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Developmental neurogenetics and multimodal neuroimaging of sex differences in autism

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Abstract

Examining sex differences in the brain has been historically contentious but is nonetheless important for advancing mental health for both girls and boys. Unfortunately, females in biomedical research remain underrepresented in most mental health conditions including autism spectrum disorders (ASD), even though equal inclusion of females would improve treatment for girls and yield benefits to boys. This review examines sex differences in the relationship between neuroanatomy and neurogenetics of ASD. Recent findings reveal that girls diagnosed with ASD exhibit more intellectual and behavioral problems compared to their male counterparts, suggesting that girls may be less likely diagnosed in the absence of such problems or that they require a higher mutational load to meet the diagnostic criteria. Thus far, the female biased effect of chromosome 4, 5p15.33, 8p, 9p24.1, 11p12-13, 15q, and Xp22.3 and the male biased effect of 1p31.3, 5q12.3, 7q, 9q33.3, 11q13.4, 13q33.3, 16p11.2, 17q11-21, Xp22.33/Yp11.31, DRD1, NLGN3, MAOA, and SHANK1 deletion have been discovered in ASD. The SNPs of genes such as RYR2, UPP2, and the androgen receptor gene have been shown to have sex-biasing factors in both girls and boys diagnosed with ASD. These sex-related genetic factors may drive sex differences in the neuroanatomy of these girls and boys, including abnormal enlargement in temporal gray and white matter volumes, and atypical reduction in cerebellar gray matter volumes and corpus callosum fibers projecting to the anterior frontal cortex in ASD girls relative to boys. Such factors may also be responsible for the attenuation of brain sexual differentiation in adult men and women with ASD; however, much remains to be uncovered or replicated. Future research should leverage further the association between neuroanatomy and genetics in girls for an integrated and interdisciplinary understanding of ASD.

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References

  • ABS (2011). All Persons with autism, by sex - 2009. Canberra, Australia.

  • Ahmed, E. I., Zehr, J. L., Schulz, K. M., Lorenz, B. H., DonCarlos, L. L., & Sisk, C. L. (2008). Pubertal hormones modulate the addition of new cells to sexually dimorphic brain regions. Nature Neuroscience, 11(9), 995–997.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Al-Farsi, Y. M., Al-Sharbati, M. M., Al-Farsi, O. A., Al-Shafaee, M. S., Brooks, D. R., & Waly, M. I. (2011). Brief report: prevalence of autistic spectrum disorders in the Sultanate of Oman. Journal of Autism and Developmental Disorders, 41(6), 821–825.

    Article  PubMed  Google Scholar 

  • Andersson, G. W., Gillberg, C., & Miniscalco, C. (2013). Pre-school children with suspected autism spectrum disorders: do girls and boys have the same profiles? Research in Developmental Disabilities, 34(1), 413–422.

    Article  PubMed  Google Scholar 

  • APA. (2013). Diagnostic and statistical manual of mental disorders. Washington: American Psychiatric Association.

    Google Scholar 

  • Arnold, A. P. (2004). Sex chromosomes and brain gender. Nature Review Neuroscience, 5(9), 701–708.

    Article  CAS  Google Scholar 

  • Bailey, A., Le Couteur, A., Gottesman, I., Bolton, P., Simonoff, E., Yuzda, E., & Rutter, M. (1995). Autism as a strongly genetic disorder: evidence from a British twin study. Psychological Medicine, 25(1), 63–77.

    Article  CAS  PubMed  Google Scholar 

  • Ballif, B. C., Hornor, S. A., Jenkins, E., Madan-Khetarpal, S., Surti, U., Jackson, K. E., Asamoah, A., Brock, P. L., Gowans, G. C., Conway, R. L., Graham, J. M., Medne, L., Zackai, E. H., Shaikh, T. H., Geoghegan, J., Selzer, R. R., Eis, P. S., Bejjani, B. A., & Shaffer, L. G. (2007). Discovery of a previously unrecognized microdeletion syndrome of 16p11.2–p12.2. Nature Genetics, 39(9), 1071–1073.

    Article  CAS  PubMed  Google Scholar 

  • Banach, R., Thompson, A., Szatmari, P., Goldberg, J., Tuff, L., Zwaigenbaum, L., & Mahoney, W. (2009). Brief report: relationship between non-verbal IQ and gender in autism. Journal of Autism and Developmental Disorders, 39(1), 188–193.

    Article  PubMed  Google Scholar 

  • Baron-Cohen, S., Knickmeyer, R. C., & Belmonte, M. K. (2005). Sex differences in the brain: implications for explaining autism. Science, 310(5749), 819–823.

    Article  CAS  PubMed  Google Scholar 

  • Baron-Cohen, S., Lombardo, M. V., Auyeung, B., Ashwin, E., Chakrabarti, B., & Knickmeyer, R. (2011). Why are autism spectrum conditions more prevalent in males? PLoS Biology, 9(6), e1001081.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bava, S., Boucquey, V., Goldenberg, D., Thayer, R. E., Ward, M., Jacobus, J., & Tapert, S. F. (2011). Sex differences in adolescent white matter architecture. Brain Research, 1375, 41–48.

    Article  CAS  PubMed  Google Scholar 

  • Beacher, F. D., Minati, L., Baron-Cohen, S., Lombardo, M. V., Lai, M. C., Gray, M. A., Harrison, N. A., & Critchley, H. D. (2012). Autism attenuates sex differences in brain structure: a combined voxel-based morphometry and diffusion tensor imaging study. AJNR - American Journal of Neuroradiology, 33(1), 83–89.

    Article  CAS  PubMed  Google Scholar 

  • Beery, A. K., & Zucker, I. (2011). Sex bias in neuroscience and biomedical research. Neuroscience and Biobehavioral Reviews, 35(3), 565–572.

    Article  PubMed  Google Scholar 

  • Begeer, S., Mandell, D., Wijnker-Holmes, B., Venderbosch, S., Rem, D., Stekelenburg, F., & Koot, H. M. (2013). Sex differences in the timing of identification among children and adults with autism spectrum disorders. Journal of Autism and Developmental Disorders, 43(5), 1151–1156.

    Article  PubMed  Google Scholar 

  • Bishop, D. V., Jacobs, P. A., Lachlan, K., Wellesley, D., Barnicoat, A., Boyd, P. A., Fryer, A., Middlemiss, P., Smithson, S., Metcalfe, K., Shears, D., Leggett, V., Nation, K., & Scerif, G. (2011). Autism, language and communication in children with sex chromosome trisomies. Archives of Disease in Childhood, 96(10), 954–959.

    Article  PubMed  Google Scholar 

  • Bloss, C. S., & Courchesne, E. (2007). MRI neuroanatomy in young girls with autism: a preliminary study. Journal of the American Academy of Child and Adolescent Psychiatry, 46(4), 515–523.

