87. Hornickel, J., & Kraus, N. (2013). Unstable representation of sound: A biological marker of dyslexia. Journal of Neuroscience, 33, 3500– 3504. 10.1523/JNEUROSCI.4205-12.2013 23426677 PMC3599785 · DOI
  88. Housden, B. E., Muhar, M., Gemberling, M., Gersbach, C. A., Stainier, D. Y., Seydoux, G., … Perrimon, N. (2017). Loss‐of‐function genetic tools for animal models: Cross‐species and cross‐platform differences. Nature Reviews Genetics, 18, 24– 40. 10.1038/nrg.2016.118 PMC5206767 27795562 · DOI
  89. Humphreys, P., Kaufmann, W. E., & Galaburda, A. M. (1990). Developmental dyslexia in women: Neuropathological findings in three patients. Annals of Neurology, 28, 727– 738. 10.1002/ana.410280602 2285260 · DOI
  90. Ivliev, A. E., t Hoen, P. A., van Roon‐Mom, W. M., Peters, D. J., & Sergeeva, M. G. (2012). Exploring the transcriptome of ciliated cells using in silico dissection of human tissues. PLoS One, 7, e35618 10.1371/journal.pone.0035618 22558177 PMC3338421 · DOI
  91. Jackson, A. L., & Linsley, P. S. (2010). Recognizing and avoiding siRNA off‐target effects for target identification and therapeutic application. Nature Reviews Drug Discovery, 9, 57– 67. 10.1038/nrd3010 20043028 · DOI
  92. Jednoróg, K., Marchewka, A., Altarelli, I., Monzalvo Lopez, A. K., van Ermingen‐Marbach, M., Grande, M., … Ramus, F. (2015). How reliable are gray matter disruptions in specific reading disability across multiple countries and languages? Insights from a large‐scale voxel‐based morphometry study. Human Brain Mapping, 36, 1741– 1754. 10.1002/hbm.22734 25598483 PMC6869714 · DOI
  93. Johnson, E. C., Border, R., Melroy‐Greif, W. E., de Leeuw, C. A., Ehringer, M. A., & Keller, M. C. (2017). No evidence that schizophrenia candidate genes are more associated with schizophrenia than noncandidate genes. Biological Psychiatry, 82, 702– 708. 10.1016/j.biopsych.2017.06.033 28823710 PMC5643230 · DOI
  94. Kaufmann, W. E., & Galaburda, A. M. (1989). Cerebrocortical microdysgenesis in neurologically normal subjects: A histopathologic study. Neurology, 39, 238– 244. 10.1212/WNL.39.2.238 2915796 · DOI
  95. Kere, J. (2014). The molecular genetics and neurobiology of developmental dyslexia as model of a complex phenotype. Biochemical and Biophysical Research Communications, 452, 236– 243. 10.1016/j.bbrc.2014.07.102 25078623 · DOI
  96. Kidd, S., Lieber, T., & Young, M. W. (1998). Ligand‐induced cleavage and regulation of nuclear entry of Notch in Drosophila melanogaster embryos. Genes & Development, 12, 3728– 3740. 10.1101/gad.12.23.3728 9851979 PMC317253 · DOI
  97. Kiggins, J. T., Comins, J. A., & Gentner, T. Q. (2012). Targets for a comparative neurobiology of language. Frontiers in Evolutionary Neuroscience, 4, 6 10.3389/fnevo.2012.00006 22509163 PMC3321487 · DOI
  98. Kitano, H. (2004). Biological robustness. Nature Reviews Genetics, 5, 826– 837. 10.1038/nrg1471 15520792 · DOI · Paper page
  99. Koizumi, H., Tanaka, T., & Gleeson, J. G. (2006). Doublecortin‐like kinase functions with doublecortin to mediate fiber tract decussation and neuronal migration. Neuron, 49, 55– 66. 10.1016/j.neuron.2005.10.040 16387639 · DOI
  100. Kok, F. O., Shin, M., Ni, C. W., Gupta, A., Grosse, A. S., van Impel, A., … Lawson, N. D. (2015). Reverse genetic screening reveals poor correlation between morpholino‐induced and mutant phenotypes in zebrafish. Developmental Cell, 32, 97– 108. 10.1016/j.devcel.2014.11.018 25533206 PMC4487878 · DOI
