The brain basis of handwriting deficits in Chinese children with developmental dyslexia.

Yang Yang, Zhentao Zuo, Fred Tam, Simon J Graham, Junjun Li, Yuzhu Ji, Zelong Meng, Chanyuan Gu, Hong-Yan Bi, Jian Ou, Min Xu
Author Information
  1. Yang Yang: CAS Key Laboratory of Behavioral Science, Center for Brain Science and Learning Difficulties, Institute of Psychology,Chinese Academy of Sciences, Beijing, China.
  2. Zhentao Zuo: State Key Laboratory of Brain and Cognitive Science, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China.
  3. Fred Tam: Physical Sciences Platform, Sunnybrook Research Institute, Toronto, Canada.
  4. Simon J Graham: Physical Sciences Platform, Sunnybrook Research Institute, Toronto, Canada.
  5. Junjun Li: CAS Key Laboratory of Behavioral Science, Center for Brain Science and Learning Difficulties, Institute of Psychology,Chinese Academy of Sciences, Beijing, China.
  6. Yuzhu Ji: Department of Psychology, College of Education, Zhejiang University of Technology, Hangzhou, China.
  7. Zelong Meng: Department of Psychology, School of Humanities and Social Sciences, Beijing Forestry University, Beijing, China.
  8. Chanyuan Gu: Department of Chinese and Bilingual Studies, Faculty of Humanities, The Hong Kong Polytechnic University, Hong Kong, China.
  9. Hong-Yan Bi: CAS Key Laboratory of Behavioral Science, Center for Brain Science and Learning Difficulties, Institute of Psychology,Chinese Academy of Sciences, Beijing, China.
  10. Jian Ou: Center for Brain Disorders and Cognitive Sciences, Shenzhen University, Shenzhen, China.
  11. Min Xu: Center for Brain Disorders and Cognitive Sciences, Shenzhen University, Shenzhen, China. ORCID

Abstract

Abundant behavioral studies have demonstrated high comorbidity of reading and handwriting difficulties in developmental dyslexia (DD), a neurological condition characterized by unexpectedly low reading ability despite adequate nonverbal intelligence and typical schooling. The neural correlates of handwriting deficits remain largely unknown; however, as well as the extent that handwriting deficits share common neural bases with reading deficits in DD. The present work used functional magnetic resonance imaging to examine brain activity during handwriting and reading tasks in Chinese dyslexic children (n = 18) and age-matched controls (n = 23). Compared to controls, dyslexic children exhibited reduced activation during handwriting tasks in brain regions supporting sensory-motor processing (including supplementary motor area and postcentral gyrus) and visual-orthography processing (including bilateral precuneus and right cuneus). Among these regions, the left supplementary motor area and the right precuneus also showed a trend of reduced activation during reading tasks in dyslexics. Moreover, increased activation was found in the left inferior frontal gyrus and anterior cingulate cortex in dyslexics, which may reflect more efforts of executive control to compensate for the impairments of motor and visual-orthographic processing. Finally, dyslexic children exhibited aberrant functional connectivity among brain areas for cognitive control and sensory-motor processes during handwriting tasks. Together, these findings suggest that handwriting deficits in DD are associated with functional abnormalities of multiple brain regions implicated in motor execution, visual-orthographic processing, and cognitive control, providing important implications for the diagnosis and treatment of dyslexia.

