Psychiatry Research: Neuroimaging
Volume 174, Issue 2 , Pages 138-145 , 30 November 2009

A voxel-based morphometry comparison of regional gray matter between fragile X syndrome and autism

  • Lisa B. Wilson

      Affiliations

    • Department of Psychiatry, University of Colorado at Denver, Denver, CO, 80045, USA
    • ,
  • Jason R. Tregellas

      Affiliations

    • Department of Psychiatry, University of Colorado at Denver, Denver, CO, 80045, USA
    • ,
  • Randi J. Hagerman

      Affiliations

    • Department of Pediatrics and M.I.N.D. Institute, University of California at Davis, Sacramento, CA 95817, USA
    • ,
  • Sally J. Rogers

      Affiliations

    • Department of Psychiatry and M.I.N.D. Institute, University of California at Davis, Sacramento, CA 95817, USA
    • ,
  • Donald C. Rojas

      Affiliations

    • Department of Psychiatry, University of Colorado at Denver, Denver, CO, 80045, USA
    • Corresponding Author InformationCorresponding author. Department of Psychiatry, University of Colorado Denver, Bldg. 500, N2224G, Denver, CO 80045, USA. Tel.: +1 303 724 4994; fax: +1 303 724 3594.

Received 12 May 2008 ,Revised 2 March 2009 ,Accepted 27 April 2009.