  101. Kvajo, M., McKellar, H., & Gogos, J. A. (2012). Avoiding mouse traps in schizophrenia genetics: Lessons and promises from current and emerging mouse models. Neuroscience, 211, 136– 164. 10.1016/j.neuroscience.2011.07.051 21821099 PMC3351555 · DOI
  102. Lazic, S. E. (2016). Experimental design for laboratory biologists: Maximising information and improving reproducibility. Cambridge: Cambridge University Press 10.1017/9781139696647 · DOI
  103. Lee, M. C., Kim, G. M., Woo, Y. J., Kim, M. K., Kim, J. H., Nam, S. C., … Kim, S. U. (2001). Pathogenic significance of neuronal migration disorders in temporal lobe epilepsy. Human Pathology, 32, 643– 648. 10.1053/hupa.2001.24997 11431720 · DOI
  104. Lefly, D. L., & Pennington, B. F. (1991). Spelling errors and reading fluency in compensated adult dyslexics. Annals of Dyslexia, 41, 141– 162. 10.1007/BF02648083 24233762 · DOI · Paper page
  105. Leventer, R. J., Jansen, A., Pilz, D. T., Stoodley, N., Marini, C., Dubeau, F., … Dobyns, W. B. (2010). Clinical and imaging heterogeneity of polymicrogyria: A study of 328 patients. Brain, 133, 1415– 1427. 10.1093/brain/awq078 20403963 PMC2859156 · DOI
  106. Levine, D. N., Hier, D. B., & Calvanio, R. (1981). Acquired learning disability for reading after left temporal lobe damage in childhood. Neurology, 31, 257– 264. 10.1212/WNL.31.3.257 7193819 · DOI
  107. Liao, B. Y., & Zhang, J. (2008). Null mutations in human and mouse orthologs frequently result in different phenotypes. Proceedings of the National Academy of Sciences of the United States of America, 105, 6987– 6992. 10.1073/pnas.0800387105 18458337 PMC2383943 · DOI · Paper page
  108. Livingstone, M. S., Rosen, G. D., Drislane, F. W., & Galaburda, A. M. (1991). Physiological and anatomical evidence for a magnocellular defect in developmental dyslexia. Proceedings of the National Academy of Sciences of the United States of America, 88, 7943– 7947. 10.1073/pnas.88.18.7943 1896444 PMC52421 · DOI
  109. Logothetis, N. K., & Sheinberg, D. L. (1996). Visual object recognition. Annual Review of Neuroscience, 19, 577– 621. 10.1146/annurev.ne.19.030196.003045 8833455 · DOI
  110. Lopez‐Bendito, G., Flames, N., Ma, L., Fouquet, C., Di Meglio, T., Chedotal, A., … Marin, O. (2007). Robo1 and Robo2 cooperate to control the guidance of major axonal tracts in the mammalian forebrain. Journal of Neuroscience, 27, 3395– 3407. 10.1523/JNEUROSCI.4605-06.2007 17392456 PMC6672128 · DOI
  111. LoTurco, J., Manent, J. B., & Sidiqi, F. (2009). New and improved tools for in utero electroporation studies of developing cerebral cortex. Cerebral Cortex, 19, i120– i125. 10.1093/cercor/bhp033 19395528 PMC3859267 · DOI
  112. Luciano, M., Evans, D. M., Hansell, N. K., Medland, S. E., Montgomery, G. W., Martin, N. G., … Bates, T. C. (2013). A genome‐wide association study for reading and language abilities in two population cohorts. Genes, Brain, and Behavior, 12, 645– 652. 10.1111/gbb.12053 PMC3908370 23738518 · DOI
  113. Maisog, J. M., Einbinder, E. R., Flowers, D. L., Turkeltaub, P. E., & Eden, G. F. (2008). A meta‐analysis of functional neuroimaging studies of dyslexia. Annals of the New York Academy of Sciences, 1145, 237– 259. 10.1196/annals.1416.024 19076401 · DOI · Paper page
  114. Martinez‐Garay, I., Guidi, L. G., Holloway, Z. G., Bailey, M. A., Lyngholm, D., Schneider, T., … Velayos‐Baeza, A. (2017). Normal radial migration and lamination are maintained in dyslexia‐susceptibility candidate gene homolog Kiaa0319 knockout mice. Brain Structure and Function, 222, 1367– 1384. 10.1007/s00429-016-1282-1 27510895 PMC5368214 · DOI
