Female children with autism spectrum disorder: An insight from mass-univariate and pattern classification analyses

NeuroImage

Volumn 59, Issue 2, 2012, Pages 1013-1022

  Calderoni, Sara ^a,b   Retico, Alessandra ^c   Biagi, Laura ^a   Tancredi, Raffaella ^a   Muratori, Filippo ^a,b   Tosetti, Michela ^a  

^a DEPARTMENT OF DEVELOPMENTAL NEUROSCIENCE   (Italy)

^b UNIVERSITY OF PISA   (Italy)

^c INFN SEZIONE DI PISA   (Italy)

Author keywords

Autism spectrum disorders; Children; Female; Magnetic resonance imaging; Support vector machine; Voxel based morphometry

Indexed keywords

AREA UNDER THE CURVE; ARTICLE; AUTISM; BRAIN REGION; BRAIN SIZE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GRAY MATTER; HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOGENESIS; PATHOLOGICAL ANATOMY; PRIORITY JOURNAL; SCHOOL CHILD; SCORING SYSTEM; SUPERIOR FRONTAL GYRUS; SUPPORT VECTOR MACHINE; VOXEL BASED MORPHOMETRY;

ALGORITHMS; ARTIFICIAL INTELLIGENCE; BRAIN; CHILD; CHILD DEVELOPMENT DISORDERS, PERVASIVE; CHILD, PRESCHOOL; FEMALE; HUMANS; IMAGE ENHANCEMENT; IMAGE INTERPRETATION, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; MAGNETIC RESONANCE IMAGING; MULTIVARIATE ANALYSIS; NEURONS; ORGAN SIZE; PATTERN RECOGNITION, AUTOMATED; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY;

EID: 83055181241     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.08.070     Document Type: Article

References (85)