References 

  1. Abell F, Krams M, Ashburner J, Passingham R, Friston K, Frackowiak R, et al. The neuroanatomy of autism: a voxel-based whole brain analysis of structural scans. Neuroreport. 1999;10:1647–1651
  2. American Psychiatric Association . Diagnostic and Statistical Manual of Mental Disorders IV. Washington, DC: APA; 1994;
  3. Aylward EH, Minshew NJ, Field K, Sparks BF, Singh N. Effects of age on brain volume and head circumference in autism. Neurology. 2002;59:175–183
  4. Bailey A, Le Couteur A, Gottesman I, Bolton P, Simonoff E, Yuzda E, et al. Autism as a strongly genetic disorder: evidence from a British twin study. Psychological Medicine. 1995;25:63–77
  5. Bailey DB, Mesibov GB, Hatton DD, Clark RD, Roberts JE, Mayhew L. Autistic behavior in young boys with fragile X syndrome. Journal of Autism and Developmental Disorders. 1998;28:499–508
  6. Barnea-Goraly N, Eliez S, Hedeus M, Menon V, White CD, Moseley M, et al. White matter tract alterations in fragile X syndrome: preliminary evidence from diffusion tensor imaging. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics. 2003;118:81–88
  7. Baumgardner TL, Reiss AL, Freund LS, Abrams MT. Specification of the neurobehavioral phenotype in males with fragile X syndrome. Pediatrics. 1995;95:744–752
  8. Boddaert N, Chabane N, Gervais H, Good CD, Bourgeois M, Plumet MH, et al. Superior temporal sulcus anatomical abnormalities in childhood autism: a voxel-based morphometry MRI study. Neuroimage. 2004;23:364–369
  9. Brieber S, Neufang S, Bruning N, Kamp-Becker I, Remschmidt H, Herpertz-Dahlmann B, et al. Structural brain abnormalities in adolescents with autism spectrum disorder and patients with attention deficit/hyperactivity disorder. Journal of Child Psychology and Psychiatry and Allied Disciplines. 2007;48:1251–1258
  10. Brown WT, Friedman E, Jenkins EC, Brooks J, Wisniewski K, Raguthu S, et al. Association of fragile X syndrome with autism. Lancet. 1982;1:100
  11. Brown WT, Jenkins EC, Friedman E, Brooks J, Wisniewski K, Raguthu S, et al. Autism is associated with the fragile-X syndrome. Journal of Autism and Developmental Disorders. 1982;12:303–308
  12. Centers for Disease Control and Prevention . Prevalence of Autism Spectrum Disorders — Autism and Developmental Disabilities Monitoring Network, 14 Sites, United States, 2002. Surveillance Summaries, February 9. MMWR; 2007;56 (No. 12–28)
  13. Chakos MH, Lieberman JA, Bilder RM, Borenstein M, Lerner G, Bogerts B, et al. Increase in caudate nuclei volumes of first-episode schizophrenic patients taking antipsychotic drugs. American Journal of Psychiatry. 1994;151:1430–1436
  14. Chudasama Y, Robbins TW. Functions of frontostriatal systems in cognition: comparative neuropsychopharmacological studies in rats, monkeys and humans. Biological Psychology. 2006;73:19–38
  15. Cornish K, Swainson R, Cunnington R, Wilding J, Morris P, Jackson G. Do women with fragile X syndrome have problems in switching attention: preliminary findings from ERP and fMRI. Brain and Cognition. 2004;54:235–239
  16. Courchesne E. Brainstem, cerebellar and limbic neuroanatomical abnormalities in autism. Current Opinion in Neurobiology. 1997;7:269–278
  17. Courchesne E, Yeung-Courchesne R, Press GA, Hesselink JR, Jernigan TL. Hypoplasia of cerebellar vermal lobules VI and VII in autism. New England Journal of Medicine. 1988;318:1349–1354
  18. Courchesne E, Saitoh O, Yeung-Courchesne R, Press GA, Lincoln AJ, Haas RH, et al. Abnormality of cerebellar vermian lobules VI and VII in patients with infantile autism: identification of hypoplastic and hyperplastic subgroups with MR imaging. American Journal of Roentgenology. 1994;162:123–130
  19. Courchesne E, Karns CM, Davis HR, Ziccardi R, Carper RA, Tigue ZD, et al. Unusual brain growth patterns in early life in patients with autistic disorder: an MRI study. Neurology. 2001;57:245–254
  20. Courchesne E, Carper R, Akshoomoff N. Evidence of brain overgrowth in the first year of life in autism. Journal of the American Medical Association. 2003;290:337–344
  21. Egaas B, Courchesne E, Saitoh O. Reduced size of corpus callosum in autism. Archives of Neurology. 1995;52:794–801
  22. Eliez S, Blasey CM, Freund LS, Hastie T, Reiss AL. Brain anatomy, gender and IQ in children and adolescents with fragile X syndrome. Brain. 2001;124:1610–1618
  23. Frings M, Dimitrova A, Schorn CF, Elles HG, Hein-Kropp C, Gizewski ER, et al. Cerebellar involvement in verb generation: an fMRI study. Neuroscience Letters. 2006;409:19–23
