Abnormal age-related cortical folding and neurite morphology in children with developmental dyslexia.

Eduardo Caverzasi, Maria Luisa Mandelli, Fumiko Hoeft, Christa Watson, Marita Meyer, Isabel E Allen, Nico Papinutto, Cheng Wang, Claudia A M Gandini Wheeler-Kingshott, Elysa J Marco, Pratik Mukherjee, Zachary A Miller, Bruce L Miller, Robert Hendren, Kevin A Shapiro, Maria Luisa Gorno-Tempini
Author Information
  1. Eduardo Caverzasi: Dyslexia Center, University of California, San Francisco, San Francisco, CA, USA; Department of Neurology, University of California, San Francisco, San Francisco, CA, USA; Biomedical Sciences PhD, Department of Brain and Behavioral Sciences, University of Pavia, Pavia, Italy. Electronic address: eduardo.caverzasi@ucsf.edu.
  2. Maria Luisa Mandelli: Dyslexia Center, University of California, San Francisco, San Francisco, CA, USA; Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA.
  3. Fumiko Hoeft: Dyslexia Center, University of California, San Francisco, San Francisco, CA, USA; Department of Psychiatry and Weill Institute for Neurosciences, University of California, San Francisco, CA, USA.
  4. Christa Watson: Dyslexia Center, University of California, San Francisco, San Francisco, CA, USA; Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA.
  5. Marita Meyer: Dyslexia Center, University of California, San Francisco, San Francisco, CA, USA.
  6. Isabel E Allen: Department of Epidemiology and Biostatistics, University of California, San Francisco, San Francisco, CA, USA.
  7. Nico Papinutto: Department of Neurology, University of California, San Francisco, San Francisco, CA, USA.
  8. Cheng Wang: Dyslexia Center, University of California, San Francisco, San Francisco, CA, USA; Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA; Department of Psychiatry and Weill Institute for Neurosciences, University of California, San Francisco, CA, USA.
  9. Claudia A M Gandini Wheeler-Kingshott: Queen Square MS Centre, Department of Neuroinflammation, UCL Institute of Neurology, Russel Square House, London, United Kingdom; Department of Brain and Behavioral Sciences, University of Pavia, Pavia, Italy; Brain MRI 3T Mondino Research Center, C. Mondino National Neurological Institute, Pavia, Italy.
  10. Elysa J Marco: Department of Neurology, University of California, San Francisco, San Francisco, CA, USA; Department of Psychiatry and Weill Institute for Neurosciences, University of California, San Francisco, CA, USA; Department of Pediatrics, University of California, San Francisco, San Francisco, CA, USA.
  11. Pratik Mukherjee: Neuroradiology Section, Department of Radiology and Biomedical Imaging, University of California, San Francisco, USA.
  12. Zachary A Miller: Dyslexia Center, University of California, San Francisco, San Francisco, CA, USA; Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA.
  13. Bruce L Miller: Department of Neurology, University of California, San Francisco, San Francisco, CA, USA; Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA.
  14. Robert Hendren: Dyslexia Center, University of California, San Francisco, San Francisco, CA, USA; Department of Psychiatry and Weill Institute for Neurosciences, University of California, San Francisco, CA, USA.
  15. Kevin A Shapiro: Dyslexia Center, University of California, San Francisco, San Francisco, CA, USA; Department of Neurology, University of California, San Francisco, San Francisco, CA, USA.
  16. Maria Luisa Gorno-Tempini: Dyslexia Center, University of California, San Francisco, San Francisco, CA, USA; Memory and Aging Center, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA.

Abstract

There is increasing recognition of a relationship between regional variability in cerebral gyrification and neurodevelopment. Recent work in morphometric MRI has shown that the local gyrification index (lGI), a measure of regional brain folding, may be altered in certain neurodevelopmental disorders. Other studies report that the lGI generally decreases with age in adolescence and young adulthood; however, little is known about how these age-dependent differences in brain maturation occur in atypical neurodevelopment and mechanisms underlying gyrification, such as synaptic pruning. Organization and optimization of dendrites and axons connections across the brain might be driving gyrification and folding processes. In this study, we first assessed lGI differences in the left hemisphere in a cohort of 39 children with developmental dyslexia (DD) between the ages of 7 and 15 years in comparison to 56 typically developing controls (TDC). To better understand the microstructural basis of these changes, we next explored the relationship between lGI differences and cortical thickness and neurite morphology by applying neurite orientation dispersion and density imaging (NODDI). We identified significant differences in lGI between children with DD and TDC in left lateral temporal and middle frontal regions. Further, DD failed to show the expected age-related decreases in lGI in the same regions. Age-related differences in lGI in DD were not explained by differences in cortical thickness, but did correlate with NODDI neurite density and orientation dispersion index. Our findings suggest that gyrification changes in DD are related to abnormal neurite morphology, and are possibly an expression of differences in synaptic pruning.