    Article  PubMed  Google Scholar 

  • Blumberg, S.J., Bramlett, M.D., Kogan, M.D., Schieve, L.A., Jones, J.R. & Lu, M.C. (2013). Changes in prevalence of parent-reported autism spectrum disorder in school-aged U.S. children: 2007 to 2011–2012. National Health Statistic Report, (65), 1–11, 11 p following 11.

  • Bölte, S., Duketis, E., Poustka, F., & Holtmann, M. (2011). Sex differences in cognitive domains and their clinical correlates in higher-functioning autism spectrum disorders. Autism, 15(4), 497–511.

    Article  PubMed  Google Scholar 

  • Boronat, S., Mehan, W. A., Shaaya, E. A., Thibert, R. L., & Caruso, P. (2015). Hippocampal abnormalities in magnetic resonance imaging (MRI) of 15q duplication syndromes. Journal of Child Neurology, 30(3), 333–338.

    Article  PubMed  Google Scholar 

  • Bortolato, M., Godar, S. C., Alzghoul, L., Zhang, J., Darling, R. D., Simpson, K. L., Bini, V., Chen, K., Wellman, C. L., Lin, R. C., & Shih, J. C. (2013). Monoamine oxidase A and A/B knockout mice display autistic-like features. International Journal of Neuropsychopharmacology, 16(4), 869–888.

    Article  CAS  PubMed  Google Scholar 

  • Brown, S., Gersen, S., Anyane-Yeboa, K., & Warburton, D. (1993). Preliminary definition of a “critical region” of chromosome 13 in q32: report of 14 cases with 13q deletions and review of the literature. American Journal of Medical Genetics, 45(1), 52–59.

    Article  CAS  PubMed  Google Scholar 

  • Brugha, T. S., McManus, S., Bankart, J., Scott, F., Purdon, S., Smith, J., Bebbington, P., Jenkins, R., & Meltzer, H. (2011). Epidemiology of autism spectrum disorders in adults in the community in England. Archives of General Psychiatry, 68(5), 459–465.

    Article  PubMed  Google Scholar 

  • Cahill, L. (2006). Why sex matters for neuroscience. Nature Review Neuroscience, 7(6), 477–484.

    Article  CAS  PubMed  Google Scholar 

  • Cahill, L. (2014). Equal ≠ the same: sex differences in the human brain. Cerebrum, 2014, 5.

    PubMed  PubMed Central  Google Scholar 

  • Calderoni, S., Retico, A., Biagi, L., Tancredi, R., Muratori, F., & Tosetti, M. (2012). Female children with autism spectrum disorder: an insight from mass-univariate and pattern classification analyses. NeuroImage, 59(2), 1013–1022.

    Article  PubMed  Google Scholar 

  • Cantor, R. M., Kono, N., Duvall, J. A., Alvarez-Retuerto, A., Stone, J. L., Alarcón, M., Nelson, S. F., & Geschwind, D. H. (2005). Replication of autism linkage: fine-mapping peak at 17q21. American Journal of Human Genetics, 76(6), 1050–1056.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carayol, J., Schellenberg, G. D., Dombroski, B., Amiet, C., Genin, B., Fontaine, K., Rousseau, F., Vazart, C., Cohen, D., Frazier, T. W., Hardan, A. Y., Dawson, G., & Rio Frio, T. (2014). A scoring strategy combining statistics and functional genomics supports a possible role for common polygenic variation in autism. Frontiers in Genetics, 5, 33.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carruth, L. L., Reisert, I., & Arnold, A. P. (2002). Sex chromosome genes directly affect brain sexual differentiation. Nature Neuroscience, 5(10), 933–934.

    Article  CAS  PubMed  Google Scholar 

  • Carter, A. S., Black, D. O., Tewani, S., Connolly, C. E., Kadlec, M. B., & Tager-Flusberg, H. (2007). Sex differences in toddlers with autism spectrum disorders. Journal of Autism and Developmental Disorders, 37(1), 86–97.

    Article  PubMed  Google Scholar 

  • CDC. (2007a). Prevalence of autism spectrum disorders --- autism and developmental disabilities monitoring network, 14 sites, United States, 2002. Morbidity and Mortality Weekly Report, 56(1), 12–28.

    Google Scholar 

  • CDC. (2007b). Prevalence of autism spectrum disorders --- autism and developmental disabilities monitoring network, six sites, United States, 2000. Morbidity and Mortality Weekly Report, 56(1), 1–11.

    Google Scholar 

  • CDC. (2009a). Brief update: prevalence of Autism Spectrum Disorders (ASDs) --- Autism and Developmental Disabilities Monitoring (ADDM) network, United States, 2004. Morbidity and Mortality Weekly Report, 58(10), 21–24.

    Google Scholar 

  • CDC. (2009b). Prevalence of autism spectrum disorders --- autism and developmental disabilities monitoring network, United States, 2006. Morbidity and Mortality Weekly Report, 58(10), 1–20.

    Google Scholar 

  • CDC. (2012). Prevalence of autism spectrum disorders - autism and developmental disabilities monitoring network, 14 sites, United States, 2008. Morbidity and Mortality Weekly Report, 61(3), 1–19.

    Google Scholar 

  • CDC. (2014). Prevalence of autism spectrum disorder among children aged 8 years — autism and developmental disabilities monitoring network, 11 sites, United States, 2010. Morbidity and Mortality Weekly Report, 63(2), 1–21.

    Google Scholar 

  • Chang, S. C., Pauls, D. L., Lange, C., Sasanfar, R., & Santangelo, S. L. (2013). Sex-specific association of a common variant of the XG gene with autism spectrum disorders. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 162B(7), 742–750.

    Article  CAS  Google Scholar 

  • Cheslack-Postava, K., & Jordan-Young, R. M. (2012). Autism spectrum disorders: toward a gendered embodiment model. Social Science and Medicine, 74(11), 1667–1674.

    Article  PubMed  Google Scholar 

  • Constantino, J. N., & Todd, R. D. (2000). Genetic structure of reciprocal social behavior. The American Journal of Psychiatry, 157(12), 2043–2045.

    Article  CAS  PubMed  Google Scholar 

  • Constantino, J. N., & Todd, R. D. (2003). Autistic traits in the general population: a twin study. Archives of General Psychiatry, 60(5), 524–530.

    Article  PubMed  Google Scholar 

  • Constantino, J. N., & Todd, R. D. (2005). Intergenerational transmission of subthreshold autistic traits in the general population. Biological Psychiatry, 57(6), 655–660.