  24. Gaffney GR, Tsai LY, Kuperman S, Minchin S. Cerebellar structure in autism. American Journal of Diseases of Children. 1987;141:1330–1332
  25. Gizewski ER, Timmann D, Forsting M. Specific cerebellar activation during Braille reading in blind subjects. Human Brain Mapping. 2004;22:229–235
  26. Gizewski ER, Lambertz N, Ladd ME, Timmann D, Forsting M. Cerebellar activation patterns in deaf participants for perception of sign language and written text. Neuroreport. 2005;16:1913–1917
  27. Good CD, Johnsrude IS, Ashburner J, Henson RN, Friston KJ, Frackowiak RS. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage. 2001;14:21–36
  28. Gothelf D, Furfaro JA, Hoeft F, Eckert MA, Hall SS, O'Hara R, et al. Neuroanatomy of fragile X syndrome is associated with aberrant behavior and the fragile X mental retardation protein (FMRP). Annals of Neurology. 2007;63:40–51
  29. Grossman AW, Aldridge GM, Weiler IJ, Greenough WT. Local protein synthesis and spine morphogenesis: fragile X syndrome and beyond. Journal of Neuroscience. 2006;26:7151–7155
  30. Hadjikhani N, Joseph RM, Snyder J, Tager-Flusberg H. Anatomical differences in the mirror neuron system and social cognition network in autism. Cerebral Cortex. 2006;16:1276–1282
  31. Hagerman PJ. Lessons from fragile X regarding neurobiology, autism, and neurodegeneration. Journal of Developmental and Behavioral Pediatrics. 2006;27:63–74
  32. Hagerman PJ. The fragile X prevalence paradox. Journal of Medical Genetics. 2008;45:498–499
  33. Hagerman RJ. Fragile X syndrome. Molecular and clinical insights and treatment issues. Western Journal of Medicine. 1997;166:129–137
  34. Hagerman RJ, Jackson AW, Levitas A, Rimland B, Braden M. An analysis of autism in fifty males with the fragile X syndrome. American Journal of Medical Genetics. 1986;23:359–374
  35. Hagerman RJ, Rivera S, Hagerman PJ. The fragile X family of disorders: a model for autism and targeted treatments. Current Pediatric Reviews. 2008;4:40–52
  36. Hallahan B, Daly EM, McAlonan G, Loth E, Toal F, O'Brien F, et al. Brain morphometry volume in autistic spectrum disorder: a magnetic resonance imaging study of adults. Psychological Medicine. 2009;39:337–346
  37. Hardan AY, Minshew NJ, Harenski K, Keshavan MS. Posterior fossa magnetic resonance imaging in autism. Journal of the American Academy of Child and Adolescent Psychiatry. 2001;40:666–672
  38. Harris GJ, Chabris CF, Clark J, Urban T, Aharon I, Steele S, et al. Brain activation during semantic processing in autism spectrum disorders via functional magnetic resonance imaging. Brain and Cognition. 2006;61:54–68
  39. Hashimoto T, Tayama M, Miyazaki M, Murakawa K, Kuroda Y. Brainstem and cerebellar vermis involvement in autistic children. Journal of Child Neurology. 1993;8:149–153
  40. Herbert MR. Large brains in autism: the challenge of pervasive abnormality. Neuroscientist. 2005;11:417–440
  41. Herbert MR, Harris GJ, Adrien KT, Ziegler DA, Makris N, Kennedy DN, et al. Abnormal asymmetry in language association cortex in autism. Annals of Neurology. 2002;52:588–596
  42. Herbert MR, Ziegler DA, Deutsch CK, O'Brien LM, Lange N, Bakardjiev A, et al. Dissociations of cerebral cortex, subcortical and cerebral white matter volumes in autistic boys. Brain. 2003;126:1182–1192
  43. Hjalgrim H, Jacobsen TB, Norgaard K, Lou HC, Brondum-Nielsen K, Jonassen O. Frontal-subcortical hypofunction in the fragile X syndrome. American Journal of Medical Genetics. 1999;83:140–141
  44. Hoeft F, Hernandez A, Parthasarathy S, Watson CL, Hall SS, Reiss AL. Fronto-striatal dysfunction and potential compensatory mechanisms in male adolescents with fragile X syndrome. Human Brain Mapping. 2007;28:543–554
  45. Hollander E, Anagnostou E, Chaplin W, Esposito K, Haznedar MM, Licalzi E, et al. Striatal volume on magnetic resonance imaging and repetitive behaviors in autism. Biological Psychiatry. 2005;58:226–232
  46. Irwin SA, Galvez R, Greenough WT. Dendritic spine structural anomalies in fragile-X mental retardation syndrome. Cerebral Cortex. 2000;10:1038–1044
  47. Just MA, Cherkassky VL, Keller TA, Minshew NJ. Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain. 2004;127:1811–1821
  48. Kaufmann WE, Cooper KL, Mostofsky SH, Capone GT, Kates WR, Newschaffer CJ, et al. Specificity of cerebellar vermian abnormalities in autism: a quantitative magnetic resonance imaging study. Journal of Child Neurology. 2003;18:463–470
  49. Ke X, Hong S, Tang T, Zou B, Li H, Hang Y, et al. Voxel-based morphometry study on brain structure in children with high-functioning autism. Neuroreport. 2008;19:921–925