  115. Massinen, S., Hokkanen, M. E., Matsson, H., Tammimies, K., Tapia‐Paez, I., Dahlstrom‐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, e20580 10.1371/journal.pone.0020580 21698230 PMC3116825 · DOI
  116. McBride, J. L., Boudreau, R. L., Harper, S. Q., Staber, P. D., Monteys, A. M., Martins, I., … Davidson, B. L. (2008). Artificial miRNAs mitigate shRNA‐mediated toxicity in the brain: Implications for the therapeutic development of RNAi. Proceedings of the National Academy of Sciences of the United States of America, 105, 5868– 5873. 10.1073/pnas.0801775105 18398004 PMC2311380 · DOI
  117. McKavanagh, R., Buckley, E., & Chance, S. A. (2015). Wider minicolumns in autism: A neural basis for altered processing? Brain, 138, 2034– 2045. 10.1093/brain/awv110 25935724 · DOI
  118. Meng, H., Smith, S. D., Hager, K., Held, M., Liu, J., Olson, R. K., … Gruen, J. R. (2005). DCDC2 is associated with reading disability and modulates neuronal development in the brain. Proceedings of the National Academy of Sciences of the United States of America, 102, 17053– 17058. 10.1073/pnas.0508591102 16278297 PMC1278934 · DOI
  119. Mitchell, K. J. (2012). What is complex about complex disorders? Genome Biology, 13, 237 10.1186/gb-2012-13-1-237 22269335 PMC3334577 · DOI
  120. Mitchell, K. J. (2018). Neurogenomics—Towards a more rigorous science. European Journal of Neuroscience, 47, 109– 114. 10.1111/ejn.13801 29230896 · DOI
  121. Monzalvo, K., Fluss, J., Billard, C., Dehaene, S., & Dehaene‐Lambertz, G. (2012). Cortical networks for vision and language in dyslexic and normal children of variable socio‐economic status. NeuroImage, 61, 258– 274. 10.1016/j.neuroimage.2012.02.035 22387166 · DOI
  122. Morel, F., & Wildi, E. (1952). [Disseminated nodular dysgenesis of the frontal cortex]. Revue Neurologique, 87, 251– 270. 13014794
  123. Morgan, A. (2013). Speech‐language pathology insights into genetics and neuroscience: Beyond surface behaviour. International Journal of Speech‐Language Pathology, 15, 245– 254. 10.3109/17549507.2013.777786 23586582 · DOI
  124. Munafò, M. R., Nosek, B. A., Bishop, D. V. M., Button, K. S., Chambers, C. D., Percie du Sert, N., … Ioannidis, J. P. A. (2017). A manifesto for reproducible science. Nature Human Behaviour, 1, 0021 10.1038/s41562-016-0021 PMC7610724 33954258 · DOI · Paper page
  125. Newbury, D. F., Monaco, A. P., & Paracchini, S. (2014). Reading and language disorders: The importance of both quantity and quality. Genes (Basel), 5, 285– 309. 10.3390/genes5020285 24705331 PMC4094934 · DOI
  126. Newbury, D. F., Paracchini, S., Scerri, T. S., Winchester, L., Addis, L., Richardson, A. J., … Monaco, A. P. (2011). Investigation of dyslexia and SLI risk variants in reading‐ and language‐impaired subjects. Behavior Genetics, 41, 90– 104. 10.1007/s10519-010-9424-3 21165691 PMC3029677 · DOI
  127. Norton, E. S., Beach, S. D., & Gabrieli, J. D. (2015). Neurobiology of dyslexia. Current Opinion in Neurobiology, 30, 73– 78. 10.1016/j.conb.2014.09.007 25290881 PMC4293303 · DOI
  128. Ohno, S. (1970). Evolution by gene duplication. New York, NY: Springer‐Verlag 10.1007/978-3-642-86659-3 · DOI · Paper page
  129. Oliveira, E. P., Hage, S. R., Guimaraes, C. A., Brandao‐Almeida, I., Lopes‐Cendes, I., Guerreiro, C. A., … Guerreiro, M. M. (2008). Characterization of language and reading skills in familial polymicrogyria. Brain & Development, 30, 254– 260. 10.1016/j.braindev.2007.08.010 17920799 · DOI
