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How interindividual differences in brain anatomy shape reading accuracy

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Abstract

The capacity to read develops throughout intensive academic learning and training. Several studies have investigated the impact of reading on the brain, and particularly how the anatomy of the brain changes with reading acquisition. In the present study, we investigated the converse issue, namely whether and how reading acquisition is constrained by the anatomy of the brain. Using multimodal MRI, we found that (a) the pattern (continuous or interrupted sulcus) of the posterior part of the left lateral occipito-temporal sulcus (OTS) hosting the visual word form area (VWFA) predicts reading skills in adults; that (b) this effect is modulated by the age of reading acquisition; and that (c) the length of the OTS sulcal interruption is associated with reading skills. Because the sulcal pattern is determined in utero, our findings suggest that individual difference in reading skills can be traced back to early stages of brain development in addition to the well-established socioeconomic and educational factors.

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References

  • Aikens NL, Barbarin O (2008) Socioeconomic differences in reading trajectories: the contribution of family, neighborhood, and school contexts. J Educ Psychol 100(2):235

    Article  Google Scholar 

  • Amiez C, Petrides M (2014) Neuroimaging evidence of the anatomo-functional organization of the human cingulate motor areas. Cereb Cortex 24(3):563–578. doi:10.1093/cercor/bhs329

    Article  PubMed  Google Scholar 

  • Borst G, Cachia A, Tissier C, Ahr E, Simon G, Houdé O (2016) Early cerebral constraint on reading skills of 10-years-old children. Mind Brain Educ 10(1):47–54

    Article  Google Scholar 

  • Bouhali F, Thiebaut de Schotten M, Pinel P, Poupon C, Mangin JF, Dehaene S, Cohen L (2014) Anatomical connections of the visual word form area. J Neurosci 34(46):15402–15414. doi:10.1523/JNEUROSCI.4918-13.2014

    Article  CAS  PubMed  Google Scholar 

  • Brem S, Bach S, Kucian K, Guttorm TK, Martin E, Lyytinen H, Brandeis D, Richardson U (2010) Brain sensitivity to print emerges when children learn letter-speech sound correspondences. Proc Natl Acad Sci USA 107(17):7939–7944. doi:10.1073/pnas.0904402107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cachia A, Borst G, Tissier C, Fisher C, Plaze M, Gay O, Riviere D, Gogtay N, Giedd J, Mangin JF, Houde O, Raznahan A (2016) Longitudinal stability of the folding pattern of the anterior cingulate cortex during development. Dev Cogn Neurosci 19:122–127. doi:10.1016/j.dcn.2016.02.011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carreiras M, Seghier ML, Baquero S, Estevez A, Lozano A, Devlin JT, Price CJ (2009) An anatomical signature for literacy. Nature 461(7266):983–986. doi:10.1038/nature08461

    Article  CAS  PubMed  Google Scholar 

  • Castro-Caldas A, Nunes MV, Maestu F, Ortiz T, Simoes R, Fernandes R, de La Guia E, Garcia E, Goncalves M (2009) Learning orthography in adulthood: a magnetoencephalographic study. J Neuropsychol 3(Pt 1):17–30. doi:10.1348/174866408X289953

    Article  CAS  PubMed  Google Scholar 

  • Cohen L, Dehaene S (2004) Specialization within the ventral stream: the case for the visual word form area. Neuroimage 22(1):466–476. doi:10.1016/j.neuroimage.2003.12.049

    Article  PubMed  Google Scholar 

  • Dehaene S, Cohen L (2011) The unique role of the visual word form area in reading. Trends Cogn Sci 15(6):254–262. doi:10.1016/j.tics.2011.04.003

    Article  PubMed  Google Scholar 

  • Dehaene S, Pegado F, Braga LW, Ventura P, Nunes Filho G, Jobert A, Dehaene-Lambertz G, Kolinsky R, Morais J, Cohen L (2010) How learning to read changes the cortical networks for vision and language. Science 330(6009):1359–1364. doi:10.1126/science.1194140