    Article  PubMed  Google Scholar 

  • Coppola, A., Striano, P., Gimelli, S., Ciampa, C., Santulli, L., Caranci, F., Zuffardi, O., Gimelli, G., Striano, S., & Zara, F. (2010). A de novo 11p12-p15.4 duplication in a patient with pharmacoresistant epilepsy, mental retardation, and dysmorphisms. Brain Dev, 32(3), 248–252.

    Article  PubMed  Google Scholar 

  • Courchesne, E., Carper, R., & Akshoomoff, N. (2003). Evidence of brain overgrowth in the first year of life in autism. JAMA, 290(3), 337–344.

    Article  PubMed  Google Scholar 

  • Cox, K. H., Quinnies, K. M., Eschendroeder, A., Didrick, P. M., Eugster, E. A., & Rissman, E. F. (2015). Number of X-chromosome genes influences social behavior and vasopressin gene expression in mice. Psychoneuroendocrinology, 51, 271–281.

    Article  CAS  PubMed  Google Scholar 

  • 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. (2007). Women with autistic-spectrum disorder: magnetic resonance imaging study of brain anatomy. British Journal of Psychiatry, 191, 224–228.

    Article  PubMed  Google Scholar 

  • Creswell, C. S., & Skuse, D. H. (1999). Autism in association with Turner syndrome: genetic implications for male vulnerability to pervasive developmental disorders. Neurocase, 5(6), 511–518.

    Article  Google Scholar 

  • Cruts, M., Gijselinck, I., van der Zee, J., Engelborghs, S., Wils, H., Pirici, D., Rademakers, R., Vandenberghe, R., Dermaut, B., Martin, J. J., van Duijn, C., Peeters, K., Sciot, R., Santens, P., De Pooter, T., Mattheijssens, M., Van den Broeck, M., Cuijt, I., Vennekens, K., De Deyn, P. P., Kumar-Singh, S., & Van Broeckhoven, C. (2006). Null mutations in progranulin cause ubiquitin-positive frontotemporal dementia linked to chromosome 17q21. Nature, 442(7105), 920–924.

    Article  CAS  PubMed  Google Scholar 

  • Dai, X., Gao, Y., Xu, Z., Cui, X., Liu, J., Li, Y., Xu, H., Liu, M., Wang, Q. K., & Liu, J. Y. (2010). Identification of a novel genetic locus on chromosome 8p21.1-q11.23 for idiopathic basal ganglia calcification. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 153B(7), 1305–1310.

    Article  Google Scholar 

  • De Rubeis, S., & Buxbaum, J. D. (2015). Recent advances in the genetics of autism spectrum disorder. Current Neurology and Neuroscience Reports, 15(6), 36.

    Article  PubMed  CAS  Google Scholar 

  • De Rubeis, S., He, X., Goldberg, A. P., Poultney, C. S., Samocha, K., Cicek, A. E., Kou, Y., Liu, L., Fromer, M., Walker, S., Singh, T., Klei, L., Kosmicki, J., Shih-Chen, F., Aleksic, B., Biscaldi, M., Bolton, P. F., Brownfeld, J. M., Cai, J., Campbell, N. G., Carracedo, A., Chahrour, M. H., Chiocchetti, A. G., Coon, H., Crawford, E. L., Curran, S. R., Dawson, G., Duketis, E., Fernandez, B. A., Gallagher, L., Geller, E., Guter, S. J., Hill, R. S., Ionita-Laza, J., Jimenz Gonzalez, P., Kilpinen, H., Klauck, S. M., Kolevzon, A., Lee, I., Lei, I., Lei, J., Lehtimaki, T., Lin, C. F., Ma’ayan, A., Marshall, C. R., McInnes, A. L., Neale, B., Owen, M. J., Ozaki, N., Parellada, M., Parr, J. R., Purcell, S., Puura, K., Rajagopalan, D., Rehnstrom, K., Reichenberg, A., Sabo, A., Sachse, M., Sanders, S. J., Schafer, C., Schulte-Ruther, M., Skuse, D., Stevens, C., Szatmari, P., Tammimies, K., Valladares, O., Voran, A., Li-San, W., Weiss, L. A., Willsey, A. J., Yu, T. W., Yuen, R. K., Cook, E. H., Freitag, C. M., Gill, M., Hultman, C. M., Lehner, T., Palotie, A., Schellenberg, G. D., Sklar, P., State, M. W., Sutcliffe, J. S., Walsh, C. A., Scherer, S. W., Zwick, M. E., Barett, J. C., Cutler, D. J., Roeder, K., Devlin, B., Daly, M. J., Buxbaum, J. D., Study, DDD, Homozygosity Mapping Collaborative for, A., & Consortium, UK. (2014). Synaptic, transcriptional and chromatin genes disrupted in autism. Nature, 515(7526), 209–215.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dean, M., Kasari, C., Shih, W., Frankel, F., Whitney, R., Landa, R., Lord, C., Orlich, F., King, B., & Harwood, R. (2014). The peer relationships of girls with ASD at school: comparison to boys and girls with and without ASD. Journal of Child Psychology and Psychiatry, 55(11), 1218–1225.

    Article  PubMed  Google Scholar 

  • Dong, S., Walker, M. F., Carriero, N. J., DiCola, M., Willsey, A. J., Ye, A. Y., Waqar, Z., Gonzalez, L. E., Overton, J. D., Frahm, S., Keaney, J. F., 3rd, Teran, N. A., Dea, J., Mandell, J. D., Hus Bal, V., Sullivan, C. A., DiLullo, N. M., Khalil, R. O., Gockley, J., Yuksel, Z., Sertel, S. M., Ercan-Sencicek, A. G., Gupta, A. R., Mane, S. M., Sheldon, M., Brooks, A. I., Roeder, K., Devlin, B., State, M. W., Wei, L., & Sanders, S. J. (2014). De novo insertions and deletions of predominantly paternal origin are associated with autism spectrum disorder. Cell Reports, 9(1), 16–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Donnelly, S. L., Wolpert, C. M., Menold, M. M., Bass, M. P., Gilbert, J. R., Cuccaro, M. L., Delong, G. R., & Pericak-Vance, M. A. (2000). Female with autistic disorder and monosomy X (Turner syndrome): parent-of-origin effect of the X chromosome. American Journal of Medical Genetics, 96(3), 312–316.

    Article  CAS  PubMed  Google Scholar 

  • Dworzynski, K., Ronald, A., Bolton, P., & Happé, F. (2012). How different are girls and boys above and below the diagnostic threshold for autism spectrum disorders? Journal of the American Academy of Child and Adolescent Psychiatry, 51(8), 788–797.

    Article  PubMed  Google Scholar 

  • Egloff, M., Encha-Razavi, F., Garel, C., Bonnière-Darcy, M., Millischer, A. E., Lapierre, J. M., Fontaine, S., de Blois, M. C., Vekemans, M., Turleau, C., Ville, Y., & Malan, V. (2014). 17q21.31 microdeletion: brain anomalies leading to prenatal diagnosis. Cytogenetic and Genome Research, 144(3), 178–182.