  130. Pagnamenta, A. T., Bacchelli, E., de Jonge, M. V., Mirza, G., Scerri, T. S., Minopoli, F., … Monaco, A. P. (2010). Characterization of a family with rare deletions in CNTNAP5 and DOCK4 suggests novel risk loci for autism and dyslexia. Biological Psychiatry, 68, 320– 328. 10.1016/j.biopsych.2010.02.002 20346443 PMC2941017 · DOI · Paper page
  131. Paracchini, S. (2011). Dissection of genetic associations with language‐related traits in population‐based cohorts. Journal of Neurodevelopmental Disorders, 3, 365– 373. 10.1007/s11689-011-9091-6 21894572 PMC3230763 · DOI
  132. Paracchini, S., Diaz, R., & Stein, J. (2016). Advances in dyslexia genetics—New insights into the role of brain asymmetries. Advances in Genetics, 96, 53– 97. 10.1016/bs.adgen.2016.08.003 27968731 · DOI
  133. Paracchini, S., Scerri, T., & Monaco, A. P. (2007). The genetic lexicon of dyslexia. Annual Review of Genomics and Human Genetics, 8, 57– 79. 10.1146/annurev.genom.8.080706.092312 17444811 · DOI
  134. Paracchini, S., Thomas, A., Castro, S., Lai, C., Paramasivam, M., Wang, Y., … Monaco, A. P. (2006). The chromosome 6p22 haplotype associated with dyslexia reduces the expression of KIAA0319, a novel gene involved in neuronal migration. Human Molecular Genetics, 15, 1659– 1666. 10.1093/hmg/ddl089 16600991 · DOI
  135. Pardoe, H., & Kuzniecky, R. (2014). Advanced imaging techniques in the diagnosis of nonlesional epilepsy: MRI, MRS, PET, and SPECT. Epilepsy Currents, 14, 121– 124. 10.5698/1535-7597-14.3.121 24940151 PMC4038272 · DOI
  136. Park, J. H., Wacholder, S., Gail, M. H., Peters, U., Jacobs, K. B., Chanock, S. J., & Chatterjee, N. (2010). Estimation of effect size distribution from genome‐wide association studies and implications for future discoveries. Nature Genetics, 42, 570– 575. 10.1038/ng.610 20562874 PMC4615599 · DOI · Paper page
  137. Peschansky, V. J., Burbridge, T. J., Volz, A. J., Fiondella, C., Wissner‐Gross, Z., Galaburda, A. M., … Rosen, G. D. (2010). The effect of variation in expression of the candidate dyslexia susceptibility gene homolog Kiaa0319 on neuronal migration and dendritic morphology in the rat. Cerebral Cortex, 20, 884– 897. 10.1093/cercor/bhp154 19679544 PMC2837091 · DOI
  138. Peterson, R. L., & Pennington, B. F. (2015). Developmental dyslexia. Annual Review of Clinical Psychology, 11, 283– 307. 10.1146/annurev-clinpsy-032814-112842 25594880 · DOI
  139. Platt, M. P., Adler, W. T., Mehlhorn, A. J., Johnson, G. C., Wright, K. A., Choi, R. T., … Rosen, G. D. (2013). Embryonic disruption of the candidate dyslexia susceptibility gene homolog Kiaa0319‐like results in neuronal migration disorders. Neuroscience, 248, 585– 593. 10.1016/j.neuroscience.2013.06.056 23831424 PMC3843998 · DOI
  140. Poelmans, G., Buitelaar, J. K., Pauls, D. L., & Franke, B. (2011). A theoretical molecular network for dyslexia: Integrating available genetic findings. Molecular Psychiatry, 16, 365– 382. 10.1038/mp.2010.105 20956978 · DOI · Paper page
  141. Poelmans, G., Engelen, J. J., Van Lent‐Albrechts, J., Smeets, H. J., Schoenmakers, E., Franke, B., … Schrander‐Stumpel, C. (2009). Identification of novel dyslexia candidate genes through the analysis of a chromosomal deletion. American Journal of Medical Genetics. Part B, Neuropsychiatric Genetics: The Official Publication of the International Society of Psychiatric Genetics, 150B, 140– 147. 10.1002/ajmg.b.30787 18521840 · DOI