    Article  CAS  PubMed  Google Scholar 

  • Dehaene S, Cohen L, Morais J, Kolinsky R (2015) Illiterate to literate: behavioural and cerebral changes induced by reading acquisition. Nat Rev Neurosci 16(4):234–244. doi:10.1038/nrn3924

    Article  CAS  PubMed  Google Scholar 

  • Dehay C, Giroud P, Berland M, Killackey H, Kennedy H (1996) Contribution of thalamic input to the specification of cytoarchitectonic cortical fields in the primate: effects of bilateral enucleation in the fetal monkey on the boundaries, dimensions, and gyrification of striate and extrastriate cortex. J Comp Neurol 367(1):70–89

    Article  CAS  PubMed  Google Scholar 

  • Dubois J, Hertz-Pannier L, Dehaene-Lambertz G, Cointepas Y, Le Bihan D (2006) Assessment of the early organization and maturation of infants’ cerebral white matter fiber bundles: a feasibility study using quantitative diffusion tensor imaging and tractography. Neuroimage 30(4):1121–1132

    Article  CAS  PubMed  Google Scholar 

  • Dubois J, Dehaene-Lambertz G, Perrin M, Mangin JF, Cointepas Y, Duchesnay E, Le Bihan D, Hertz-Pannier L (2008) Asynchrony of the early maturation of white matter bundles in healthy infants: quantitative landmarks revealed noninvasively by diffusion tensor imaging. Hum Brain Mapp 29(1):14–27. doi:10.1002/hbm.20363

    Article  PubMed  Google Scholar 

  • Dubois J, Dehaene-Lambertz G, Kulikova S, Poupon C, Huppi PS, Hertz-Pannier L (2014) The early development of brain white matter: a review of imaging studies in fetuses, newborns and infants. Neuroscience 276:48–71. doi:10.1016/j.neuroscience.2013.12.044

    Article  CAS  PubMed  Google Scholar 

  • Dubois J, Poupon C, Thirion B, Simonnet H, Kulikova S, Leroy F, Hertz-Pannier L, Dehaene-Lambertz G (2016) Exploring the early organization and maturation of linguistic pathways in the human infant brain. Cereb Cortex 26(5):2283–2298. doi:10.1093/cercor/bhv082

    Article  PubMed  Google Scholar 

  • Duchesnay E, Cachia A, Roche A, Riviere D, Cointepas Y, Papadopoulos-Orfanos D, Zilbovicius M, Martinot JL, Regis J, Mangin JF (2007) Classification based on cortical folding patterns. IEEE Trans Med Imaging 26(4):553–565. doi:10.1109/TMI.2007.892501

    Article  PubMed  Google Scholar 

  • Dumoulin SO, Bittar RG, Kabani NJ, Baker CL Jr, Le Goualher G, Bruce Pike G, Evans AC (2000) A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. Cereb Cortex 10(5):454–463

    Article  CAS  PubMed  Google Scholar 

  • Evans GW (2004) The environment of childhood poverty. Am Psychol 59(2):77

    Article  PubMed  Google Scholar 

  • Farah MJ, Shera DM, Savage JH, Betancourt L, Giannetta JM, Brodsky NL, Malmud EK, Hurt H (2006) Childhood poverty: specific associations with neurocognitive development. Brain Res 1110(1):166–174. doi:10.1016/j.brainres.2006.06.072

    Article  CAS  PubMed  Google Scholar 

  • Fischl B, Rajendran N, Busa E, Augustinack J, Hinds O, Yeo BTT, Mohlberg H, Amunts K, Zilles K (2007) Cortical folding patterns and predicting cytoarchitecture. Cereb Cortex. doi:10.1093/cercor/bhm225

    PubMed  PubMed Central  Google Scholar 

  • Fluss J, Ziegler JC, Warszawski J, Ducot B, Richard G, Billard C (2009) Poor reading in French elementary school: the interplay of cognitive, behavioral, and socioeconomic factors. J Dev Behav Pediatr 30(3):206–216. doi:10.1097/DBP.0b013e3181a7ed6c