  50. Kerby DS, Dawson BL. Autistic features, personality, and adaptive behavior in males with the fragile X syndrome and no autism. American Journal of Mental Retardation. 1994;98:455–462
  51. Keshavan MS, Bagwell WW, Haas GL, Sweeney JA, Schooler NR, Pettegrew JW. Changes in caudate volume with neuroleptic treatment. Lancet. 1994;344:1434
  52. Kielinen M, Rantala H, Timonen E, Linna SL, Moilanen I. Associated medical disorders and disabilities in children with autistic disorder: a population-based study. Autism. 2004;8:49–60
  53. Kwon H, Ow AW, Pedatella KE, Lotspeich LJ, Reiss AL. Voxel-based morphometry elucidates structural neuroanatomy of high-functioning autism and Asperger syndrome. Developmental Medicine and Child Neurology. 2004;46:760–764
  54. Langen M, Durston S, Staal WG, Palmen SJ, van Engeland H. Caudate nucleus is enlarged in high-functioning medication-naive subjects with autism. Biological Psychiatry. 2007;62:262–266
  55. Lee AD, Leow AD, Lu A, Reiss AL, Hall S, Chiang MC, et al. 3D pattern of brain abnormalities in Fragile X syndrome visualized using tensor-based morphometry. Neuroimage. 2007;34:924–938
  56. Leiner HC, Leiner AL, Dow RS. Cognitive and language functions of the human cerebellum. Trends in Neurosciences. 1993;16:444–447
  57. Levitt JG, Blanton R, Capetillo-Cunliffe L, Guthrie D, Toga A, McCracken JT. Cerebellar vermis lobules VIII–X in autism. Progress in Neuro-Psychopharmacology and Biological Psychiatry. 1999;23:625–633
  58. Lord C, Rutter M, Le Couteur A. Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders. 1994;24:659–685
  59. Lord C, Risi S, Lambrecht L, Cook EH, Leventhal BL, DiLavore PC, et al. The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders. 2000;30:205–223
  60. Manes F, Piven J, Vrancic D, Nanclares V, Plebst C, Starkstein SE. An MRI study of the corpus callosum and cerebellum in mentally retarded autistic individuals. Journal of Neuropsychiatry and Clinical Neurosciences. 1999;11:470–474
  61. McAlonan GM, Daly E, Kumari V, Critchley HD, van Amelsvoort T, Suckling J, et al. Brain anatomy and sensorimotor gating in Asperger's syndrome. Brain. 2002;125:1594–1606
  62. McAlonan GM, Cheung V, Cheung C, Suckling J, Lam GY, Tai KS, et al. Mapping the brain in autism. A voxel-based MRI study of volumetric differences and intercorrelations in autism. Brain. 2005;128:268–276
  63. Menon V, Leroux J, White CD, Reiss AL. Frontostriatal deficits in fragile X syndrome: relation to FMR1 gene expression. Proceedings of the National Academy of Sciences of the United States of America. 2004;101:3615–3620
  64. Meryash DL, Szymanski LS, Gerald PS. Infantile autism associated with the fragile-X syndrome. Journal of Autism and Developmental Disorders. 1982;12:295–301
  65. Mostofsky SH, Mazzocco MM, Aakalu G, Warsofsky IS, Denckla MB, Reiss AL. Decreased cerebellar posterior vermis size in fragile X syndrome: correlation with neurocognitive performance. Neurology. 1998;50:121–130
  66. Murakami JW, Courchesne E, Press GA, Yeung-Courchesne R, Hesselink JR. Reduced cerebellar hemisphere size and its relationship to vermal hypoplasia in autism. Archives of Neurology. 1989;46:689–694
  67. Palmen SJ, van Engeland H. Review on structural neuroimaging findings in autism. Journal of Neural Transmission. 2004;111:903–929
  68. Palmen SJ, Hulshoff Pol HE, Kemner C, Schnack HG, Durston S, Lahuis BE, et al. Increased gray-matter volume in medication-naive high-functioning children with autism spectrum disorder. Psychological Medicine. 2005;35:561–570
  69. Penn HE. Neurobiological correlates of autism: a review of recent research. Child Neuropsychology. 2006;12:57–79
  70. Piven J, Arndt S, Bailey J, Andreasen N. Regional brain enlargement in autism: a magnetic resonance imaging study. Journal of the American Academy of Child and Adolescent Psychiatry. 1996;35:530–536
  71. Piven J, Bailey J, Ranson BJ, Arndt S. An MRI study of the corpus callosum in autism. American Journal of Psychiatry. 1997;154:1051–1056
  72. Piven J, Saliba K, Bailey J, Arndt S. An MRI study of autism: the cerebellum revisited. Neurology. 1997;49:546–551
  73. Redcay E, Courchesne E. When is the brain enlarged in autism? A meta-analysis of all brain size reports. Biological Psychiatry. 2005;58:1–9
  74. Reddy KS. Cytogenetic abnormalities and fragile-X syndrome in Autism Spectrum Disorder. BMC Medical Genetics. 2005;6:3
  75. Reiss AL, Patel S, Kumar AJ, Freund L. Preliminary communication: neuroanatomical variations of the posterior fossa in men with the fragile X (Martin-Bell) syndrome. American Journal of Medical Genetics. 1988;31:407–414