  142. Popper, K. R. (1934). The logic of scientific discovery. London, UK: Routledge.
  143. Pramparo, T., Youn, Y. H., Yingling, J., Hirotsune, S., & Wynshaw‐Boris, A. (2010). Novel embryonic neuronal migration and proliferation defects in Dcx mutant mice are exacerbated by Lis1 reduction. Journal of Neuroscience, 30, 3002– 3012. 10.1523/JNEUROSCI.4851-09.2010 20181597 PMC2861429 · DOI
  144. Prather, J. F., Okanoya, K., & Bolhuis, J. J. (2017). Brains for birds and babies: Neural parallels between birdsong and speech acquisition. Neuroscience and Biobehavioral Reviews, 81, 225– 237. 10.1016/j.neubiorev.2016.12.035 28087242 · DOI
  145. Price, C. J. (2012). A review and synthesis of the first 20 years of PET and fMRI studies of heard speech, spoken language and reading. NeuroImage, 62, 816– 847. 10.1016/j.neuroimage.2012.04.062 22584224 PMC3398395 · DOI · Paper page
  146. Rakic, P. (1988). Defects of neuronal migration and the pathogenesis of cortical malformations. Progress in Brain Research, 73, 15– 37. 10.1016/S0079-6123(08)60494-X 3047794 · DOI
  147. Ramocki, M. B., & Zoghbi, H. Y. (2008). Failure of neuronal homeostasis results in common neuropsychiatric phenotypes. Nature, 455, 912– 918. 10.1038/nature07457 18923513 PMC2696622 · DOI · Paper page
  148. Ramos, R. L., Bai, J., & LoTurco, J. J. (2006). Heterotopia formation in rat but not mouse neocortex after RNA interference knockdown of DCX. Cerebral Cortex, 16, 1323– 1331. 10.1093/cercor/bhj074 16292002 · DOI
  149. Ramus, F., & Ahissar, M. (2012). Developmental dyslexia: The difficulties of interpreting poor performance, and the importance of normal performance. Cognitive Neuropsychology, 29, 104– 122. 10.1080/02643294.2012.677420 22559749 · DOI
  150. Rana, T. M. (2007). Illuminating the silence: Understanding the structure and function of small RNAs. Nature Reviews Molecular Cell Biology, 8, 23– 36. 10.1038/nrm2085 17183358 · DOI · Paper page
  151. Raskind, W. H., Peter, B., Richards, T., Eckert, M. M., & Berninger, V. W. (2013). The genetics of reading disabilities: From phenotypes to candidate genes. Frontiers in Psychology, 3, 601 10.3389/fpsyg.2012.00601 23308072 PMC3538356 · DOI · Paper page
  152. Reiner, O. (2013). LIS1 and DCX: Implications for brain development and human disease in relation to microtubules. Scientifica (Cairo), 2013, 393975 10.1155/2013/393975 24278775 PMC3820303 · DOI
  153. Reiner, O., Gorelik, A., & Greenman, R. (2012). Use of RNA interference by in utero electroporation to study cortical development: The example of the doublecortin superfamily. Genes (Basel), 3, 759– 778. 10.3390/genes3040759 24705084 PMC3899981 · DOI
  154. Reinstein, E., Chang, B. S., Robertson, S. P., Rimoin, D. L., & Katzir, T. (2012). Filamin A mutation associated with normal reading skills and dyslexia in a family with periventricular heterotopia. American Journal of Medical Genetics. Part A, 158A, 1897– 1901. 10.1002/ajmg.a.35455 22740120 · DOI
  155. Rendall, A. R., Tarkar, A., Contreras‐Mora, H. M., LoTurco, J. J., & Fitch, R. H. (2017). Deficits in learning and memory in mice with a mutation of the candidate dyslexia susceptibility gene Dyx1c1. Brain and Language, 172, 30– 38. 10.1016/j.bandl.2015.04.008 25989970 PMC4646737 · DOI