    Article  PubMed  Google Scholar 

  • Eliot, L. (2011). The trouble with sex differences. Neuron, 72(6), 895–898.

    Article  CAS  PubMed  Google Scholar 

  • Fine, C. (2010). Delusions of gender: How our minds, society, and neurosexism create difference. New York: W. W. Norton & Company.

    Google Scholar 

  • Fombonne, E. (2002). Epidemiological trends in rates of autism. Molecular Psychiatry, 7(Suppl 2), S4–S6.

    Article  PubMed  Google Scholar 

  • Fombonne, E., Quirke, S., & Hagen, A. (2009). Prevalence and interpretation of recent trends in rates of pervasive developmental disorders. McGill Journal of Medicine, 12(2), 73.

    PubMed  PubMed Central  Google Scholar 

  • Frazier, T. W., Georgiades, S., Bishop, S. L., & Hardan, A. Y. (2014). Behavioral and cognitive characteristics of females and males with autism in the Simons simplex collection. Journal of the American Academy of Child and Adolescent Psychiatry, 53(3), 329-40.e1-3.

    Article  PubMed  Google Scholar 

  • Geschwind, D. H., & Levitt, P. (2007). Autism spectrum disorders: developmental disconnection syndromes. Current Opinion in Neurobiology, 17(1), 103–111.

    Article  CAS  PubMed  Google Scholar 

  • Giarelli, E., Wiggins, L. D., Rice, C. E., Levy, S. E., Kirby, R. S., Pinto-Martin, J., & Mandell, D. (2010). Sex differences in the evaluation and diagnosis of autism spectrum disorders among children. Disability and Health Journal, 3(2), 107–116.

    Article  PubMed  Google Scholar 

  • Giedd, J. N., Raznahan, A., Mills, K. L., & Lenroot, R. K. (2012). Review: magnetic resonance imaging of male/female differences in human adolescent brain anatomy. Biology of Sex Differences, 3(1), 19.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gillberg, C., Cederlund, M., Lamberg, K., & Zeijlon, L. (2006). Brief report: “the autism epidemic”. The registered prevalence of autism in a Swedish urban area. Journal of Autism and Developmental Disorders, 36(3), 429–435.

    Article  PubMed  Google Scholar 

  • Gilman, S. R., Iossifov, I., Levy, D., Ronemus, M., Wigler, M., & Vitkup, D. (2011). Rare de novo variants associated with autism implicate a large functional network of genes involved in formation and function of synapses. Neuron, 70(5), 898–907.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. (2007). Regional gray matter growth, sexual dimorphism, and cerebral asymmetry in the neonatal brain. Journal of Neuroscience, 27(6), 1255–1260.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gockley, J., Willsey, A. J., Dong, S., Dougherty, J. D., Constantino, J. N., & Sanders, S. J. (2015). The female protective effect in autism spectrum disorder is not mediated by a single genetic locus. Molecular Autism, 6, 25.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Goin-Kochel, R. P., Abbacchi, A., Constantino, J. N., & Consortium A.G.R.E. (2007). Lack of evidence for increased genetic loading for autism among families of affected females: a replication from family history data in two large samples. Autism, 11(3), 279–286.

    Article  PubMed  Google Scholar 

  • Gong, G., He, Y., & Evans, A. C. (2011). Brain connectivity: gender makes a difference. The Neuroscientist, 17(5), 575–591.

    Article  PubMed  Google Scholar 

  • Greenough, W. T., & Black, J. E. (1992). Induction of brain structure by experience: Substrates for cognitive development. New Jersey: Lawrence Earlbaum Associates.

    Google Scholar 

  • Hallmayer, J., Spiker, D., Lotspeich, L., McMahon, W. M., Petersen, P. B., Nicholas, P., Pingree, C., & Ciaranello, R. D. (1996). Male-to-male transmission in extended pedigrees with multiple cases of autism. American Journal of Medical Genetics, 67(1), 13–18.

    Article  CAS  PubMed  Google Scholar 

  • Hallmayer, J., Cleveland, S., Torres, A., Phillips, J., Cohen, B., Torigoe, T., Miller, J., Fedele, A., Collins, J., Smith, K., Lotspeich, L., Croen, L. A., Ozonoff, S., Lajonchere, C., Grether, J. K., & Risch, N. (2011). Genetic heritability and shared environmental factors among twin pairs with autism. Archives of General Psychiatry, 68(11), 1095–1102.

    Article  PubMed  PubMed Central  Google Scholar 

  • Handa, R. J., & Weiser, M. J. (2014). Gonadal steroid hormones and the hypothalamo-pituitary-adrenal axis. Frontiers in Neuroendocrinology, 35(2), 197–220.

    Article  CAS  PubMed  Google Scholar 

  • Hartley, S. L., & Sikora, D. M. (2009). Sex differences in autism spectrum disorder: an examination of developmental functioning, autistic symptoms, and coexisting behavior problems in toddlers. Journal of Autism and Developmental Disorders, 39(12), 1715–1722.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hattier, M. A., Matson, J. L., Tureck, K., & Horovitz, M. (2011). The effects of gender and age on repetitive and/or restricted behaviors and interests in adults with autism spectrum disorders and intellectual disability. Research in Developmental Disabilities, 32(6), 2346–2351.

    Article  PubMed  Google Scholar 

  • Head, A. M., McGillivray, J. A., & Stokes, M. A. (2014). Gender differences in emotionality and sociability in children with autism spectrum disorders. Molecular Autism, 5(1), 19.

    Article  PubMed  PubMed Central  Google Scholar 

  • Henningsson, S., Jonsson, L., Ljunggren, E., Westberg, L., Gillberg, C., Råstam, M., Anckarsäter, H., Nygren, G., Landén, M., Thuresson, K., Betancur, C., Leboyer, M., Eriksson, E., & Melke, J. (2009). Possible association between the androgen receptor gene and autism spectrum disorder. Psychoneuroendocrinology, 34(5), 752–761.

    Article  CAS  PubMed  Google Scholar 

  • Hettinger, J. A., Liu, X., Schwartz, C. E., Michaelis, R. C., & Holden, J. J. (2008). A DRD1 haplotype is associated with risk for autism spectrum disorders in male-only affected sib-pair families. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 147B(5), 628–636.

    Article  CAS  Google Scholar 

  • Hiller, R. M., Young, R. L., & Weber, N. (2014). Sex differences in autism spectrum disorder based on DSM-5 criteria: evidence from clinician and teacher reporting. Journal of Abnormal Child Psychology, 42(8), 1381–1393.