  76. Reiss AL, Aylward E, Freund LS, Joshi PK, Bryan RN. Neuroanatomy of fragile X syndrome: the posterior fossa. Annals of Neurology. 1991;29:26–32
  77. Reiss AL, Freund L, Tseng JE, Joshi PK. Neuroanatomy in fragile X females: the posterior fossa. American Journal of Human Genetics. 1991;49:279–288
  78. Reiss AL, Abrams MT, Greenlaw R, Freund L, Denckla MB. Neurodevelopmental effects of the FMR-1 full mutation in humans. Natural Medicines. 1995;1:159–167
  79. Rogers SJ, Wehner DE, Hagerman R. The behavioral phenotype in fragile X: symptoms of autism in very young children with fragile X syndrome, idiopathic autism, and other developmental disorders. Journal of Developmental and Behavioral Pediatrics. 2001;22:409–417
  80. Rojas DC, Peterson E, Winterrowd E, Reite ML, Rogers SJ, Tregellas JR. Regional gray matter volumetric changes in autism associated with social and repetitive behavior symptoms. BMC Psychiatry. 2006;6:56
  81. Salmond CH, Ashburner J, Connelly A, Friston KJ, Gadian DG, Vargha-Khadem F. The role of the medial temporal lobe in autistic spectrum disorders. European Journal of Neuroscience. 2005;22:764–772
  82. Salmond CH, Vargha-Khadem F, Gadian DG, de Haan M, Baldeweg T. Heterogeneity in the patterns of neural abnormality in autistic spectrum disorders: evidence from ERP and MRI. Cortex. 2007;43:686–699
  83. Schaefer GB, Lutz RE. Diagnostic yield in the clinical genetic evaluation of autism spectrum disorders. Genetics in Medicine. 2006;8:549–556
  84. Sears LL, Vest C, Mohamed S, Bailey J, Ranson BJ, Piven J. An MRI study of the basal ganglia in autism. Progress in Neuro-Psychopharmacology and Biological Psychiatry. 1999;23:613–624
  85. Sparks BF, Friedman SD, Shaw DW, Aylward EH, Echelard D, Artru AA, et al. Brain structural abnormalities in young children with autism spectrum disorder. Neurology. 2002;59:184–192
  86. Spitzer RL, Endicott J, Robins E. Research diagnostic criteria: rationale and reliability. Archives of General Psychiatry. 1978;35:773–782
  87. Steffenburg S, Gillberg C, Hellgren L, Andersson L, Gillberg IC, Jakobsson G, et al. A twin study of autism in Denmark, Finland, Iceland, Norway and Sweden. Journal of Child Psychology and Psychiatry and Allied Disciplines. 1989;30:405–416
  88. Tassone F, Hagerman RJ, Ikle DN, Dyer PN, Lampe M, Willemsen R, et al. FMRP expression as a potential prognostic indicator in fragile X syndrome. American Journal of Medical Genetics. 1999;84:250–261
  89. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 2002;15:273–289
  90. Verkerk AJ, Pieretti M, Sutcliffe JS, Fu YH, Kuhl DP, Pizzuti A, et al Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell. 1991;65:905–914
  91. Voelbel GT, Bates ME, Buckman JF, Pandina G, Hendren RL. Caudate nucleus volume and cognitive performance: are they related in childhood psychopathology?. Biological Psychiatry. 2006;60:942–950
  92. Waiter GD, Williams JH, Murray AD, Gilchrist A, Perrett DI, Whiten A. A voxel-based investigation of brain structure in male adolescents with autistic spectrum disorder. Neuroimage. 2004;22:619–625
  93. Wassink TH, Piven J, Patil SR. Chromosomal abnormalities in a clinic sample of individuals with autistic disorder. Psychiatric Genetics. 2001;11:57–63
  94. Wechsler D. Wechsler Adult Intelligence Scale-Revised Manual. San Antonio, TX: Psychological Corporation; 1981;
  95. Wechsler D. Wechsler Adult Intelligence Scale-III Manual. San Antonio, TX: Psychological Corporation; 1997;
  96. Willcutt EG, Pennington BF, Boada R, Ogline JS, Tunick RA, Chhabildas NA, et al. A comparison of the cognitive deficits in reading disability and attention-deficit/hyperactivity disorder. Journal of Abnormal Psychology. 2001;110:157–172
  97. Worsley KJ, Marrett S, Neelin P, Vandal AC, Friston KJ, Evans AC. A unified statistical approach for determining significant voxels in images of cerebral activation. Human Brain Mapping. 1996;4:58–73
  98. Yang MS, Gill M. A review of gene linkage, association and expression studies in autism and an assessment of convergent evidence. International Journal of Developmental Neuroscience. 2007;25:69–85
  99. Yeung-Courchesne R, Courchesne E. From impasse to insight in autism research: from behavioral symptoms to biological explanations. Development and Psychopathology. 1997;9:389–419

PII: S0925-4927(09)00113-9

doi: 10.1016/j.pscychresns.2009.04.013

Psychiatry Research: Neuroimaging
Volume 174, Issue 2 , Pages 138-145 , 30 November 2009

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