  156. Richardson, A. J., & Ross, M. A. (2000). Fatty acid metabolism in neurodevelopmental disorder: A new perspective on associations between attention‐deficit/hyperactivity disorder, dyslexia, dyspraxia and the autistic spectrum. Prostaglandins Leukotrienes and Essential Fatty Acids, 63, 1– 9. 10.1054/plef.2000.0184 10970706 · DOI
  157. Richardson, F. M., Seghier, M. L., Leff, A. P., Thomas, M. S., & Price, C. J. (2011). Multiple routes from occipital to temporal cortices during reading. Journal of Neuroscience, 31, 8239– 8247. 10.1523/JNEUROSCI.6519-10.2011 21632945 PMC3785141 · DOI
  158. Richlan, F. (2012). Developmental dyslexia: Dysfunction of a left hemisphere reading network. Frontiers in Human Neuroscience, 6, 120 10.3389/fnhum.2012.00120 22557962 PMC3340948 · DOI
  159. Ritchie, S. J., & Bates, T. C. (2013). Enduring links from childhood mathematics and reading achievement to adult socioeconomic status. Psychological Science, 24, 1301– 1308. 10.1177/0956797612466268 23640065 · DOI · Paper page
  160. Rosen, G. D., Bai, J., Wang, Y., Fiondella, C. G., Threlkeld, S. W., LoTurco, J. J., & Galaburda, A. M. (2007). Disruption of neuronal migration by RNAi of Dyx1c1 results in neocortical and hippocampal malformations. Cerebral Cortex, 17, 2562– 2572. 10.1093/cercor/bhl162 17218481 PMC3742088 · DOI
  161. Rossi, A., Kontarakis, Z., Gerri, C., Nolte, H., Holper, S., Kruger, M., & Stainier, D. Y. (2015). Genetic compensation induced by deleterious mutations but not gene knockdowns. Nature, 524, 230– 233. 10.1038/nature14580 26168398 · DOI
  162. Scerri, T. S., Macpherson, E., Martinelli, A., Wa, W. C., Monaco, A. P., Stein, J., … Paracchini, S. (2017). The DCDC2 deletion is not a risk factor for dyslexia. Translational Psychiatry, 7, e1182 10.1038/tp.2017.151 28742079 PMC5538127 · DOI
  163. Scerri, T. S., & Schulte‐Korne, G. (2010). Genetics of developmental dyslexia. European Child and Adolescent Psychiatry, 19, 179– 197. 10.1007/s00787-009-0081-0 20091194 · DOI
  164. Schueler, M., Braun, D. A., Chandrasekar, G., Gee, H. Y., Klasson, T. D., Halbritter, J., … Hildebrandt, F. (2015). DCDC2 mutations cause a renal‐hepatic ciliopathy by disrupting Wnt signaling. American Journal of Human Genetics, 96, 81– 92. 10.1016/j.ajhg.2014.12.002 25557784 PMC4289677 · DOI
  165. Schulze, K. D., & Braak, H. (1978). [Brain warts]. Zeitschrift für mikroskopisch‐anatomische Forschung, 92, 609– 623. 749392
  166. Schumacher, J., Hoffmann, P., Schmal, C., Schulte‐Korne, G., & Nothen, M. M. (2007). Genetics of dyslexia: The evolving landscape. Journal of Medical Genetics, 44, 289– 297. 10.1136/jmg.2006.046516 17307837 PMC2597981 · DOI
  167. Shaywitz, S. E., & Shaywitz, B. A. (2008). Paying attention to reading: The neurobiology of reading and dyslexia. Development and Psychopathology, 20, 1329– 1349. 10.1017/S0954579408000631 18838044 · DOI
  168. Sherman, G. F., Galaburda, A. M., Behan, P. O., & Rosen, G. D. (1987). Neuroanatomical anomalies in autoimmune mice. Acta Neuropathologica, 74, 239– 242. 10.1007/BF00688187 3673516 · DOI
  169. Sherman, G. F., Galaburda, A. M., & Geschwind, N. (1985). Cortical anomalies in brains of New Zealand mice: A neuropathologic model of dyslexia? Proceedings of the National Academy of Sciences of the United States of America, 82, 8072– 8074. 10.1073/pnas.82.23.8072 3865217 PMC391444 · DOI
  170. Smith, S. D. (2007). Genes, language development, and language disorders. Mental Retardation and Developmental Disabilities Research Reviews, 13, 96– 105. 10.1002/mrdd.20135 17326114 · DOI
