Home LiteratureArticle Details
PMID: 20176116 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Normal variation in fronto-occipital circuitry and cerebellar structure with an autism-associated polymorphism of CNTNAP2.

NeuroImage ·Vol. 53 ·No. 3 ·2010-11-15 ·Pages 1030-42

Tan GC, Doke TF, Ashburner J, Wood NW, Frackowiak RS

Abstract

Recent genetic studies have implicated a number of candidate genes in the pathogenesis of Autism Spectrum Disorder (ASD). Polymorphisms of CNTNAP2 (contactin-associated like protein-2), a member of the neurexin family, have already been implicated as a susceptibility gene for autism by at least 3 separate studies. We investigated variation in white and grey matter morphology using structural MRI and diffusion tensor imaging. We compared volumetric differences in white and grey matter and fractional anisotropy values in control subjects characterised by genotype at rs7794745, a single nucleotide polymorphism in CNTNAP2. Homozygotes for the risk allele showed significant reductions in grey and white matter volume and fractional anisotropy in several regions that have already been implicated in ASD, including the cerebellum, fusiform gyrus, occipital and frontal cortices. Male homozygotes for the risk alleles showed greater reductions in grey matter in the right frontal pole and in FA in the right rostral fronto-occipital fasciculus compared to their female counterparts who showed greater reductions in FA of the anterior thalamic radiation. Thus a risk allele for autism results in significant cerebral morphological variation, despite the absence of overt symptoms or behavioural abnormalities. The results are consistent with accumulating evidence of CNTNAP2's function in neuronal development. The finding suggests the possibility that the heterogeneous manifestations of ASD can be aetiologically characterised into distinct subtypes through genetic-morphological analysis.

MeSH Terms
Anisotropy Cerebellum/pathology Child Child Development Disorders, Pervasive/genetics,physiopathology Endophenotypes Female Frontal Lobe/pathology Genetic Predisposition to Disease Genotype Humans Image Interpretation, Computer-Assisted Magnetic Resonance Imaging/methods Male Membrane Proteins/genetics Nerve Tissue Proteins/genetics Neural Pathways/pathology Occipital Lobe/pathology Polymerase Chain Reaction Polymorphism, Restriction Fragment Length Polymorphism, Single Nucleotide
Chemicals
CNTNAP2 protein, human Membrane Proteins Nerve Tissue Proteins
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Tan Geoffrey C Y
Wellcome Trust Centre for Neuroimaging, Institute of Neurology, University College London, UK. [email protected]
Doke Thomas F
Ashburner John
Wood Nicholas W
Frackowiak Richard S J
References (81)
81 references, click to expand
  1. Primer3 on the WWW for general users and for biologist programmers.
    Methods Mol Biol. 2000;132:365-86 PMID: 10547847
  2. NEBcutter: A program to cleave DNA with restriction enzymes.
    Nucleic Acids Res. 2003 Jul 1;31(13):3688-91 PMID: 12824395
  3. Superior temporal sulcus anatomical abnormalities in childhood autism: a voxel-based morphometry MRI study.
    Neuroimage. 2004 Sep;23(1):364-9 PMID: 15325384
  4. A systems neuroscience approach to autism: biological, cognitive, and clinical perspectives.
    Ment Retard Dev Disabil Res Rev. 2003;9(3):205-15 PMID: 12953300
  5. Association between the HOXA1 A218G polymorphism and increased head circumference in patients with autism.
    Biol Psychiatry. 2004 Feb 15;55(4):413-9 PMID: 14960295
  6. Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders.
    J Autism Dev Disord. 1994 Oct;24(5):659-85 PMID: 7814313
  7. Bayesian decoding of brain images.
    Neuroimage. 2008 Jan 1;39(1):181-205 PMID: 17919928
  8. Face and emotion recognition deficits in Turner syndrome: a possible role for X-linked genes in amygdala development.
    Neuropsychology. 2003 Jan;17(1):39-49 PMID: 12597072
  9. White matter fiber tracts of the human brain: three-dimensional mapping at microscopic resolution, topography and intersubject variability.