    Article  PubMed  Google Scholar 

  • Glezer LS, Riesenhuber M (2013) Individual variability in location impacts orthographic selectivity in the “visual word form area”. J Neurosci 33(27):11221–11226. doi:10.1523/JNEUROSCI.5002-12.2013

    Article  CAS  PubMed  Google Scholar 

  • Gomez J, Barnett MA, Natu V, Mezer A, Palomero-Gallagher N, Weiner KS, Amunts K, Zilles K, Grill-Spector K (2017) Microstructural proliferation in human cortex is coupled with the development of face processing. Science 355(6320):68–71. doi:10.1126/science.aag0311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grömping U (2015) Variable importance in regression models. Wiley Interdiscip Rev Comput Stat 7(2):137–152

    Article  Google Scholar 

  • Hackman DA, Farah MJ (2009) Socioeconomic status and the developing brain. Trends Cogn Sci 13(2):65–73. doi:10.1016/j.tics.2008.11.003

    Article  PubMed  PubMed Central  Google Scholar 

  • Hackman DA, Farah MJ, Meaney MJ (2010) Socioeconomic status and the brain: mechanistic insights from human and animal research. Nat Rev Neurosci 11(9):651–659. doi:10.1038/nrn2897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hilgetag CC, Barbas H (2006) Role of mechanical factors in the morphology of the primate cerebral cortex. PLoS Comput Biol 2(3):e22

    Article  PubMed  PubMed Central  Google Scholar 

  • 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. Dev Sci 13(6):876–885. doi:10.1111/j.1467-7687.2009.00938.x

    Article  PubMed  Google Scholar 

  • Jednorog K, Altarelli I, Monzalvo K, Fluss J, Dubois J, Billard C, Dehaene-Lambertz G, Ramus F (2012) The influence of socioeconomic status on children’s brain structure. PLoS ONE 7(8):e42486. doi:10.1371/journal.pone.0042486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee VE, Burkam DT (2002) Inequality at the starting gate: social background differences in achievement as children begin school. Economic Policy Institute, Washington, DC

  • Leroy F, Glasel H, Dubois J, Hertz-Pannier L, Thirion B, Mangin JF, Dehaene-Lambertz G (2011) Early maturation of the linguistic dorsal pathway in human infants. J Neurosci 31(4):1500–1506. doi:10.1523/JNEUROSCI.4141-10.2011

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Sescousse G, Amiez C, Dreher JC (2015) Local morphology predicts functional organization of experienced value signals in the human orbitofrontal cortex. J Neurosci 35(4):1648–1658. doi:10.1523/JNEUROSCI.3058-14.2015

    Article  CAS  PubMed  Google Scholar 

  • Mangin JF, Riviere D, Cachia A, Duchesnay E, Cointepas Y, Papadopoulos-Orfanos D, Scifo P, Ochiai T, Brunelle F, Regis J (2004) A framework to study the cortical folding patterns. Neuroimage 23(Suppl 1):S129–S138

    Article  PubMed  Google Scholar 

  • Mangin JF, Jouvent E, Cachia A (2010) In-vivo measurement of cortical morphology: means and meanings. Curr Opin Neurol 23(4):359–367. doi:10.1097/WCO.0b013e32833a0afc

    PubMed  Google Scholar 

  • Martin A, Schurz M, Kronbichler M, Richlan F (2015) Reading in the brain of children and adults: a meta-analysis of 40 functional magnetic resonance imaging studies. Hum Brain Mapp 36(5):1963–1981. doi:10.1002/hbm.22749

    Article  PubMed  PubMed Central  Google Scholar 

  • Mongelli V, Dehaene S, Vinckier F, Peretz I, Bartolomeo P, Cohen L (2017) Music and words in the visual cortex: the impact of musical expertise. Cortex 86:260–274. doi:10.1016/j.cortex.2016.05.016