  171. Snowling, M. J. (2000). Dyslexia. Oxford: Blackwell Publishers Ltd.
  172. Stein, J. (2001). The magnocellular theory of developmental dyslexia. Dyslexia, 7, 12– 36. 10.1002/dys.186 11305228 · DOI
  173. Szalkowski, C. E., Booker, A. B., Truong, D. T., Threlkeld, S. W., Rosen, G. D., & Fitch, R. H. (2013). Knockdown of the candidate dyslexia susceptibility gene homolog Dyx1c1 in rodents: Effects on auditory processing, visual attention, and cortical and thalamic anatomy. Developmental Neuroscience, 35, 50– 68. 10.1159/000348431 23594585 PMC3980864 · DOI
  174. 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, 293– 302. 10.1016/j.ijdevneu.2012.01.009 22326444 PMC3516384 · DOI
  175. Szalkowski, C. E., Hinman, J. R., Threlkeld, S. W., Wang, Y., LePack, A., Rosen, G. D., … Fitch, R. H. (2011). Persistent spatial working memory deficits in rats following in utero RNAi of Dyx1c1. Genes, Brain, and Behavior, 10, 244– 252. 10.1111/j.1601-183X.2010.00662.x PMC3041839 20977651 · DOI
  176. Takahashi, D. Y., Fenley, A. R., Teramoto, Y., Narayanan, D. Z., Borjon, J. I., Holmes, P., & Ghazanfar, A. A. (2015). LANGUAGE DEVELOPMENT. The developmental dynamics of marmoset monkey vocal production. Science, 349, 734– 738. 10.1126/science.aab1058 26273055 · DOI
  177. Tarkar, A., Loges, N. T., Slagle, C. E., Francis, R., Dougherty, G. W., Tamayo, J. V., … Omran, H. (2013). DYX1C1 is required for axonemal dynein assembly and ciliary motility. Nature Genetics, 45, 995– 1003. 10.1038/ng.2707 23872636 PMC4000444 · DOI
  178. 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, 508– 514. 10.1016/j.brainresbull.2006.11.005 17259020 PMC1893003 · DOI
  179. 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, 802– 811. 10.1111/gbb.12170 PMC4241168 25130614 · DOI
  180. Tsuboi, D., Kuroda, K., Tanaka, M., Namba, T., Iizuka, Y., Taya, S., … Kaibuchi, K. (2015). Disrupted‐in‐schizophrenia 1 regulates transport of ITPR1 mRNA for synaptic plasticity. Nature Neuroscience, 18, 698– 707. 10.1038/nn.3984 25821909 · DOI
  181. Vandermosten, M., Boets, B., Wouters, J., & Ghesquiere, P. (2012). A qualitative and quantitative review of diffusion tensor imaging studies in reading and dyslexia. Neuroscience and Biobehavioral Reviews, 36, 1532– 1552. 10.1016/j.neubiorev.2012.04.002 22516793 · DOI
  182. Veerappa, A. M., Saldanha, M., Padakannaya, P., & Ramachandra, N. B. (2013). Family‐based genome‐wide copy number scan identifies five new genes of dyslexia involved in dendritic spinal plasticity. Journal of Human Genetics, 58, 539– 547. 10.1038/jhg.2013.47 23677055 · DOI
  183. Velayos‐Baeza, A., Levecque, C., Kobayashi, K., Holloway, Z. G., & Monaco, A. P. (2010). The dyslexia‐associated KIAA0319 protein undergoes proteolytic processing with γ‐secretase‐independent intramembrane cleavage. Journal of Biological Chemistry, 285, 40148– 40162. 10.1074/jbc.M110.145961 20943657 PMC3000997 · DOI
  184. Vernes, S. C. (2017). What bats have to say about speech and language. Psychonomic Bulletin & Review, 24, 111– 117. 10.3758/s13423-016-1060-3 27368623 PMC5325843 · DOI
  185. Vogel, A. C., Petersen, S. E., & Schlaggar, B. L. (2014). The VWFA: It's not just for words anymore. Frontiers in Human Neuroscience, 8, 88 10.3389/fnhum.2014.00088 24688462 PMC3960495 · DOI
  186. Walsh, C. A., & Goffinet, A. M. (2000). Potential mechanisms of mutations that affect neuronal migration in man and mouse. Current Opinion in Genetics & Development, 10, 270– 274. 10.1016/S0959-437X(00)00076-9 10826984 · DOI
  187. Wang, Z. I., Jones, S. E., Jaisani, Z., Najm, I. M., Prayson, R. A., Burgess, R. C., … Alexopoulos, A. V. (2015). Voxel‐based morphometric magnetic resonance imaging (MRI) postprocessing in MRI‐negative epilepsies. Annals of Neurology, 77, 1060– 1075. 10.1002/ana.24407 25807928 PMC4447617 · DOI
  188. Wang, Y., Paramasivam, M., Thomas, A., Bai, J., Kaminen‐Ahola, N., Kere, J., … Loturco, J. J. (2006). DYX1C1 functions in neuronal migration in developing neocortex. Neuroscience, 143, 515– 522. 10.1016/j.neuroscience.2006.08.022 16989952 · DOI
  189. 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 doublecortin. Neuroscience, 190, 398– 408. 10.1016/j.neuroscience.2011.06.010 21689730 PMC3170724 · DOI
  190. Webster, R. I., Erdos, C., Evans, K., Majnemer, A., Saigal, G., Kehayia, E., … Shevell, M. I. (2008). Neurological and magnetic resonance imaging findings in children with developmental language impairment. Journal of Child Neurology, 23, 870– 877. 10.1177/0883073808315620 18660471 · DOI
  191. Wilson, R., Geyer, S. H., Reissig, L., Rose, J., Szumska, D., Hardman, E., … Weninger, W. J. (2017). Highly variable penetrance of abnormal phenotypes in embryonic lethal knockout mice. Wellcome Open Res, 1, 1 10.12688/wellcomeopenres.9899.2 27996060 PMC5159622 · DOI
  192. World Health Organisation (2008). International statistical classification of diseases and related health problems (10th ed.). Geneva, Switzerland: WHO Press.