    Neuroimage. 2006 Feb 15;29(4):1092-105 PMID: 16236527
  10. The control of neuron number.
    Annu Rev Neurosci. 1988;11:423-53 PMID: 3284447
  11. Molecular cytogenetic analysis and resequencing of contactin associated protein-like 2 in autism spectrum disorders.
    Am J Hum Genet. 2008 Jan;82(1):165-73 PMID: 18179895
  12. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10.
    J Clin Psychiatry. 1998;59 Suppl 20:22-33;quiz 34-57 PMID: 9881538
  13. A functional genetic link between distinct developmental language disorders.
    N Engl J Med. 2008 Nov 27;359(22):2337-45 PMID: 18987363
  14. Automatic detection of preclinical neurodegeneration: presymptomatic Huntington disease.
    Neurology. 2009 Feb 3;72(5):426-31 PMID: 19188573
  15. Juxtaparanodal clustering of Shaker-like K+ channels in myelinated axons depends on Caspr2 and TAG-1.
    J Cell Biol. 2003 Sep 15;162(6):1149-60 PMID: 12963709
  16. Voxel-based morphometry--the methods.
    Neuroimage. 2000 Jun;11(6 Pt 1):805-21 PMID: 10860804
  17. The cerebellum and cognition.
    Eur J Paediatr Neurol. 2007 Jul;11(4):232-4 PMID: 17400009
  18. A voxel-based morphometry study of gray matter in parents of children with autism.
    Neuroreport. 2006 Aug 21;17(12):1289-92 PMID: 16951571
  19. Interpreting scan data acquired from multiple scanners: a study with Alzheimer's disease.
    Neuroimage. 2008 Feb 1;39(3):1180-5 PMID: 18032068
  20. CNTNAP2 gene dosage variation is associated with schizophrenia and epilepsy.
    Mol Psychiatry. 2008 Mar;13(3):261-6 PMID: 17646849
  21. A clinicopathological study of autism.
    Brain. 1998 May;121 ( Pt 5):889-905 PMID: 9619192
  22. Neurons in the fusiform gyrus are fewer and smaller in autism.
    Brain. 2008 Apr;131(Pt 4):987-99 PMID: 18332073
  23. Endophenotype approach to developmental psychopathology: implications for autism research.
    Behav Genet. 2007 Jan;37(1):51-60 PMID: 16988798
  24. Development of rostral prefrontal cortex and cognitive and behavioural disorders.
    Dev Med Child Neurol. 2008 Mar;50(3):168-81 PMID: 18190537
  25. A common genetic variant in the neurexin superfamily member CNTNAP2 increases familial risk of autism.
    Am J Hum Genet. 2008 Jan;82(1):160-4 PMID: 18179894
  26. Evidence for a language quantitative trait locus on chromosome 7q in multiplex autism families.
    Am J Hum Genet. 2002 Jan;70(1):60-71 PMID: 11741194
  27. Contact in the genetics of autism and schizophrenia.
    Trends Neurosci. 2009 Feb;32(2):69-72 PMID: 19135727
  28. Spatial pattern analysis of functional brain images using partial least squares.
    Neuroimage. 1996 Jun;3(3 Pt 1):143-57 PMID: 9345485
  29. MR diffusion tensor spectroscopy and imaging.
    Biophys J. 1994 Jan;66(1):259-67 PMID: 8130344
  30. Fiber tract-based atlas of human white matter anatomy.
    Radiology. 2004 Jan;230(1):77-87 PMID: 14645885
  31. The Arg451Cys-neuroligin-3 mutation associated with autism reveals a defect in protein processing.
    J Neurosci. 2004 May 19;24(20):4889-93 PMID: 15152050
  32. The neuroanatomy of autism: a voxel-based whole brain analysis of structural scans.
    Neuroreport. 1999 Jun 3;10(8):1647-51 PMID: 10501551
  33. Reduction in white matter connectivity, revealed by diffusion tensor imaging, may account for age-related changes in face perception.
    J Cogn Neurosci. 2008 Feb;20(2):268-84 PMID: 18275334
  34. Imprinting, the X-chromosome, and the male brain: explaining sex differences in the liability to autism.
    Pediatr Res. 2000 Jan;47(1):9-16 PMID: 10625077
  35. 'Theory of mind' in the brain. Evidence from a PET scan study of Asperger syndrome.