1. Abell F., Krams M., Ashburner J., Passingham R., Friston K., Frackowiak R., Happé F., Frith C., Frith U. The neuroanatomy of autism: a voxel-based whole brain analysis of structural scans. Neuroreport 1999, 10:1647-1651.
2. Amaral D.G., Schumann C.M., Nordahl C.W. Neuroanatomy of autism. Trends Neurosci. 2008, 31:137-145.
3. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders, Text Revised (DSM-IV-TR) 2000, American Psychiatric Association, Washington, D.C. 4th ed.
4. Amodio D.M., Frith C.D. Meeting of minds: the medial frontal cortex and social cognition. Nat. Rev. Neurosci. 2006, 7:268-277.
5. Ashburner J. A fast diffeomorphic image registration algorithm. NeuroImage 2007, 38:95-113.
6. Ashburner J., Friston K.J. Voxel-based morphometry-the methods. NeuroImage 2000, 11:805-821.
7. Aylward E.H., Minshew N.J., Field K., Sparks B.F., Singh N. Effects of age on brain volume and head circumference in autism. Neurology 2002, 59:175-183.
8. Baron-Cohen S. The extreme male brain theory of autism. Trends Cogn. Sci. 2002, 6:248-254.
9. Bauman M.L., Kemper T.L. Histoanatomic observations of the brain in early infantile autism. Neurology 1985, 35:866-874.
10. Bloss C.S., Courchesne E. MRI neuroanatomy in young girls with autism: a preliminary study. J. Am. Acad. Child Adolesc. Psychiatry 2007, 46:515-523.
11. Boddaert N., Chabane N., Gervais H., Good C.D., Bourgeois M., Plumet M.H., Barthélémy C., Mouren M.C., Artiges E., Samson Y., Brunelle F., Frackowiak R.S., Zilbovicius M. Superior temporal sulcus anatomical abnormalities in childhood autism: a voxel-based morphometry MRI study. NeuroImage 2004, 23:364-369.
12. Buxhoeveden D.P., Semendeferi K., Buckwalter J., Schenker N., Switzer R., Courchesne E. Reduced minicolumns in the frontal cortex of patients with autism. Neuropathol. Appl. Neurobiol. 2006, 32:483-491.
13. Canu E., McLaren D.G., Fitzgerald M.E., Bendlin B.B., Zoccatelli G., Alessandrini F., Pizzini F.B., Ricciardi G.K., Beltramello A., Johnson S.C., Frisoni G.B. Microstructural diffusion changes are independent of macrostructural volume loss in moderate to severe Alzheimer's disease. J. Alzheimers Dis. 2010, 19:963-976.
14. Carper R.A., Courchesne E. Localized enlargement of the frontal cortex in early autism. Biol. Psychiatry 2005, 57:126-133.
15. Carper R.A., Moses P., Tigue Z.D., Courchesne E. Cerebral lobes in autism: early hyperplasia and abnormal age effects. NeuroImage 2002, 16:1038-1051.
16. Casanova M.F., Buxhoeveden D.P., Switala A.E., Roy E. Minicolumnar pathology in autism. Neurology 2002, 58:428-432.
17. Centers for Disease Control and Prevention (CDC) Autism and Developmental Disabilities Monitoring Network Surveillance Year 2006 Principal Investigators. Prevalence of autism spectrum disorders - Autism and Developmental Disabilities Monitoring Network, United States, 2006. MMWR Surveill. Summ. 2009, 58:1-20.
18. Chen R., Jiao Y., Herskovits E.H. Structural MRI in autism spectrum disorder. Pediatr. Res. 2011, 69:63R-68R.
19. Courchesne E., Karns C.M., Davis H.R., Ziccardi R., Carper R.A., Tigue Z.D., Pierce K., Moses P., Chisum H.J., Lord C., Lincoln A.J., Pizzo S., Schreibman L., Haas R.H., Akshoomoff N., Courchesne R.Y. 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. JAMA 2003, 290:337-344.
21. Courchesne E., Pierce K., Schumann C.M., Redcay E., Buckwalter J.A., Kennedy D.P., Morgan J. Mapping early brain development in autism. Neuron 2007, 56:399-413.
22. Craig M.C., Zaman S.H., Daly E.M., Cutter W.J., Robertson D.M., Hallahan B., Toal F., Reed S., Ambikapathy A., Brammer M., Murphy C.M., Murphy D.G. Women with autistic-spectrum disorder: magnetic resonance imaging study of brain anatomy. Br. J. Psychiatry 2007, 191:224-228.
23. Crone E.A., Poldrack R.A., Durston S. Challenges and methods in developmental neuroimaging. Hum. Brain Mapp. 2010, 31:835-837.