Keywords

References

  1. Front Psychol. 2011 Oct 11;2:239 [PMID: 22013427]
  2. Nat Rev Neurosci. 2008 Nov;9(11):856-69 [PMID: 18843271]
  3. Ann N Y Acad Sci. 2008 Dec;1145:237-59 [PMID: 19076401]
  4. Handb Clin Neurol. 2013;111:229-35 [PMID: 23622168]
  5. Science. 2004 Feb 13;303(5660):1023-6 [PMID: 14963333]
  6. Trends Cogn Sci. 2013 Feb;17(2):56-7 [PMID: 23357712]
  7. Hum Brain Mapp. 2011 Feb;32(2):240-8 [PMID: 20336688]
  8. Proc Natl Acad Sci U S A. 2005 Jun 14;102(24):8781-5 [PMID: 15939871]
  9. Brain Lang. 2011 Nov;119(2):60-7 [PMID: 21220170]
  10. Neuroimage. 2012 Oct 15;63(1):381-91 [PMID: 22759996]
  11. Science. 2009 Jul 17;325(5938):280-3 [PMID: 19608907]
  12. J Cogn Neurosci. 1999 May;11(3):282-99 [PMID: 10402256]
  13. Res Dev Disabil. 2020 Feb;97:103553 [PMID: 31841819]
  14. Lancet. 2012 May 26;379(9830):1997-2007 [PMID: 22513218]
  15. Dev Sci. 2022 Mar;25(2):e13161 [PMID: 34288292]
  16. Neuroimage Clin. 2015 Mar 28;8:408-21 [PMID: 26106566]
  17. Hum Brain Mapp. 2017 Nov;38(11):5331-5342 [PMID: 28745021]
  18. J Cogn Neurosci. 2011 Dec;23(12):4067-81 [PMID: 21812571]
  19. Brain Struct Funct. 2021 Jun;226(5):1627-1639 [PMID: 33866405]
  20. J Neurophysiol. 1998 Nov;80(5):2671-87 [PMID: 9819272]
  21. J Exp Psychol Hum Percept Perform. 2011 Aug;37(4):1310-22 [PMID: 21500939]
  22. Cortex. 2017 Mar;88:66-80 [PMID: 28081451]
  23. Ann Dyslexia. 2015 Jul;65(2):53-68 [PMID: 25876887]
  24. Res Dev Disabil. 2011 Sep-Oct;32(5):1745-56 [PMID: 21507609]
  25. Curr Biol. 2009 Oct 13;19(19):R890-2 [PMID: 19825347]
  26. J Exp Psychol Learn Mem Cogn. 2014 Sep;40(5):1441-7 [PMID: 24548322]
  27. Hum Brain Mapp. 2018 Oct;39(10):4065-4082 [PMID: 29923271]
  28. Front Behav Neurosci. 2018 Nov 30;12:288 [PMID: 30555308]
  29. Magn Reson Med. 2010 May;63(5):1144-53 [PMID: 20432285]
  30. Nature. 2012 Aug 9;488(7410):218-21 [PMID: 22722841]
  31. Cortex. 1993 Mar;29(1):115-34 [PMID: 8472549]
  32. Neuroimage. 2012 Jul 16;61(4):1277-86 [PMID: 22484411]
  33. Nature. 2004 Sep 2;431(7004):71-6 [PMID: 15343334]
  34. Proc Natl Acad Sci U S A. 2012 Dec 11;109(50):20762-7 [PMID: 23184998]
  35. Br J Educ Psychol. 1992 Nov;62 ( Pt 3):375-90 [PMID: 1467257]
  36. Hum Brain Mapp. 2005 May;25(1):92-104 [PMID: 15846818]
  37. Neuroimage. 2011 Feb 1;54(3):2426-36 [PMID: 20934519]
  38. Brain. 2006 Mar;129(Pt 3):564-83 [PMID: 16399806]
  39. Front Hum Neurosci. 2018 Dec 06;12:490 [PMID: 30574080]
  40. Sci Stud Read. 2013 Jan 1;17(1):5-21 [PMID: 24744605]
  41. Neuroimage. 1997 Oct;6(3):218-29 [PMID: 9344826]
  42. Front Hum Neurosci. 2018 Feb 13;12:30 [PMID: 29487511]
  43. Proc Natl Acad Sci U S A. 2013 Jan 15;110(3):1119-23 [PMID: 23277555]
  44. PLoS One. 2016 Dec 16;11(12):e0168414 [PMID: 27992505]
  45. Neuropsychologia. 2013 Jan;51(1):67-78 [PMID: 23178227]
  46. Res Dev Disabil. 2018 Mar;74:146-159 [PMID: 29413429]
  47. Nat Commun. 2016 Nov 03;7:13217 [PMID: 27808095]
  48. Dev Neuropsychol. 2006;29(1):175-96 [PMID: 16390293]
  49. Br J Educ Psychol. 2002 Mar;72(Pt 1):119-33 [PMID: 11916468]
  50. Neuropsychologia. 2006;44(14):2937-49 [PMID: 16920164]
  51. Cognition. 2000 Mar 14;74(3):B27-32 [PMID: 10640574]
  52. Proc Natl Acad Sci U S A. 2016 May 3;113(18):4909-17 [PMID: 27071124]
  53. Brain. 1997 Sep;120 ( Pt 9):1587-602 [PMID: 9313642]
  54. Hum Mov Sci. 2015 Aug;42:161-82 [PMID: 26037277]
  55. Dev Neuropsychol. 2006;29(1):43-60 [PMID: 16390288]
  56. Psychol Sci. 2009 Oct;20(10):1245-53 [PMID: 19765238]
  57. Neuron. 2013 Jul 10;79(1):180-90 [PMID: 23746630]
  58. J Learn Disabil. 2020 Mar/Apr;53(2):109-119 [PMID: 31526093]
  59. Neuropsychologia. 2009 Mar;47(4):1193-9 [PMID: 19056407]
  60. J Exp Psychol Learn Mem Cogn. 2019 Apr;45(4):724-731 [PMID: 29999402]
  61. Arch Neurol. 1992 Mar;49(3):246-51 [PMID: 1536626]
  62. Hum Brain Mapp. 2005 May;25(1):83-91 [PMID: 15846817]
  63. Neuropsychologia. 2012 Jul;50(9):2224-32 [PMID: 22698991]
  64. Hum Brain Mapp. 2013 Jul;34(7):1670-84 [PMID: 22378588]
  65. Nat Rev Neurosci. 2001 Jun;2(6):417-24 [PMID: 11389475]
  66. Trends Cogn Sci. 2000 Jun;4(6):215-222 [PMID: 10827444]
  67. Elife. 2020 Oct 29;9: [PMID: 33118931]
  68. Ann Dyslexia. 2000 Jan;50(1):239-59 [PMID: 20563787]
  69. J Cogn Neurosci. 2008 May;20(5):802-15 [PMID: 18201124]
  70. Cogn Neuropsychol. 2007 Jun;24(4):431-50 [PMID: 18416500]
  71. Brain. 2016 Feb;139(Pt 2):588-604 [PMID: 26685156]
  72. Biol Psychiatry. 2014 Sep 1;76(5):397-404 [PMID: 24124929]
  73. Neuroimage. 2006 Dec;33(4):1218-26 [PMID: 17035046]
  74. Neuroimage. 2003 Aug;19(4):1492-500 [PMID: 12948705]
  75. Ann N Y Acad Sci. 2008 Dec;1145:212-21 [PMID: 19076399]
  76. Neuroimage. 2017 Feb 1;146:301-311 [PMID: 27890803]
  77. J Commun Disord. 2001 Nov-Dec;34(6):479-92 [PMID: 11725860]
  78. J Exp Child Psychol. 2011 Nov;110(3):422-33 [PMID: 21641000]
  79. Front Hum Neurosci. 2014 Mar 19;8:155 [PMID: 24678293]
  80. Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15855-60 [PMID: 9861060]
  81. Nat Neurosci. 2015 May;18(5):744-51 [PMID: 25849989]
  82. Lancet. 2004 May 1;363(9419):1451-60 [PMID: 15121410]
  83. Ment Retard Dev Disabil Res Rev. 2000;6(3):207-13 [PMID: 10982498]
  84. Hum Brain Mapp. 2020 Jul;41(10):2642-2655 [PMID: 32090433]
  85. Cortex. 2013 Nov-Dec;49(10):2772-87 [PMID: 23831432]
  86. Front Psychol. 2016 Mar 18;7:324 [PMID: 27047403]
  87. Acta Psychol (Amst). 2005 May;119(1):67-79 [PMID: 15823243]
  88. Dev Psychopathol. 2008 Fall;20(4):1329-49 [PMID: 18838044]
  89. Behav Neurol. 2007;18(2):99-114 [PMID: 17538196]