    Article  PubMed  Google Scholar 

  • Myers CA, Vandermosten M, Farris EA, Hancock R, Gimenez P, Black JM, Casto B, Drahos M, Tumber M, Hendren RL, Hulme C, Hoeft F (2014) White matter morphometric changes uniquely predict children’s reading acquisition. Psychol Sci 25(10):1870–1883. doi:10.1177/0956797614544511

    Article  PubMed  PubMed Central  Google Scholar 

  • Noble KG, McCandliss BD (2005) Reading development and impairment: behavioral, social, and neurobiological factors. J Dev Behav Pediatr 26(5):370–378

    Article  PubMed  Google Scholar 

  • Noble KG, McCandliss BD, Farah MJ (2007) Socioeconomic gradients predict individual differences in neurocognitive abilities. Dev Sci 10(4):464–480. doi:10.1111/j.1467-7687.2007.00600.x

    Article  PubMed  Google Scholar 

  • Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113

    Article  CAS  PubMed  Google Scholar 

  • Ono M, Kubik S, Abarnathey CD (1990) Atlas of the cerebral sulci. Georg Thieme, New York

    Google Scholar 

  • Pegado F, Comerlato E, Ventura F, Jobert A, Nakamura K, Buiatti M, Ventura P, Dehaene-Lambertz G, Kolinsky R, Morais J, Braga LW, Cohen L, Dehaene S (2014) Timing the impact of literacy on visual processing. Proc Natl Acad Sci USA 111(49):E5233–E5242. doi:10.1073/pnas.1417347111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plomin R, Deary IJ (2015) Genetics and intelligence differences: five special findings. Mol Psychiatry 20(1):98–108. doi:10.1038/mp.2014.105

    Article  CAS  PubMed  Google Scholar 

  • Raizada RD, Kishiyama MM (2010) Effects of socioeconomic status on brain development, and how cognitive neuroscience may contribute to levelling the playing field. Front Hum Neurosci 4(3):1000

    Google Scholar 

  • Saygin ZM, Osher DE, Norton ES, Youssoufian DA, Beach SD, Feather J, Gaab N, Gabrieli JD, Kanwisher N (2016) Connectivity precedes function in the development of the visual word form area. Nat Neurosci 19(9):1250–1255. doi:10.1038/nn.4354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simon G, Lanoe C, Poirel N, Rossi S, Lubin A, Pineau A, Houde O (2013) Dynamics of the anatomical changes that occur in the brains of schoolchildren as they learn to read. PLoS ONE 8(12):e81789. doi:10.1371/journal.pone.0081789

    Article  PubMed  PubMed Central  Google Scholar 

  • Thiebaut de Schotten M, Cohen L, Amemiya E, Braga LW, Dehaene S (2014) Learning to read improves the structure of the arcuate fasciculus. Cereb Cortex 24(4):989–995. doi:10.1093/cercor/bhs383

    Article  PubMed  Google Scholar 

  • Tomalski P, Johnson MH (2010) The effects of early adversity on the adult and developing brain. Curr Opin Psychiatry 23(3):233–238. doi:10.1097/YCO.0b013e3283387a8c

    Article  PubMed  Google Scholar 

  • Van Essen DC (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature 385(6614):313–318

    Article  PubMed  Google Scholar 

  • Vinckier F, Dehaene S, Jobert A, Dubus JP, Sigman M, Cohen L (2007) Hierarchical coding of letter strings in the ventral stream: dissecting the inner organization of the visual word-form system. Neuron 55(1):143–156. doi:10.1016/j.neuron.2007.05.031

    Article  CAS  PubMed  Google Scholar 

  • Weiner KS, Barnett MA, Lorenz S, Caspers J, Stigliani A, Amunts K, Zilles K, Fischl B, Grill-Spector K (2017) The cytoarchitecture of domain-specific regions in human high-level visual cortex. Cereb Cortex 27(1):146–161. doi:10.1093/cercor/bhw361

