Skip to main content
Log in

Atypical characteristic changes of surface morphology and structural covariance network in developmental dyslexia

  • Original Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Background

Developmental dyslexia (DD) is a neurodevelopmental disorder that is characterized by difficulties with all aspects of information acquisition in the written word, including slow and inaccurate word recognition. The neural basis behind DD has not been fully elucidated.

Method

The study included 22 typically developing (TD) children, 16 children with isolated spelling disorder (SpD), and 20 children with DD. The cortical thickness, folding index, and mean curvature of Broca’s area, including the triangular part of the left inferior frontal gyrus (IFGtriang) and the opercular part of the left inferior frontal gyrus, were assessed to explore the differences of surface morphology among the TD, SpD, and DD groups. Furthermore, the structural covariance network (SCN) of the triangular part of the left inferior frontal gyrus was analyzed to explore the changes of structural connectivity in the SpD and DD groups.

Results

The DD group showed higher curvature and cortical folding of the left IFGtriang than the TD group and SpD group. In addition, compared with the TD group and the SpD group, the structural connectivity between the left IFGtriang and the left middle-frontal gyrus and the right mid-orbital frontal gyrus was increased in the DD group, and the structural connectivity between the left IFGtriang and the right precuneus and anterior cingulate was decreased in the DD group.

Conclusion

DD had atypical structural connectivity in brain regions related to visual attention, memory and which might impact the information input and integration needed for reading and spelling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Neuroimaging data was obtained from the open access dataset hosted on the OpenNeuro.org (https://doi.org/10.18112/openneuro.ds003126.v1.0.0), which is a free and open platform that allows researchers to upload and share neuroimaging data.

References

  1. Alexander-Bloch A, Raznahan A, Bullmore E, Giedd J (2013) The convergence of maturational change and structural covariance in human cortical networks. J Neurosci 33(7):2889–2899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Banfi C, Koschutnig K, Moll K, Schulte-Körne G, Fink A, Landerl K (2020) Reading-related functional activity in children with isolated spelling deficits and dyslexia. Lang, Cogn Neurosci 36(5):543–561

    Article  Google Scholar 

  3. Battistella G, Henry M, Gesierich B et al (2019) Differential intrinsic functional connectivity changes in semantic variant primary progressive aphasia. Neuroimage Clin 22:101797

    Article  PubMed  PubMed Central  Google Scholar 

  4. Beelen C, Vanderauwera J, Wouters J, Vandermosten M, Ghesquière P (2019) Atypical gray matter in children with dyslexia before the onset of reading instruction. Cortex 121:399–413

    Article  PubMed  Google Scholar 

  5. Bergmann HC, Rijpkema M, Fernández G, Kessels RP (2012) Distinct neural correlates of associative working memory and long-term memory encoding in the medial temporal lobe. Neuroimage 63(2):989–997

    Article  PubMed  Google Scholar 

  6. Blankenship TL, Slough MA, Calkins SD, Deater-Deckard K, Kim-Spoon J, Bell MA (2019) Attention and executive functioning in infancy: links to childhood executive function and reading achievement. Dev Sci 22(6):e12824

    Article  PubMed  PubMed Central  Google Scholar 

  7. Boets B, Op de Beeck HP, Vandermosten M et al (2013) Intact but less accessible phonetic representations in adults with dyslexia. Science 342(6163):1251–1254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Botvinick MM, Braver TS, Barch DM, Carter CS, Cohen JD (2001) Conflict monitoring and cognitive control. Psychol Rev 108(3):624–652

    Article  CAS  PubMed  Google Scholar 

  9. Braid J, Richlan F (2022) The functional neuroanatomy of reading intervention. Front Neurosci 16:921931

    Article  PubMed  PubMed Central  Google Scholar 

  10. Carmichael ST, Price JL (1995) Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 363(4):642–664

    Article  CAS  PubMed  Google Scholar 

  11. Chung KKH, Lam CB (2020) Cognitive-linguistic skills underlying word reading and spelling difficulties in Chinese adolescents with dyslexia. J Learn Disabil 53(1):48–59