MeSH Term

Brain
Brain Mapping
Child
China
Dyslexia
Handwriting
Humans
Magnetic Resonance Imaging
Reading

Word Cloud

Created with Highcharts 10.0.0handwritingreadingbraindeficitsdyslexiafunctionaltaskschildrenactivationprocessingmotordevelopmentalDDdyslexicregionscontrolneuralChinesecontrolsexhibitedreducedsensory-motorincludingsupplementaryareagyrusprecuneusrightleftdyslexicsvisual-orthographicconnectivitycognitiveAbundantbehavioralstudiesdemonstratedhighcomorbiditydifficultiesneurologicalconditioncharacterizedunexpectedlylowabilitydespiteadequatenonverbalintelligencetypicalschoolingcorrelatesremainlargelyunknownhoweverwellextentsharecommonbasespresentworkusedmagneticresonanceimagingexamineactivityn = 18age-matchedn = 23Comparedsupportingpostcentralvisual-orthographybilateralcuneusAmongalsoshowedtrendMoreoverincreasedfoundinferiorfrontalanteriorcingulatecortexmayreflecteffortsexecutivecompensateimpairmentsFinallyaberrantamongareasprocessesTogetherfindingssuggestassociatedabnormalitiesmultipleimplicatedexecutionprovidingimportantimplicationsdiagnosistreatmentbasisfMRI

Similar Articles

Cited By