    Article  PubMed  Google Scholar 

  • Hoekstra, R. A., Bartels, M., Verweij, C. J., & Boomsma, D. I. (2007). Heritability of autistic traits in the general population. Archives of Pediatrics & Adolescent Medicine, 161(4), 372–377.

    Article  Google Scholar 

  • Holtmann, M., Bolte, S., & Poustka, F. (2007). Autism spectrum disorders: sex differences in autistic behaviour domains and coexisting psychopathology. Developmental Medicine and Child Neurology, 49, 361–366.

    Article  PubMed  Google Scholar 

  • Horiuchi, F., Oka, Y., Uno, H., Kawabe, K., Okada, F., Saito, I., Tanigawa, T., & Ueno, S. (2014). Age- and sex-related emotional and behavioral problems in children with autism spectrum disorders: comparison with control children. Psychiatry and Clinical Neurosciences, 68(7), 542–550.

    Article  PubMed  Google Scholar 

  • Hu, V.W., Sarachana, T., Sherrard, R., & Kocher, K. (2015). Investigation of sex differences in the expression of RORA and its transcriptional targets in the brain as a potential contributor to the sex bias in autism. Molecular Autism, 6(7).

  • Idring, S., Rai, D., Dal, H., Dalman, C., Sturm, H., Zander, E., Lee, B. K., Serlachius, E., & Magnusson, C. (2012). Autism spectrum disorders in the Stockholm youth cohort: design, prevalence and validity. PLoS ONE, 7(7), e41280.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ingalhalikar, M., Smith, A., Parker, D., Satterthwaite, T. D., Elliott, M. A., Ruparel, K., Hakonarson, H., Gur, R. E., Gur, R. C., & Verma, R. (2014). Sex differences in the structural connectome of the human brain. Proceedings of the National Academy of Sciences of the United States of America, 111(2), 823–828.

    Article  CAS  PubMed  Google Scholar 

  • Iossifov, I., Ronemus, M., Levy, D., Wang, Z., Hakker, I., Rosenbaum, J., Yamrom, B., Lee, Y. H., Narzisi, G., Leotta, A., Kendall, J., Grabowska, E., Ma, B., Marks, S., Rodgers, L., Stepansky, A., Troge, J., Andrews, P., Bekritsky, M., Pradhan, K., Ghiban, E., Kramer, M., Parla, J., Demeter, R., Fulton, L. L., Fulton, R. S., Magrini, V. J., Ye, K., Darnell, J. C., Darnell, R. B., Mardis, E. R., Wilson, R. K., Schatz, M. C., McCombie, W. R., & Wigler, M. (2012). De novo gene disruptions in children on the autistic spectrum. Neuron, 74(2), 285–299.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iossifov, I., O’Roak, B. J., Sanders, S. J., Ronemus, M., Krumm, N., Levy, D., Stessman, H. A., Witherspoon, K. T., Vives, L., Patterson, K. E., Smith, J. D., Paeper, B., Nickerson, D. A., Dea, J., Dong, S., Gonzalez, L. E., Mandell, J. D., Mane, S. M., Murtha, M. T., Sullivan, C. A., Walker, M. F., Waqar, Z., Wei, L., Willsey, A. J., Yamrom, B., Lee, Y. H., Grabowska, E., Dalkic, E., Wang, Z., Marks, S., Andrews, P., Leotta, A., Kendall, J., Hakker, I., Rosenbaum, J., Ma, B., Rodgers, L., Troge, J., Narzisi, G., Yoon, S., Schatz, M. C., Ye, K., McCombie, W. R., Shendure, J., Eichler, E. E., State, M. W., & Wigler, M. (2014). The contribution of de novo coding mutations to autism spectrum disorder. Nature, 515(7526), 216–221.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacquemont, S., Coe, B. P., Hersch, M., Duyzend, M. H., Krumm, N., Bergmann, S., Beckmann, J. S., Rosenfeld, J. A., & Eichler, E. E. (2014). A higher mutational burden in females supports a “female protective model” in neurodevelopmental disorders. American Journal of Human Genetics, 94(3), 415–425.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jazin, E., & Cahill, L. (2010). Sex differences in molecular neuroscience: from fruit flies to humans. Nature Review Neuroscience, 11(1), 9–17.

    Article  CAS  Google Scholar 

  • Jha, P., Sheth, D., & Ghaziuddin, M. (2007). Autism spectrum disorder and Klinefelter syndrome. European Child and Adolescent Psychiatry, 16(5), 305–308.

    Article  CAS  PubMed  Google Scholar 

  • Joel, D. (2011). Male or female? Brains are intersex. Frontiers in Integrative Neuroscience, 5, 57.

    Article  PubMed  PubMed Central  Google Scholar 

  • Keehn, B., Wagner, J. B., Tager-Flusberg, H., & Nelson, C. A. (2013). Functional connectivity in the first year of life in infants at-risk for autism: a preliminary near-infrared spectroscopy study. Frontiers in Human Neuroscience, 7, 444.

    Article  PubMed  PubMed Central  Google Scholar 

  • Keller, T. A., Kana, R. K., & Just, M. A. (2007). A developmental study of the structural integrity of white matter in autism. Neuroreport, 18(1), 23–27.

    Article  PubMed  Google Scholar 

  • Kim, J. E., O’Sullivan, M. L., Sanchez, C. A., Hwang, M., Israel, M. A., Brennand, K., Deerinck, T. J., Goldstein, L. S., Gage, F. H., Ellisman, M. H., & Ghosh, A. (2011a). Investigating synapse formation and function using human pluripotent stem cell-derived neurons. Proceedings of the National Academy of Sciences of the United States of America, 108(7), 3005–3010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim, Y. S., Leventhal, B. L., Koh, Y. J., Fombonne, E., Laska, E., Lim, E. C., Cheon, K. A., Kim, S. J., Kim, Y. K., Lee, H., Song, D. H., & Grinker, R. R. (2011b). Prevalence of autism spectrum disorders in a total population sample. The American Journal of Psychiatry, 168(9), 904–912.

    Article  PubMed  Google Scholar 

  • Kirkovski, M., Enticott, P. G., & Fitzgerald, P. B. (2013). A review of the role of female gender in autism spectrum disorders. Journal of Autism and Developmental Disorders, 43(11), 2584–2603.

    Article  PubMed  Google Scholar 

  • Klei, L., Sanders, S. J., Murtha, M. T., Hus, V., Lowe, J. K., Willsey, A. J., Moreno-De-Luca, D., Yu, T. W., Fombonne, E., Geschwind, D., Grice, D. E., Ledbetter, D. H., Lord, C., Mane, S. M., Martin, C. L., Martin, D. M., Morrow, E. M., Walsh, C. A., Melhem, N. M., Chaste, P., Sutcliffe, J. S., State, M. W., Cook, E. H., Roeder, K., & Devlin, B. (2012). Common genetic variants, acting additively, are a major source of risk for autism. Molecular Autism, 3(1), 9.