24. Davatzikos C. Why voxel-based morphometric analysis should be used with great caution when characterizing group differences. NeuroImage 2004, 23:17-20.
25. De Martino F., Valente G., Staeren N., Ashburner J., Goebel R., Formisano E. Combining multivariate voxel selection and support vector machines for mapping and classification of fMRI spatial patterns. NeuroImage 2008, 43:44-58.
26. Duncan J., Owen A.M. Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci. 2000, 23:475-483.
27. Ecker C., Rocha-Rego V., Johnston P., Mourao-Miranda J., Marquand A., Daly E.M., Brammer M.J., Murphy C., Murphy D.G. Investigating the predictive value of whole-brain structural MR scans in autism: a pattern classification approach. NeuroImage 2010, 49:44-56. MRC AIMS Consortium.
28. Ecker C., Marquand A., Mourão-Miranda J., Johnston P., Daly E.M., Brammer M.J., Maltezos S., Murphy C.M., Robertson D., Williams S.C., Murphy D.G. Describing the brain in autism in five dimensions-magnetic resonance imaging-assisted diagnosis of autism spectrum disorder using a multiparameter classification approach. J. Neurosci. 2010, 30:10612-10623.
29. Fan Y., Shen D., Davatzikos C. Classification of structural images via high-dimensional image warping, robust feature extraction, and SVM. Med. Image Comput. Comput. Assist. Interv. 2005, 8:1-8.
30. Fatemi S.H., Earle J., Kanodia R., Kist D., Emamian E.S., Patterson P.H., Shi L., Sidwell R. Prenatal viral infection leads to pyramidal cell atrophy and macrocephaly in adulthood: implications for genesis of autism and schizophrenia. Cell. Mol. Neurobiol. 2002, 22:25-33.
31. Frith U. Mind blindness and the brain in autism. Neuron 2001, 32:969-979.
32. Frith U., Morton J., Leslie A. The cognitive basis of a biological disorder: autism. Trends Neurosci. 1991, 14:433-438.
33. Fukumoto A., Hashimoto T., Mori K., Tsuda Y., Arisawa K., Kagami S. Head circumference and body growth in autism spectrum disorders. Brain Dev. 2011, 33:569-575.
34. Gillberg C., Cederlund M., Lamberg K., Zeijlon L. Brief report: "the autism epidemic". The registered prevalence of autism in a Swedish urban area. J. Autism Dev. Disord. 2006, 36:429-435.
35. Gilmore J.H., Lin W., Prastawa M.W., Looney C.B., Vetsa Y.S., Knickmeyer R.C., Evans D.D., Smith J.K., Hamer R.M., Lieberman J.A., Gerig G. Regional gray matter growth, sexual dimorphism, and cerebral asymmetry in the neonatal brain. J. Neurosci. 2007, 27:1255-1260.
36. Green D.M., Swets J.A. Signal Detection Theory and Psychophysics 1966, Wiley, New York.
37. Griffiths R. The Abilities of Young Children: A Comprehensive System of Mental Measurement for the First Eight Years of Life 1984, A.R.I.C.D. The Test Agency Limited, Bucks, U.K. Revised ed.
38. Guyon I., Weston J., Barnhill S., Vapnik V. Gene selection for cancer classification using support vector machines. Mach. Learn. 2002, 46:389-422.
39. Hardan A.Y., Libove R.A., Keshavan M.S., Melhem N.M., Minshew N.J. A preliminary longitudinal magnetic resonance imaging study of brain volume and cortical thickness in autism. Biol. Psychiatry 2009, 66:320-326.
40. Hazlett H.C., Poe M., Gerig G., Smith R.G., Provenzale J., Ross A., Gilmore J., Piven J. Magnetic resonance imaging and head circumference study of brain size in autism: birth through age 2years. Arch. Gen. Psychiatry 2005, 62:1366-1376.
41. Herbert M.R., Ziegler D.A., Deutsch C.K., O'Brien L.M., Lange N., Bakardjiev A., Hodgson J., Adrien K.T., Steele S., Makris N., Kennedy D., Harris G.J., Caviness V.S. Dissociations of cerebral cortex, subcortical and cerebral white matter volumes in autistic boys. Brain 2003, 126:1182-1192.
42. Joachims T. Making Large-scale SVM Learning Practical. Advances in Kernel Methods - Support Vector Learning 1999, MIT-Press. http://svmlight.joachims.org/, B. Scholkopf, C. Burges, A. Smola (Eds.).