    Article  PubMed  Google Scholar 

  • Whitehurst GJ, Lonigan CJ (1998) Child development and emergent literacy. Child Dev 69(3):848–872

    Article  CAS  PubMed  Google Scholar 

  • Xue Y, Meisels SJ (2004) Early literacy instruction and learning in kindergarten: evidence from the early childhood longitudinal study—kindergarten class of 1998–1999. Am Educ Res J 41(1):191–229

    Article  Google Scholar 

  • Yeatman JD, Dougherty RF, Ben-Shachar M, Wandell BA (2012) Development of white matter and reading skills. Proc Natl Acad Sci USA 109(44):E3045–E3053. doi:10.1073/pnas.1206792109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zilles K, Palomero-Gallagher N, Amunts K (2013) Development of cortical folding during evolution and ontogeny. Trends Neurosci 36(5):275–284. doi:10.1016/j.tins.2013.01.006

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We thank S. F. Pegado, P. Ventura, G. Nunes Filho, G. Dehaene-Lambertz, R. Kolinsky, J. Morais, and L. Cohen for participant recruitment.

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Author notes

  1. Arnaud Cachia and Margot Roell have equally contributed to this study.

Authors and Affiliations

  1. Laboratory for the Psychology of Child Development and Education, CNRS UMR8240, Sorbonne, 46 Rue Saint-Jacques, 75005, Paris, France

    Arnaud Cachia, Margot Roell, Olivier Houde & Grégoire Borst

  2. Paris Descartes University, Sorbonne Paris Cité, Paris, France

    Arnaud Cachia, Margot Roell, Olivier Houde & Grégoire Borst

  3. Institut Universitaire de France, Paris, France

    Arnaud Cachia, Olivier Houde & Grégoire Borst

  4. Biomarkers of Brain Development and Disorders, Center of Psychiatry and Neurosciences, INSERM UMR894, Paris, France

    Arnaud Cachia

  5. Cognitive Neuroimaging Unit, CEA DSV/I2BM, INSERM, NeuroSpin Center, Université Paris-Sud, Université Paris-Saclay, Gif-sur-Yvette, France

    Margot Roell & Stanislas Dehaene

  6. Ecole des Neurosciences de Paris (ENP), Paris, France

    Arnaud Cachia, Margot Roell, Jean-François Mangin, Zhong Yi Sun, Olivier Houde, Stanislas Dehaene & Grégoire Borst

  7. UNATI, Neurospin, CEA, 91191, Gif-sur-Yvette, France

    Jean-François Mangin, Zhong Yi Sun & Antoinette Jobert

  8. CATI Multicenter Neuroimaging Platform, Neurospin, cati-neuroimaging.com, 91191, Gif-sur-Yvette, France

    Jean-François Mangin & Zhong Yi Sun

  9. SARAH Network-International Center for Neurosciences and Rehabilitation, QL 13, Lago Norte, 71, Brasilia, DF, 535-005, Brazil

    Lucia Braga

  10. Collège de France, Paris, France

    Stanislas Dehaene

Authors
  1. Arnaud Cachia
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  2. Margot Roell
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  3. Jean-François Mangin
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  4. Zhong Yi Sun
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  5. Antoinette Jobert
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  6. Lucia Braga
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  7. Olivier Houde
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  8. Stanislas Dehaene
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  9. Grégoire Borst
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Contributions

AC, GB, SD, and OH designed the study. AJ, LB, and SD provided MRI and cognitive data. MR, AC, GB, AJ, J-FM, and ZYS analyzed the data. AC, GB, SD, OH, J-FM, and MR interpreted the results and wrote the manuscript.

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Correspondence to Arnaud Cachia.

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Cachia, A., Roell, M., Mangin, JF. et al. How interindividual differences in brain anatomy shape reading accuracy. Brain Struct Funct 223, 701–712 (2018). https://doi.org/10.1007/s00429-017-1516-x

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