    Neuroreport. 1996 Dec 20;8(1):197-201 PMID: 9051780
  36. Why the frontal cortex in autism might be talking only to itself: local over-connectivity but long-distance disconnection.
    Curr Opin Neurobiol. 2005 Apr;15(2):225-30 PMID: 15831407
  37. A voxel-based investigation of brain structure in male adolescents with autistic spectrum disorder.
    Neuroimage. 2004 Jun;22(2):619-25 PMID: 15193590
  38. Recessive symptomatic focal epilepsy and mutant contactin-associated protein-like 2.
    N Engl J Med. 2006 Mar 30;354(13):1370-7 PMID: 16571880
  39. Mind blindness and the brain in autism.
    Neuron. 2001 Dec 20;32(6):969-79 PMID: 11754830
  40. Cerebral asymmetry and the effects of sex and handedness on brain structure: a voxel-based morphometric analysis of 465 normal adult human brains.
    Neuroimage. 2001 Sep;14(3):685-700 PMID: 11506541
  41. A 12Mb deletion at 7q33-q35 associated with autism spectrum disorders and primary amenorrhea.
    Eur J Med Genet. 2008 Nov-Dec;51(6):631-8 PMID: 18675947
  42. The UCSC Genome Browser Database: 2008 update.
    Nucleic Acids Res. 2008 Jan;36(Database issue):D773-9 PMID: 18086701
  43. Dosage-sensitive X-linked locus influences the development of amygdala and orbitofrontal cortex, and fear recognition in humans.
    Brain. 2003 Nov;126(Pt 11):2431-46 PMID: 12958079
  44. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data.
    Neuroimage. 2006 Jul 15;31(4):1487-505 PMID: 16624579
  45. Characterization and propagation of uncertainty in diffusion-weighted MR imaging.
    Magn Reson Med. 2003 Nov;50(5):1077-88 PMID: 14587019
  46. The fusiform face area: a module in human extrastriate cortex specialized for face perception.
    J Neurosci. 1997 Jun 1;17(11):4302-11 PMID: 9151747
  47. Imaging data in autism: from structure to malfunction.
    Semin Pediatr Neurol. 2004 Sep;11(3):205-13 PMID: 15575415
  48. Genome-wide analyses of human perisylvian cerebral cortical patterning.
    Proc Natl Acad Sci U S A. 2007 Nov 6;104(45):17849-54 PMID: 17978184
  49. Social interest and the development of cortical face specialization: what autism teaches us about face processing.
    Dev Psychobiol. 2002 Apr;40(3):213-25 PMID: 11891634
  50. The primate cortico-cerebellar system: anatomy and function.
    Nat Rev Neurosci. 2006 Jul;7(7):511-22 PMID: 16791141
  51. Towards a neuroanatomy of autism: a systematic review and meta-analysis of structural magnetic resonance imaging studies.
    Eur Psychiatry. 2008 Jun;23(4):289-99 PMID: 17765485
  52. Autism spectrum disorder in fragile X syndrome: a longitudinal evaluation.
    Am J Med Genet A. 2009 Jun;149A(6):1125-37 PMID: 19441123
  53. Brief report: epidemiology of autism.
    J Autism Dev Disord. 1996 Apr;26(2):165-7 PMID: 8744478
  54. A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function.
    Cell. 1996 Dec 13;87(6):1059-68 PMID: 8978610
  55. Mechanisms and roles of axon-Schwann cell interactions.
    J Neurosci. 2004 Oct 20;24(42):9250-60 PMID: 15496660
  56. Advances in functional and structural MR image analysis and implementation as FSL.
    Neuroimage. 2004;23 Suppl 1:S208-19 PMID: 15501092
  57. A fast diffeomorphic image registration algorithm.
    Neuroimage. 2007 Oct 15;38(1):95-113 PMID: 17761438
  58. Nonstationary cluster-size inference with random field and permutation methods.
    Neuroimage. 2004 Jun;22(2):676-87 PMID: 15193596
  59. Virtual in vivo interactive dissection of white matter fasciculi in the human brain.
    Neuroimage. 2002 Sep;17(1):77-94 PMID: 12482069
  60. Diffusion tensor imaging of frontal lobe in autism spectrum disorder.
    Cereb Cortex. 2008 Nov;18(11):2659-65 PMID: 18359780
  61. The role of the fusiform face area in social cognition: implications for the pathobiology of autism.
    Philos Trans R Soc Lond B Biol Sci. 2003 Feb 28;358(1430):415-27 PMID: 12639338
  62. Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism.