    Article  CAS  PubMed  Google Scholar 

  12. D’Mello AM, Gabrieli JDE (2018) Cognitive neuroscience of dyslexia. Lang Speech Hear Serv Sch 49(4):798–809

    Article  PubMed  Google Scholar 

  13. Dębska A, Banfi C, Chyl K et al (2021) Neural patterns of word processing differ in children with dyslexia and isolated spelling deficit. Brain Struct Funct 226(5):1467–1478

    Article  PubMed  PubMed Central  Google Scholar 

  14. DeMarco AT, Wilson SM, Rising K, Rapcsak SZ, Beeson PM (2017) Neural substrates of sublexical processing for spelling. Brain Lang 164:118–128

    Article  PubMed  Google Scholar 

  15. Démonet JF, Taylor MJ, Chaix Y (2004) Developmental dyslexia. Lancet 363(9419):1451–1460

    Article  PubMed  Google Scholar 

  16. Dynak A, Kossowski B, Chyl K et al (2021) Separating the influences of late talking and dyslexia on brain structure. J Abnorm Psychol 130(3):286–296

    Article  PubMed  Google Scholar 

  17. Fiebach CJ, Schlesewsky M, Lohmann G, von Cramon DY, Friederici AD (2005) Revisiting the role of Broca’s area in sentence processing: syntactic integration versus syntactic working memory. Hum Brain Mapp 24(2):79–91

    Article  CAS  PubMed  Google Scholar 

  18. Fine JM, Hayden BY (2022) The whole prefrontal cortex is premotor cortex. Philos Trans R Soc Lond B Biol Sci 377(1844):20200524

    Article  PubMed  Google Scholar 

  19. Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A 97(20):11050–11055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Fischl B, Liu A, Dale AM (2001) Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging 20(1):70–80

    Article  CAS  PubMed  Google Scholar 

  21. Frye RE, Liederman J, Malmberg B, McLean J, Strickland D, Beauchamp MS (2010) Surface area accounts for the relation of gray matter volume to reading-related skills and history of dyslexia. Cereb Cortex 20(11):2625–2635

    Article  PubMed  PubMed Central  Google Scholar 

  22. Hauswald A, Lithari C, Collignon O, Leonardelli E, Weisz N (2018) A visual cortical network for deriving phonological information from intelligible lip movements. Curr Biol 28(9):1453-1459.e3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Heim S, Wehnelt A, Grande M, Huber W, Amunts K (2013) Effects of lexicality and word frequency on brain activation in dyslexic readers. Brain Lang 125(2):194–202

    Article  PubMed  Google Scholar 

  24. Hofmann MJ, Dambacher M, Jacobs AM et al (2014) Occipital and orbitofrontal hemodynamics during naturally paced reading: an fNIRS study. Neuroimage 94:193–202

    Article  PubMed  Google Scholar 

  25. Hosseini SM, Black JM, Soriano T et al (2013) Topological properties of large-scale structural brain networks in children with familial risk for reading difficulties. Neuroimage 71:260–274

    Article  PubMed  Google Scholar 

  26. Jedidi Z, Manard M, Balteau E et al (2021) Incidental verbal semantic processing recruits the fronto-temporal semantic control network. Cereb Cortex 31(12):5449–5459

    Article  CAS  PubMed  Google Scholar 

  27. Jobard G, Crivello F, Tzourio-Mazoyer N (2003) Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies. Neuroimage 20(2):693–712

    Article  CAS  PubMed  Google Scholar 

  28. Jones AC, Rawson KA (2016) Do reading and spelling share a lexicon? Cogn Psychol 86:152–184

    Article  PubMed  Google Scholar 

  29. Knudsen EB, Wallis JD (2022) Taking stock of value in the orbitofrontal cortex. Nat Rev Neurosci 23(7):428–438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Kuhl U, Neef NE, Kraft I et al (2020) The emergence of dyslexia in the developing brain. Neuroimage 211:116633

    Article  PubMed  Google Scholar 

  31. Lee MM, Drury BC, McGrath LM, Stoodley CJ (2023) Shared grey matter correlates of reading and attention. Brain Lang 237:105230

    Article  PubMed  PubMed Central  Google Scholar 

  32. Li Y, Bi HY (2022) Comparative research on neural dysfunction in children with dyslexia under different writing systems: a meta-analysis study. Neurosci Biobehav Rev 137:104650