    Article  PubMed  PubMed Central  Google Scholar 

  • Knickmeyer, R. C., Wheelwright, S., & Baron-Cohen, S. B. (2008). Sex-typical play: masculinization/defeminization in girls with an autism spectrum condition. Journal of Autism and Developmental Disorders, 38(6), 1028–1035.

    Article  PubMed  Google Scholar 

  • Knickmeyer, R. C., Wang, J., Zhu, H., Geng, X., Woolson, S., Hamer, R. M., Konneker, T., Styner, M., & Gilmore, J. H. (2014). Impact of sex and gonadal steroids on neonatal brain structure. Cerebral Cortex, 24(10), 2721–2731.

    Article  PubMed  Google Scholar 

  • Kobayashi, E., Facchin, D., Steiner, C. E., Leone, A. A., Campos, N. L., Cendes, F., & Lopes-Cendes, I. (2002). Mesial temporal lobe abnormalities in a family with 15q26qter trisomy. Archives of Neurology, 59(9), 1476–1479.

    Article  PubMed  Google Scholar 

  • Koolen, D. A., Vissers, L. E., Pfundt, R., de Leeuw, N., Knight, S. J., Regan, R., Kooy, R. F., Reyniers, E., Romano, C., Fichera, M., Schinzel, A., Baumer, A., Anderlid, B. M., Schoumans, J., Knoers, N. V., van Kessel, A. G., Sistermans, E. A., Veltman, J. A., Brunner, H. G., & de Vries, B. B. (2006). A new chromosome 17q21.31 microdeletion syndrome associated with a common inversion polymorphism. Nature Genetics, 38(9), 999–1001.

    Article  CAS  PubMed  Google Scholar 

  • Kopp, S., & Gillberg, C. (2011). The Autism Spectrum Screening Questionnaire (ASSQ)-Revised Extended Version (ASSQ-REV): an instrument for better capturing the autism phenotype in girls? A preliminary study involving 191 clinical cases and community controls. Research in Developmental Disabilities, 32(6), 2875–2888.

    Article  PubMed  Google Scholar 

  • Kreiser, N. L., & White, S. W. (2014). ASD in females: are we overstating the gender difference in diagnosis? Clinical Child and Family Psychology Review, 17(1), 67–84.

    Article  PubMed  Google Scholar 

  • Kumazakia, H., Muramatsub, T., Kosakaa, H., Fujisawaa, T., Iwatac, K., Tomodaa, A., Tsuchiyad, K., & Mimurab, M. (2015). Sex differences in cognitive and symptom profiles in children with high functioning autism spectrum disorders. Research in Autism Spectrum Disorders, 13–14, 1–7.

    Article  Google Scholar 

  • Lai, M. C., Lombardo, M. V., Pasco, G., Ruigrok, A. N., Wheelwright, S. J., Sadek, S. A., Chakrabarti, B., Baron-Cohen, S., & Consortium, M. A. (2011). A behavioral comparison of male and female adults with high functioning autism spectrum conditions. PLoS ONE, 6(6), e20835.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lai, M.-C, Lombardo, M. V., Ruigrok, A. N. V., Chakrabarti, B., Wheelwright, S. J., Auyeung B., et al. (2012) Cognition in males and females with autism: similarities and differences. PLoS ONE 7(10):e47198. doi:10.1371/journal.pone.0047198

  • Lai, D. C., Tseng, Y. C., Hou, Y. M., & Guo, H. R. (2012). Gender and geographic differences in the prevalence of autism spectrum disorders in children: analysis of data from the national disability registry of Taiwan. Research in Developmental Disabilities, 33(3), 909–915.

    Article  PubMed  Google Scholar 

  • Lai, M. C., Lombardo, M. V., Suckling, J., Ruigrok, A. N., Chakrabarti, B., Ecker, C., Deoni, S. C., Craig, M. C., Murphy, D. G., Bullmore, E. T., Baron-Cohen, S., & Consortium, M.A. (2013). Biological sex affects the neurobiology of autism. Brain, 136(Pt 9), 2799–2815.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lai, M. C., Baron-Cohen, S., & Buxbaum, J. D. (2015a). Understanding autism in the light of sex/gender. Molecular Autism, 6, 24.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lai, M. C., Lombardo, M. V., Auyeung, B., Chakrabarti, B., & Baron-Cohen, S. (2015b). Sex/gender differences and autism: setting the scene for future research. Journal of the American Academy of Child and Adolescent Psychiatry, 54(1), 11–24.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lainhart, J. E., Piven, J., Wzorek, M., Landa, R., Santangelo, S. L., Coon, H., & Folstein, S. E. (1997). Macrocephaly in children and adults with autism. Journal of the American Academy of Child and Adolescent Psychiatry, 36(2), 282–290.

    Article  CAS  PubMed  Google Scholar 

  • Lamb, J. A., Barnby, G., Bonora, E., Sykes, N., Bacchelli, E., Blasi, F., Maestrini, E., Broxholme, J., Tzenova, J., Weeks, D., Bailey, A. J., Monaco, A. P., & I. M. G. S. o. A. C. (2005). Analysis of IMGSAC autism susceptibility loci: evidence for sex limited and parent of origin specific effects. Journal of Medical Genetics, 42(2), 132–137.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lenroot, R. K., & Giedd, J. N. (2010). Sex differences in the adolescent brain. Brain and Cognition, 72(1), 46–55.

    Article  PubMed  Google Scholar 

  • Lenroot, R. K., Gogtay, N., Greenstein, D. K., Wells, E. M., Wallace, G. L., Clasen, L. S., Blumenthal, J. D., Lerch, J., Zijdenbos, A. P., Evans, A. C., Thompson, P. M., & Giedd, J. N. (2007). Sexual dimorphism of brain developmental trajectories during childhood and adolescence. NeuroImage, 36(4), 1065–1073.

    Article  PubMed  PubMed Central  Google Scholar 

  • Levey, A. I., Hersch, S. M., Rye, D. B., Sunahara, R. K., Niznik, H. B., Kitt, C. A., Price, D. L., Maggio, R., Brann, M. R., & Ciliax, B. J. (1993). Localization of D1 and D2 dopamine receptors in brain with subtype-specific antibodies. Proceedings of the National Academy of Sciences of the United States of America, 90(19), 8861–8865.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levy, D., Ronemus, M., Yamrom, B., Lee, Y. H., Leotta, A., Kendall, J., Marks, S., Lakshmi, B., Pai, D., Ye, K., Buja, A., Krieger, A., Yoon, S., Troge, J., Rodgers, L., Iossifov, I., & Wigler, M. (2011). Rare de novo and transmitted copy-number variation in autistic spectrum disorders. Neuron, 70(5), 886–897.