43. Jou R.J., Minshew N.J., Keshavan M.S., Hardan A.Y. Cortical gyrification in autistic and Asperger disorders: a preliminary magnetic resonance imaging study. J. Child Neurol. 2010, 25:1462-1467.
44. Kates W.R., Burnette C.P., Eliez S., Strunge L.A., Kaplan D., Landa R., Reiss A.L., Pearlson G.D. Neuroanatomic variation in monozygotic twin pairs discordant for the narrow phenotype for autism. Am. J. Psychiatry 2004, 161:539-546.
45. Klöppel S., Stonnington C.M., Chu C., Draganski B., Scahill R.I., Rohrer J.D., Fox N.C., Jack C.R., Ashburner J., Frackowiak R.S. Automatic classification of MR scans in Alzheimer's disease. Brain 2008, 131:681-689.
46. Lao Z., Shen D., Xue Z., Karacali B., Resnick S.M., Davatzikos C. Morphological classification of brains via high-dimensional shape transformations and machine learning methods. NeuroImage 2004, 21:46-57.
47. Levitt J.G., Blanton R.E., Smalley S., Thompson P.M., Guthrie D., McCracken J.T., Sadoun T., Heinichen L., Toga A.W. Cortical sulcal maps in autism. Cereb. Cortex 2003, 13:728-735.
48. Lombardo M.V., Chakrabarti B., Bullmore E.T., Sadek S.A., Pasco G., Wheelwright S.J., Suckling J., MRC AIMS Consortium, Baron-Cohen S. Atypical neural self-representation in autism. Brain 2010, 133:611-624.
49. Lombardo M.V., Chakrabarti B., Bullmore E.T., Baron-Cohen S., MRC AIMS Consortium Specialization of right temporo-parietal junction for mentalizing and its relation to social impairments in autism. NeuroImage 2011.
50. Lord C., Risi S., Lambrecht L., Cook E., Leventhal B.L., DiLavore P.C., Pickles A., Rutter M. The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J. Autism Dev. Disord. 2000, 30:205-223.
51. McLaren D.G., Kostmatka K.J., Kastman E.K., Bendlin B.B., Johnson S.C. Rhesus macaque brain morphometry: a methodological comparison of voxel-wise approaches. Methods 2010, 50:157-165.
52. Metz C.E. ROC methodology in radiologic imaging. Invest. Radiol. 1986, 21:720-733.
53. Minshew N., Luna B., Sweeney J. Oculomotor evidence for neocortical systems but not cerebellar dysfunction in autism. Neurology 1999, 52:917-922.
54. Mosconi M.W., Cody-Hazlett H., Poe M.D., Gerig G., Gimpel-Smith R., Piven J. Longitudinal study of amygdala volume and joint attention in 2- to 4-year-old children with autism. Arch. Gen. Psychiatry 2009, 66:509-516.
55. Mourão-Miranda J., Bokde A.L., Born C., Hampel H., Stetter M. Classifying brain states and determining the discriminating activation patterns: support vector machine on functional MRI data. NeuroImage 2005, 28:980-995.
56. Palmen S.J., Hulshoff Pol H.E., Kemner C., Schnack H.G., Durston S., Lahuis B.E., Kahn R.S., Van Engeland H. Increased gray-matter volume in medication naive high-functioning children with autism spectrum disorder. Psychol. Med. 2005, 35:561-570.
57. Piven J., Arndt S., Bailey J., Havercamp S., Andreasen N.C., Palmer P. An MRI study of brain size in autism. Am. J. Psychiatry 1995, 152:1145-1149.
58. Piven J., Arndt S., Bailey J., Andreasen N. Regional brain enlargement in autism: a magnetic resonance imaging study. J. Am. Acad. Child Adolesc. Psychiatry 1996, 35:530-536.
59. Radua J., Via E., Catani M., Mataix-Cols D. Voxel-based meta-analysis of regional white-matter volume differences in autism spectrum disorder versus healthy controls. Psychol. Med. 2010, 16:1-12.
60. Ramnani N., Owen A.M. Anterior prefrontal cortex: insights into function from anatomy and neuroimaging. Nat. Rev. Neurosci. 2004, 5:184-194.
61. Ringo J.L. Neuronal interconnection as a function of brain size. Brain Behav. Evol. 1991, 38:1-6.
62. Roid G.H., Miller L.J. The Leiter International Performance Scale-revised Edition 1997, Psychological Assessment Resources, Lutz, FL.
63. Saxe R., Kanwisher N. People thinking about thinking people. The role of the temporo-parietal junction in "theory of mind". NeuroImage 2003, 19:1835-1842.
64. Schmitz N., Rubia K., van Amelsvoort T., Daly E., Smith A., Murphy D.G. Neural correlates of reward in autism. Br. J. Psychiatry 2008, 192:19-24.