    Article  PubMed  Google Scholar 

  33. Liang S, Huang L, Zhan S, et al (2023) Altered morphological characteristics and structural covariance connectivity associated with verbal working memory performance in ADHD children. Br J Radiol 96(1151):20230409

  34. Londei A, D’Ausilio A, Basso D, Sestieri C, Gratta CD, Romani GL, Belardinelli MO (2010) Sensory-motor brain network connectivity for speech comprehension. Hum Brain Mapp 31(4):567–580

    Article  PubMed  Google Scholar 

  35. Lubeiro A, de Luis-García R, Rodríguez M, Álvarez A, de la Red H, Molina V (2017) Biological and cognitive correlates of cortical curvature in schizophrenia. Psychiatry Res Neuroimaging 270:68–75

    Article  PubMed  Google Scholar 

  36. Ludersdorfer P, Kronbichler M, Wimmer H (2015) Accessing orthographic representations from speech: the role of left ventral occipitotemporal cortex in spelling. Hum Brain Mapp 36(4):1393–1406

    Article  PubMed  Google Scholar 

  37. MacSweeney M, Brammer MJ, Waters D, Goswami U (2009) Enhanced activation of the left inferior frontal gyrus in deaf and dyslexic adults during rhyming. Brain 132(Pt 7):1928–1940

    Article  PubMed  PubMed Central  Google Scholar 

  38. Morken F, Helland T, Hugdahl K, Specht K (2017) Reading in dyslexia across literacy development: a longitudinal study of effective connectivity. Neuroimage 144(Pt A):92–100

    Article  PubMed  Google Scholar 

  39. Nestor PG, Nakamura M, Niznikiewicz M, Levitt JJ, Newell DT, Shenton ME, McCarley RW (2015) Attentional control and intelligence: MRI orbital frontal gray matter and neuropsychological correlates. Behav Neurol 2015:354186

    Article  PubMed  PubMed Central  Google Scholar 

  40. Niolaki GZ, Negoita A, Vousden JI, Terzopoulos AR, Taylor L, Masterson J (2023) What spelling errors can tell us about the development of processes involved in children’s spelling. Front Psychol 14:1178427

    Article  PubMed  PubMed Central  Google Scholar 

  41. Nora A, Renvall H, Ronimus M, Kere J, Lyytinen H, Salmelin R (2021) Children at risk for dyslexia show deficient left-hemispheric memory representations for new spoken word forms. Neuroimage 229:117739

    Article  CAS  PubMed  Google Scholar 

  42. Nouwens S, Groen MA, Kleemans T, Verhoeven L (2021) How executive functions contribute to reading comprehension. Br J Educ Psychol 91(1):169–192

    Article  PubMed  Google Scholar 

  43. Ojanen V, Möttönen R, Pekkola J, Jääskeläinen IP, Joensuu R, Autti T, Sams M (2005) Processing of audiovisual speech in Broca’s area. Neuroimage 25(2):333–338

    Article  PubMed  Google Scholar 

  44. Ostertag C, Reynolds JE, Dewey D, Landman B, Huo Y, Lebel C (2022) Altered gray matter development in pre-reading children with a family history of reading disorder. Dev Sci 25(2):e13160

    Article  PubMed  Google Scholar 

  45. Paulesu E, Frith U, Snowling M, Gallagher A, Morton J, Frackowiak RS, Frith CD (1996) Is developmental dyslexia a disconnection syndrome? Evidence from PET scanning. Brain 119(Pt 1):143–157

    Article  PubMed  Google Scholar 

  46. Paz-Alonso PM, Oliver M, Lerma-Usabiaga G et al (2018) Neural correlates of phonological, orthographic and semantic reading processing in dyslexia. Neuroimage Clin 20:433–447

    Article  PubMed  PubMed Central  Google Scholar 

  47. Peterson RL, Pennington BF (2012) Developmental dyslexia. Lancet 379(9830):1997–2007

    Article  PubMed  PubMed Central  Google Scholar 

  48. Peyrin C, Démonet JF, N’Guyen-Morel MA, Le Bas JF, Valdois S (2011) Superior parietal lobule dysfunction in a homogeneous group of dyslexic children with a visual attention span disorder. Brain Lang 118(3):128–138

    Article  CAS  PubMed  Google Scholar 

  49. Purcell JJ, Jiang X, Eden GF (2017) Shared orthographic neuronal representations for spelling and reading. Neuroimage 147:554–567