References

  1. Neuropsychologia. 2016 Jan 29;81:68-78 [PMID: 26679527]
  2. Biol Cybern. 1995 Nov;73(6):529-45 [PMID: 8527499]
  3. Curr Opin Neurobiol. 2013 Feb;23(1):37-42 [PMID: 23040541]
  4. Brain Cogn. 2010 Feb;72(1):36-45 [PMID: 19942335]
  5. Hum Brain Mapp. 2017 Feb;38(2):900-908 [PMID: 27712002]
  6. Nat Rev Neurosci. 2008 May;9(5):357-69 [PMID: 18425090]
  7. Neuroimage. 2006 Jul 1;31(3):968-80 [PMID: 16530430]
  8. PLoS One. 2014 Jan 15;9(1):e84914 [PMID: 24454765]
  9. Ann Neurol. 1985 Aug;18(2):222-33 [PMID: 4037763]
  10. Psychiatry Res. 2014 Feb 28;221(2):169-71 [PMID: 24377834]
  11. Neuroimage Clin. 2015 Apr 30;8:253-60 [PMID: 26106549]
  12. Ann Neurol. 1977 Jan;1(1):86-93 [PMID: 560818]
  13. Brain. 2005 Oct;128(Pt 10):2453-61 [PMID: 15975942]
  14. Ann Clin Transl Neurol. 2017 Aug 15;4(9):663-679 [PMID: 28904988]
  15. Dev Cogn Neurosci. 2015 Aug;14:8-15 [PMID: 26048528]
  16. Dev Neuropsychol. 2010;35(5):475-93 [PMID: 20721770]
  17. Neuroimage. 2016 Jun;133:207-223 [PMID: 26826512]
  18. Trends Neurosci. 2013 May;36(5):275-84 [PMID: 23415112]
  19. Hum Brain Mapp. 1999;8(4):272-84 [PMID: 10619420]
  20. Cereb Cortex. 2016 Mar;26(3):1138-1148 [PMID: 25576531]
  21. Dev Psychopathol. 2008 Fall;20(4):1161-75 [PMID: 18838036]
  22. Proc Natl Acad Sci U S A. 2012 Feb 7;109(6):2156-61 [PMID: 22308323]
  23. Cereb Cortex. 2018 Mar 1;28(3):963-973 [PMID: 28108497]
  24. Neuroimage. 2003 Oct;20(2):870-88 [PMID: 14568458]
  25. Cereb Cortex. 2016 Jul;26(7):3297-309 [PMID: 27130663]
  26. Anat Embryol (Berl). 1988;179(2):173-9 [PMID: 3232854]
  27. Neuroimage. 1999 Feb;9(2):179-94 [PMID: 9931268]
  28. IEEE Trans Med Imaging. 2008 Feb;27(2):161-70 [PMID: 18334438]
  29. J Vis Exp. 2012 Jan 02;(59):e3417 [PMID: 22230945]
  30. Neuroimage. 2004;23 Suppl 1:S208-19 [PMID: 15501092]
  31. Nature. 1997 Jan 23;385(6614):313-8 [PMID: 9002514]
  32. Front Neuroanat. 2016 Jan 26;9:169 [PMID: 26858611]
  33. Annu Rev Neurosci. 2007;30:475-503 [PMID: 17600524]
  34. Hum Brain Mapp. 2013 Nov;34(11):3055-65 [PMID: 22711189]
  35. Neuroimage. 2012 Jul 16;61(4):1000-16 [PMID: 22484410]
  36. Ann Dyslexia. 1985 Jan;35(1):19-33 [PMID: 24243407]
  37. J Neuroimaging. 2016 Sep;26(5):494-8 [PMID: 27214558]
  38. Cereb Cortex. 2001 Jun;11(6):558-71 [PMID: 11375917]
  39. Ann N Y Acad Sci. 2010 Mar;1191:62-88 [PMID: 20392276]
  40. PLoS One. 2012;7(8):e43122 [PMID: 22916214]
  41. Neuroimage. 1999 Feb;9(2):195-207 [PMID: 9931269]

Grants

  1. P50 AG023501/NIA NIH HHS
  2. U01 AG052943/NIA NIH HHS
  3. P01 AG019724/NIA NIH HHS
  4. R01 NS050915/NINDS NIH HHS
  5. K24 DC015544/NIDCD NIH HHS
  6. R01 HD086168/NICHD NIH HHS
  7. R01 HD078351/NICHD NIH HHS

MeSH Term

Adolescent
Age Factors
Brain Mapping
Cerebral Cortex
Child
Dyslexia
Female
Humans
Image Processing, Computer-Assisted
Magnetic Resonance Imaging
Male
Neurites

Word Cloud

Created with Highcharts 10.0.0lGIdifferencesgyrificationDDneuritebrainfoldingchildrencorticalmorphologyrelationshipregionalneurodevelopmentindexdecreasessynapticpruningleftdevelopmentaldyslexiaTDCchangesthicknessorientationdispersiondensityNODDIregionsage-relatedincreasingrecognitionvariabilitycerebralRecentworkmorphometricMRIshownlocalmeasuremayalteredcertainneurodevelopmentaldisordersstudiesreportgenerallyageadolescenceyoungadulthoodhoweverlittleknownage-dependentmaturationoccuratypicalmechanismsunderlyingOrganizationoptimizationdendritesaxonsconnectionsacrossmightdrivingprocessesstudyfirstassessedhemispherecohort39ages715 yearscomparison56typicallydevelopingcontrolsbetterunderstandmicrostructuralbasisnextexploredapplyingimagingidentifiedsignificantlateraltemporalmiddlefrontalfailedshowexpectedAge-relatedexplainedcorrelatefindingssuggestrelatedabnormalpossiblyexpressionAbnormal

Similar Articles

Cited By