65. Schopler E., Reichler R.J., Renner B.R. The Childhood Autism Rating Scale 1988, Western Psychological Services, Los Angeles, CA.
66. Schumann C.M., Bloss C.S., Barnes C.C., Wideman G.M., Carper R.A., Akshoomoff N., Pierce K., Hagler D., Schork N., Lord C., Courchesne E. Longitudinal magnetic resonance imaging study of cortical development through early childhood in autism. J. Neurosci. 2010, 30:4419-4427.
67. Solomon M., Ozonoff S.J., Ursu S., Ravizza S., Cummings N., Ly S., Carter C.S. The neural substrates of cognitive control deficits in autism spectrum disorders. Neuropsychologia 2009, 47:2515-2526.
68. Sparks B.F., Friedman S.D., Shaw D.W., Aylward E.H., Echelard D., Artru A.A., Maravilla K.R., Giedd J.N., Munson J., Dawson G., Dager S.R. Brain structural abnormalities in young children with autism spectrum disorder. Neurology 2002, 59:184-192.
69. Tsai L.Y., Beisler J.M. The development of sex differences in infantile autism. Br. J. Psychiatry 1983, 142:373-378.
70. Tsai L., Stewart M.A., August G. Implication of sex differences in the familial transmission of infantile autism. J. Autism Dev. Disord. 1981, 11:165-173.
71. Van Overwalle F. A dissociation between social mentalizing and general reasoning. NeuroImage 2011, 54:1589-1599.
72. Van Overwalle F., Baetens K. Understanding others' actions and goals by mirror and mentalizing systems: a meta-analysis. NeuroImage 2009, 48:564-584.
73. Vapnik V.N. The Nature of Statistical Learning Theory 1995, Springer, New York.
74. Via E., Radua J., Cardoner N., Happé F., Mataix-Cols D. Meta-analysis of gray matter abnormalities in autism spectrum disorder: should Asperger disorder be subsumed under a broader umbrella of autistic spectrum disorder?. Arch. Gen. Psychiatry 2011, 68:409-418.
75. Waiter G.D., Williams J.H., Murray A.D., Gilchrist A., Perrett D.I., Whiten A. A voxel-based investigation of brain structure in male adolescents with autistic spectrum disorder. NeuroImage 2004, 22:619-625.
76. Wassink T.H., Hazlett H.C., Epping E.A., Arndt S., Dager S.R., Schellenberg G.D., Dawson G., Piven J. Cerebral cortical gray matter overgrowth and functional variation of the serotonin transporter gene in autism. Arch. Gen. Psychiatry 2007, 64:709-717.
77. Wechsler D. Wechsler Preschool and Primary Scale of Intelligence (WWPSI) 1973, Organizzazioni Speciali, Firenze (Italy).
78. Wechsler D. Wechsler Intelligence Scale for Children - Revised (WISC-R) 1986, Organizzazioni Speciali, Firenze (Italy).
79. Williams J.H., Waiter G.D., Perra O., Perrett D.I., Whiten A. An fMRI study of joint attention experience. NeuroImage 2005, 25:133-140.
80. Williams D.L., Goldstein G., Minshew N.J. Neuropsychologic functioning in children with autism: further evidence for disordered complex information-processing. Child Neuropsychol. 2006, 12:279-298.
81. Wing L. Sex ratios in early childhood autism and related conditions. Psychiatry Res. 1981, 5:129-137.
82. Yassa M.A., Stark C.E. A quantitative evaluation of cross-participant registration techniques for MRI studies of the medial temporal lobe. NeuroImage 2009, 44:319-327.
83. Zaitchik D., Walker C., Miller S., LaViolette P., Feczko E., Dickerson B.C. Mental state attribution and the temporoparietal junction: an fMRI study comparing belief, emotion, and perception. Neuropsychologia 2010, 48:2528-2536.
84. Zeegers M., Pol H.H., Durston S., Nederveen H., Schnack H., van Daalen E., Dietz C., van Engeland H., Buitelaar J. No differences in MR-based volumetry between 2 and 7-year-old children with autism spectrum disorder and developmental delay. Brain Dev. 2009, 31:725-730.
85. Zysset S., Huber O., Samson A., Ferstl E.C., von Cramon D.Y. Functional specialization within the anterior medial prefrontal cortex: a functional magnetic resonance imaging study with human subjects. Neurosci. Lett. 2003, 335:183-186.