    Article  PubMed  Google Scholar 

  50. Purcell JJ, Napoliello EM, Eden GF (2011) A combined fMRI study of typed spelling and reading. Neuroimage 55(2):750–762

    Article  PubMed  Google Scholar 

  51. Qi T, Schaadt G, Cafiero R, Brauer J, Skeide MA, Friederici AD (2019) The emergence of long-range language network structural covariance and language abilities. Neuroimage 191:36–48

    Article  PubMed  Google Scholar 

  52. Reuter M, Rosas HD, Fischl B (2010) Highly accurate inverse consistent registration: a robust approach. Neuroimage 53(4):1181–1196

    Article  PubMed  Google Scholar 

  53. Richlan F (2014) Functional neuroanatomy of developmental dyslexia: the role of orthographic depth. Front Hum Neurosci 8:347

    Article  PubMed  PubMed Central  Google Scholar 

  54. Richlan F, Kronbichler M, Wimmer H (2013) Structural abnormalities in the dyslexic brain: a meta-analysis of voxel-based morphometry studies. Hum Brain Mapp 34(11):3055–3065

    Article  PubMed  Google Scholar 

  55. Rodriguez-Carranza CE, Mukherjee P, Vigneron D, Barkovich J, Studholme C (2008) A framework for in vivo quantification of regional brain folding in premature neonates. Neuroimage 41(2):462–478

    Article  CAS  PubMed  Google Scholar 

  56. Rogalsky C, LaCroix AN, Chen KH, Anderson SW, Damasio H, Love T, Hickok G (2018) The neurobiology of agrammatic sentence comprehension: a lesion study. J Cogn Neurosci 30(2):234–255

    Article  PubMed  Google Scholar 

  57. Sanfilippo J, Ness M, Petscher Y, Rappaport L, Zuckerman B, Gaab N (2020) Reintroducing dyslexia: early identification and implications for pediatric practice. Pediatrics 146(1):e20193046

  58. Schulte-Körne G (2010) The prevention, diagnosis, and treatment of dyslexia. Dtsch Arztebl Int 107(41):718–26 (quiz 27)

    PubMed  PubMed Central  Google Scholar 

  59. Ségonne F, Dale AM, Busa E, Glessner M, Salat D, Hahn HK, Fischl B (2004) A hybrid approach to the skull stripping problem in MRI. Neuroimage 22(3):1060–1075

    Article  PubMed  Google Scholar 

  60. Shaywitz SE, Shaywitz JE, Shaywitz BA (2021) Dyslexia in the 21st century. Curr Opin Psychiatry 34(2):80–86

    Article  PubMed  Google Scholar 

  61. Sheena MK, Jimmy J, Burkhouse KL, Klumpp H (2021) Anterior cingulate cortex activity during attentional control corresponds with rumination in depression and social anxiety. Psychiatry Res Neuroimaging 317:111385

    Article  PubMed  PubMed Central  Google Scholar 

  62. Sheppard SM, Meier EL, Kim KT et al (2022) Neural correlates of syntactic comprehension: a longitudinal study. Brain Lang 225:105068

    Article  PubMed  Google Scholar 

  63. Terras MM, Thompson LC, Minnis H (2009) Dyslexia and psycho-social functioning: an exploratory study of the role of self-esteem and understanding. Dyslexia 15(4):304–327

    Article  PubMed  Google Scholar 

  64. Trambaiolli LR, Peng X, Lehman JF et al (2022) Anatomical and functional connectivity support the existence of a salience network node within the caudal ventrolateral prefrontal cortex. Elife 11:e76334

  65. van der Mark S, Klaver P, Bucher K et al (2011) The left occipitotemporal system in reading: disruption of focal fMRI connectivity to left inferior frontal and inferior parietal language areas in children with dyslexia. Neuroimage 54(3):2426–2436

    Article  PubMed  Google Scholar 

  66. Van Essen DC, Dierker D, Snyder AZ, Raichle ME, Reiss AL, Korenberg J (2006) Symmetry of cortical folding abnormalities in Williams syndrome revealed by surface-based analyses. J Neurosci 26(20):5470–5483