  193. Yeh, M. L., Gonda, Y., Mommersteeg, M. T., Barber, M., Ypsilanti, A. R., Hanashima, C., … Andrews, W. D. (2014). Robo1 modulates proliferation and neurogenesis in the developing neocortex. Journal of Neuroscience, 34, 5717– 5731. 10.1523/JNEUROSCI.4256-13.2014 24741061 PMC3988420 · DOI
  194. Yuan, W., Zhou, L., Chen, J. H., Wu, J. Y., Rao, Y., & Ornitz, D. M. (1999). The mouse SLIT family: Secreted ligands for ROBO expressed in patterns that suggest a role in morphogenesis and axon guidance. Developmental Biology, 212, 290– 306. 10.1006/dbio.1999.9371 10433822 · DOI
  195. Zhao, J., Thiebaut de Schotten, M., Altarelli, I., Dubois, J., & Ramus, F. (2016). Altered hemispheric lateralization of white matter pathways in developmental dyslexia: Evidence from spherical deconvolution tractography. Cortex, 76, 51– 62. 10.1016/j.cortex.2015.12.004 26859852 · DOI

Cited by

Sorted by citations

Authors
Guidi, L. G., Velayos‐Baeza, A., Martinez‐Garay, I., Monaco, A. P., Paracchini, S., Bishop, D. V. M., & Molnár, Z.
Affiliations
  • Centre for Human Genetics (GB)
  • Department of Physiology, Anatomy, and Genetics University of Oxford Oxford UK
  • Tufts University (US)
  • University of St Andrews (GB)
  • University of Oxford (GB)
Corresponding author
  • Velayos‐Baeza, Antonio
  • Molnár, Zoltán
ORCID
Venue
European Journal of Neuroscience
Publisher
Wiley
Published
2018-10-06
Volume
48
Issue
10
Pages
3212-3233
ISSN
  • 0953-816X (ISSN-L)
  • 1460-9568
DOI
10.1111/ejn.14149
PMC
PMC6282621
OpenAlex
W2790086104
Cited by
59
References
9
Citations by year
2026: 5 · 2025: 3 · 2024: 4 · 2023: 7 · 2022: 13 · 2021: 13 · 2020: 7 · 2019: 5 · 2018: 1 · 2017: 1
FWCI
1.39
Type
journal article
Language
en
Open access
Licence
Locations
  • European Journal of Neuroscience (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, other-oa)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • ORCA Online Research @Cardiff (Cardiff University) (acceptedVersion)
Funders
  • Royal Society (Silvia Paracchini is a Royal Society University Research Fellow)
  • Wellcome Trust (082498/Z/07/Z, 092071/Z/10/Z)
  • Medical Research Council (Luiz G. Guidi received a Doctoral Training Award)
Topics
  • Social Sciences › Psychology › Developmental and Educational Psychology › Reading and Literacy Development
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
  • Social Sciences › Psychology › Developmental and Educational Psychology › Language Development and Disorders
Keywords
developmental dyslexia, neuronal migration, neocortex development, language evolution, postmortem brain studies
MeSH terms
Animals, Cell Movement, Disease Models, Animal, Dyslexia, Humans, Neurons, Neocortex, Genetic Predisposition to Disease

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review