    Article  CAS  PubMed  Google Scholar 

  • Li, N., Chen, G., Song, X., Du, W., & Zheng, X. (2011). Prevalence of autism-caused disability among Chinese children: a national population-based survey. Epilepsy and Behavior, 22(4), 786–789.

    Article  PubMed  Google Scholar 

  • Lichtenstein, P., Carlstrom, E., Rastam, M., Gillberg, C., & Anckarsater, H. (2010). The genetics of autism spectrum disorders and related neuropsychiatric disorders in childhood. The American Journal of Psychiatry, 167(11), 1357–1363.

    Article  PubMed  Google Scholar 

  • Lim, S., Naisbitt, S., Yoon, J., Hwang, J. I., Suh, P. G., Sheng, M., & Kim, E. (1999). Characterization of the Shank family of synaptic proteins. Multiple genes, alternative splicing, and differential expression in brain and development. The Journal of Biological Chemistry, 274(41), 29510–29518.

    Article  CAS  PubMed  Google Scholar 

  • Lord, C., & Schopler, E. (1985). Differences in sex ratios in autism as a function of measured intelligence. Journal of Autism and Developmental Disorders, 15(2), 185–193.

    Article  CAS  PubMed  Google Scholar 

  • Lord, C., Schopler, E., & Revicki, D. (1982). Sex differences in autism. Journal of Autism and Developmental Disorders, 12(4), 317–330.

    Article  CAS  PubMed  Google Scholar 

  • Lu, A. T., & Cantor, R. M. (2012). Allowing for sex differences increases power in a GWAS of multiplex autism families. Molecular Psychiatry, 17(2), 215–222.

    Article  CAS  PubMed  Google Scholar 

  • Luders, E., Narr, K. L., Thompson, P. M., Rex, D. E., Jancke, L., Steinmetz, H., & Toga, A. W. (2004). Gender differences in cortical complexity. Nature Neuroscience, 7(8), 799–800.

    Article  CAS  PubMed  Google Scholar 

  • Lundstrom, S., Chang, Z., Rastam, M., Gillberg, C., Larsson, H., Anckarsater, H., & Lichtenstein, P. (2012). Autism spectrum disorders and autistic like traits: similar etiology in the extreme end and the normal variation. Archives of General Psychiatry, 69(1), 46–52.

    Article  PubMed  Google Scholar 

  • Mackenzie, I. R., Baker, M., West, G., Woulfe, J., Qadi, N., Gass, J., Cannon, A., Adamson, J., Feldman, H., Lindholm, C., Melquist, S., Pettman, R., Sadovnick, A. D., Dwosh, E., Whiteheart, S. W., Hutton, M., & Pickering-Brown, S. M. (2006). A family with tau-negative frontotemporal dementia and neuronal intranuclear inclusions linked to chromosome 17. Brain, 129(Pt 4), 853–867.

    Article  PubMed  Google Scholar 

  • Majchrzak, M., & Malendowicz, L. K. (1983). Sex differences in adrenocortical structure and function. XII. Stereologic studies of rat adrenal cortex in the course of maturation. Cell and Tissue Research, 232(2), 457–469.

    Article  CAS  PubMed  Google Scholar 

  • Mandic-Maravic, V., Pejovic-Milovancevic, M., Mitkovic-Voncina, M., Kostic, M., Aleksic-Hil, O., Radosavljev-Kircanski, J., Mincic, T., & Lecic-Tosevski, D. (2015). Sex differences in autism spectrum disorders: does sex moderate the pathway from clinical symptoms to adaptive behavior? Scientific Reports, 5(10418), 1–8.

    Google Scholar 

  • Mandy, W., & Tchanturia, K. (2015). Do women with eating disorders who have social and flexibility difficulties really have autism? A case series. Molecular Autism, 6(6).

  • Mandy, W., Chilvers, R., Chowdhury, U., Salter, G., Seigal, A., & Skuse, D. (2012). Sex differences in autism spectrum disorder: evidence from a large sample of children and adolescents. Journal of Autism and Developmental Disorders, 42(7), 1304–1313.

    Article  PubMed  Google Scholar 

  • Mattila, M. L., Kielinen, M., Linna, S. L., Jussila, K., Ebeling, H., Bloigu, R., Joseph, R. M., & Moilanen, I. (2011). Autism spectrum disorders according to DSM-IV-TR and comparison with DSM-5 draft criteria: an epidemiological study. Journal of the American Academy of Child and Adolescent Psychiatry, 50(6), 583.e511–592.e511.

    Article  Google Scholar 

  • May, T., Cornish, K., & Rinehart, N.J. (2012). Gender profiles of behavioral attention in children with autism spectrum disorder. Journal of Attention Disorders.

  • May, T., Cornish, K., & Rinehart, N. (2014). Does gender matter? A one year follow-up of autistic, attention and anxiety symptoms in high-functioning children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 44(5), 1077–1086.

    Article  PubMed  Google Scholar 

  • McCarthy, M. M., & Arnold, A. P. (2011). Reframing sexual differentiation of the brain. Nature Neuroscience, 14(6), 677–683.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Messinger, D. S., Young, G. S., Webb, S. J., Ozonoff, S., Bryson, S. E., Carter, A., Carver, L., Charman, T., Chawarska, K., Curtin, S., Dobkins, K., Hertz-Picciotto, I., Hutman, T., Iverson, J. M., Landa, R., Nelson, C. A., Stone, W. L., Tager-Flusberg, H. and Zwaigenbaum, L. (2015). Early sex differences are not autism-specific: A Baby Siblings Research Consortium (BSRC) study. Molecular Autism 6, 32.

  • Miles, J. H., & Hillman, R. E. (2000). Value of a clinical morphology examination in autism. American Journal of Medical Genetics, 91(4), 245–253.

    Article  CAS  PubMed  Google Scholar 

  • Miller, M., Bales, K. L., Taylor, S. L., Yoon, J., Hostetler, C. M., Carter, C. S., & Solomon, M. (2013). Oxytocin and vasopressin in children and adolescents with autism spectrum disorders: sex differences and associations with symptoms. Autism Research, 6(2), 91–102.

    Article  PubMed  PubMed Central  Google Scholar 

  • Money, K. M., & Stanwood, G. D. (2013). Developmental origins of brain disorders: roles for dopamine. Frontiers in Cellular Neuroscience, 7, 260.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Montiel-Nava, C., & Peña, J. A. (2008). Epidemiological findings of pervasive developmental disorders in a Venezuelan study. Autism, 12(2), 191–202.