    Article  PubMed  PubMed Central  Google Scholar 

  67. Vandermosten M, Boets B, Poelmans H, Sunaert S, Wouters J, Ghesquière P (2012) A tractography study in dyslexia: neuroanatomic correlates of orthographic, phonological and speech processing. Brain 135(Pt 3):935–948

    Article  PubMed  Google Scholar 

  68. Vandermosten M, Boets B, Wouters J, Ghesquière P (2012) A qualitative and quantitative review of diffusion tensor imaging studies in reading and dyslexia. Neurosci Biobehav Rev 36(6):1532–1552

    Article  PubMed  Google Scholar 

  69. Vogel AC, Church JA, Power JD, Miezin FM, Petersen SE, Schlaggar BL (2013) Functional network architecture of reading-related regions across development. Brain Lang 125(2):231–243

    Article  PubMed  Google Scholar 

  70. Vossel S, Geng JJ, Fink GR (2014) Dorsal and ventral attention systems: distinct neural circuits but collaborative roles. Neuroscientist 20(2):150–159

    Article  PubMed  PubMed Central  Google Scholar 

  71. Wandell BA, Rauschecker AM, Yeatman JD (2012) Learning to see words. Annu Rev Psychol 63:31–53

    Article  PubMed  Google Scholar 

  72. Wu Y, Wang J, Zhang Y et al (2016) The neuroanatomical basis for posterior superior parietal lobule control lateralization of visuospatial attention. Front Neuroanat 10:32

    Article  PubMed  PubMed Central  Google Scholar 

  73. Xia Z, Yang T, Cui X et al (2021) Atypical relationships between neurofunctional features of print-sound integration and reading abilities in Chinese children with dyslexia. Front Psychol 12:748644

    Article  PubMed  Google Scholar 

  74. Xu Q, Zhang Q, Liu G et al (2021) BCCT: a GUI toolkit for brain structural covariance connectivity analysis on MATLAB. Front Hum Neurosci 15:641961

    Article  PubMed  PubMed Central  Google Scholar 

  75. Yang Y, Zuo Z, Tam F et al (2022) The brain basis of handwriting deficits in Chinese children with developmental dyslexia. Dev Sci 25(2):e13161

  76. Yu X, Ferradal S, Dunstan J et al (2022) Patterns of neural functional connectivity in infants at familial risk of developmental dyslexia. JAMA Netw Open 5(10):e2236102

    Article  PubMed  PubMed Central  Google Scholar 

  77. Yun JY, Boedhoe PSW, Vriend C et al (2020) Brain structural covariance networks in obsessive-compulsive disorder: a graph analysis from the ENIGMA Consortium. Brain 143(2):684–700

    PubMed  PubMed Central  Google Scholar 

  78. Yun JY, Kim SN, Lee TY, Chon MW, Kwon JS (2016) Individualized covariance profile of cortical morphology for auditory hallucinations in first-episode psychosis. Hum Brain Mapp 37(3):1051–1065

    Article  PubMed  Google Scholar 

  79. Zoccolotti P, De Luca M, Marinelli CV, Spinelli D (2020) Predicting individual differences in reading, spelling and maths in a sample of typically developing children: a study in the perspective of comorbidity. PLoS One 15(4):e0231937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by the Natural Science Foundation of Fujian Province (2022J01880), the Scientific Research Foundation for the High-level Talents funded by Fujian University of Traditional Chinese Medicine (X2019002—talents), the Youth Science and Technology Innovation Cultivation Program by Fujian University of Traditional Chinese Medicine (XQC2023003), the Natural Science Foundation of Henan Province (222300420250), and the Municipal Science and Technology Plan Project of Nanyang City (JCQY009).

Author information

Authors and Affiliations

Authors

Contributions

LSX was responsible for the study concept and design. ZYS, HJY, HL, PLX, WXX, ZQQ, YJC, LZF, and SX were responsible for the data analyses. ZYS, HJY, and HL drafted the manuscript. LSX, SX, and ZY critically reviewed the manuscript. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Shengxiang Liang.

Ethics declarations

Ethical approval

None.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, Y., Huang, J., Huang, L. et al. Atypical characteristic changes of surface morphology and structural covariance network in developmental dyslexia. Neurol Sci 45, 2261–2270 (2024). https://doi.org/10.1007/s10072-023-07193-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-023-07193-x

Keywords

Navigation