    Nat Genet. 2003 May;34(1):27-9 PMID: 12669065
  63. Regional gray matter volumetric changes in autism associated with social and repetitive behavior symptoms.
    BMC Psychiatry. 2006 Dec 13;6:56 PMID: 17166273
  64. Genetic advances in autism: heterogeneity and convergence on shared pathways.
    Curr Opin Genet Dev. 2009 Jun;19(3):271-8 PMID: 19477629
  65. Synapse elimination and plasticity in developing human cerebral cortex.
    Am J Ment Defic. 1984 Mar;88(5):488-96 PMID: 6731486
  66. Voxel-based morphometry study on brain structure in children with high-functioning autism.
    Neuroreport. 2008 Jun 11;19(9):921-5 PMID: 18520994
  67. Psychological markers in the detection of autism in infancy in a large population.
    Br J Psychiatry. 1996 Feb;168(2):158-63 PMID: 8837904
  68. The endophenotype concept in psychiatry: etymology and strategic intentions.
    Am J Psychiatry. 2003 Apr;160(4):636-45 PMID: 12668349
  69. Linkage, association, and gene-expression analyses identify CNTNAP2 as an autism-susceptibility gene.
    Am J Hum Genet. 2008 Jan;82(1):150-9 PMID: 18179893
  70. Bayesian analysis of neuroimaging data in FSL.
    Neuroimage. 2009 Mar;45(1 Suppl):S173-86 PMID: 19059349
  71. Histoanatomic observations of the brain in early infantile autism.
    Neurology. 1985 Jun;35(6):866-74 PMID: 4000488
  72. Unusual brain growth patterns in early life in patients with autistic disorder: an MRI study.
    Neurology. 2001 Jul 24;57(2):245-54 PMID: 11468308
  73. The autism-spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians.
    J Autism Dev Disord. 2001 Feb;31(1):5-17 PMID: 11439754
  74. Unified segmentation.
    Neuroimage. 2005 Jul 1;26(3):839-51 PMID: 15955494
  75. Strong association of de novo copy number mutations with autism.
    Science. 2007 Apr 20;316(5823):445-9 PMID: 17363630
  76. Autism as a strongly genetic disorder: evidence from a British twin study.
    Psychol Med. 1995 Jan;25(1):63-77 PMID: 7792363
  77. Optimisation of the 3D MDEFT sequence for anatomical brain imaging: technical implications at 1.5 and 3 T.
    Neuroimage. 2004 Feb;21(2):757-67 PMID: 14980579
  78. Caspr2, a new member of the neurexin superfamily, is localized at the juxtaparanodes of myelinated axons and associates with K+ channels.
    Neuron. 1999 Dec;24(4):1037-47 PMID: 10624965
  79. Genetics of brain structure and intelligence.
    Annu Rev Neurosci. 2005;28:1-23 PMID: 15651931
  80. Altered cerebellar feedback projections in Asperger syndrome.
    Neuroimage. 2008 Jul 15;41(4):1184-91 PMID: 18495494
  81. Microstructural organization of the cingulum tract and the level of default mode functional connectivity.
    J Neurosci. 2008 Oct 22;28(43):10844-51 PMID: 18945892
Article Info
Journal
NeuroImage
Abbr.
Neuroimage
ISSN
1095-9572
Published
2010-11-15
Epub
2010-00-20
Pages
1030-42
Language
English
Region
United States
NLM ID
9215515
PMCID
PMC2941042
Subset
IM
Grants
Wellcome Trust · 075696/Z/4/Z · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]