    Article  PubMed  Google Scholar 

  • Mukamel, Z., Konopka, G., Wexler, E., Osborn, G. E., Dong, H., Bergman, M. Y., Levitt, P., & Geschwind, D. H. (2011). Regulation of MET by FOXP2, genes implicated in higher cognitive dysfunction and autism risk. Journal of Neuroscience, 31(32), 11437–11442.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nava, C., Lamari, F., Heron, D., Mignot, C., Rastetter, A., Keren, B., Cohen, D., Faudet, A., Bouteiller, D., Gilleron, M., Jacquette, A., Whalen, S., Afenjar, A., Perisse, D., Laurent, C., Dupuits, C., Gautier, C., Gerard, M., Huguet, G., Caillet, S., Leheup, B., Leboyer, M., Gillberg, C., Delorme, R., Bourgeron, T., Brice, A., & Depienne, C. (2012). Analysis of the chromosome X exome in patients with autism spectrum disorders identified novel candidate genes, including TMLHE. Transcultural Psychiatry, 2, e179.

    Article  CAS  Google Scholar 

  • Neale, B. M., Kou, Y., Liu, L., Ma’ayan, A., Samocha, K. E., Sabo, A., Lin, C. F., Stevens, C., Wang, L. S., Makarov, V., Polak, P., Yoon, S., Maguire, J., Crawford, E. L., Campbell, N. G., Geller, E. T., Valladares, O., Schafer, C., Liu, H., Zhao, T., Cai, G., Lihm, J., Dannenfelser, R., Jabado, O., Peralta, Z., Nagaswamy, U., Muzny, D., Reid, J. G., Newsham, I., Wu, Y., Lewis, L., Han, Y., Voight, B. F., Lim, E., Rossin, E., Kirby, A., Flannick, J., Fromer, M., Shakir, K., Fennell, T., Garimella, K., Banks, E., Poplin, R., Gabriel, S., DePristo, M., Wimbish, J. R., Boone, B. E., Levy, S. E., Betancur, C., Sunyaev, S., Boerwinkle, E., Buxbaum, J. D., Cook, E. H., Jr., Devlin, B., Gibbs, R. A., Roeder, K., Schellenberg, G. D., Sutcliffe, J. S., & Daly, M. J. (2012). Patterns and rates of exonic de novo mutations in autism spectrum disorders. Nature, 485(7397), 242–245.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • NEDSAC (2013). Estimated prevalence of autism spectrum disorders among children 2–14 years of age in three Canadian regions (2003–2010). Kingston, Ontario, Canada.

  • Nelson, C. A. (2014). Commentary: becoming social--a commentary on Happé & Frith (2014). Journal of Child Psychology and Psychiatry, 55(6), 578–581.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen, C., & Ronald, A. (2014). How do girls with low functioning autism compare to boys with autism and typically developing girls with regard to behavior, cognition, and psychopathology? Scandinavian Journal of Child and Adolescent Psychiatry and Psychology, 2(2), 55–65.

    Article  Google Scholar 

  • Nordahl, C. W., Iosif, A. M., Young, G. S., Perry, L. M., Dougherty, R., Lee, A., Li, D., Buonocore, M. H., Simon, T., Rogers, S., Wandell, B., & Amaral, D. G. (2015). Sex differences in the corpus callosum in preschool-aged children with autism spectrum disorder. Molecular Autism, 6, 26.

    Article  PubMed  PubMed Central  Google Scholar 

  • O’Roak, B. J., Vives, L., Girirajan, S., Karakoc, E., Krumm, N., Coe, B. P., Levy, R., Ko, A., Lee, C., Smith, J. D., Turner, E. H., Stanaway, I. B., Vernot, B., Malig, M., Baker, C., Reilly, B., Akey, J. M., Borenstein, E., Rieder, M. J., Nickerson, D. A., Bernier, R., Shendure, J., & Eichler, E. E. (2012). Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations. Nature, 485(7397), 246–250.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ozonoff, S., Young, G. S., Carter, A., Messinger, D., Yirmiya, N., Zwaigenbaum, L., Bryson, S., Carver, L. J., Constantino, J. N., Dobkins, K., Hutman, T., Iverson, J. M., Landa, R., Rogers, S. J., Sigman, M., & Stone, W. L. (2011). Recurrence risk for autism spectrum disorders: a baby siblings research consortium study. Pediatrics, 128(3), e488–e495.

    PubMed  PubMed Central  Google Scholar 

  • Pelphrey, K. A., Yang, D. Y., & McPartland, J. C. (2014). Building a social neuroscience of autism spectrum disorder. Current Topics in Behavioral Neurosciences, 16, 215–233.

    Article  PubMed  Google Scholar 

  • Peper, J. S., Hulshoff Pol, H. E., Crone, E. A., & van Honk, J. (2011). Sex steroids and brain structure in pubertal boys and girls: a mini-review of neuroimaging studies. Neuroscience, 191, 28–37.

    Article  CAS  PubMed  Google Scholar 

  • Philippi, A., Tores, F., Carayol, J., Rousseau, F., Letexier, M., Roschmann, E., Lindenbaum, P., Benajjou, A., Fontaine, K., Vazart, C., Gesnouin, P., Brooks, P., & Hager, J. (2007). Association of autism with polymorphisms in the paired-like homeodomain transcription factor 1 (PITX1) on chromosome 5q31: a candidate gene analysis. BMC Medical Genetics, 8, 74.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pickles, A., Starr, E., Kazak, S., Bolton, P., Papanikolaou, K., Bailey, A., Goodman, R., & Rutter, M. (2000). Variable expression of the autism broader phenotype: findings from extended pedigrees. Journal of Child Psychology and Psychiatry, 41(4), 491–502.

    Article  CAS  PubMed  Google Scholar 

  • Pilowsky, T., Yirmiya, N., Shulman, C., & Dover, R. (1998). The autism diagnostic interview-revised and the childhood autism rating scale: differences between diagnostic systems and comparison between genders. Journal of Autism and Developmental Disorders, 28(2), 143–151.

    Article  CAS  PubMed  Google Scholar 

  • Pisula, E., Kawa, R., Szostakiewicz, Ł., Łucka, I., Kawa, M., & Rynkiewicz, A. (2013). Autistic traits in male and female students and individuals with high functioning autism spectrum disorders measured by the Polish version of the autism-spectrum quotient. PLoS ONE, 8(9), e75236.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piven, J., Arndt, S., Bailey, J., & Andreasen, N. (1996). Regional brain enlargement in autism: a magnetic resonance imaging study. Journal of the American Academy of Child and Adolescent Psychiatry, 35(4), 530–536.

    Article  CAS  PubMed  Google Scholar 

  • Plummer, J. T., Evgrafov, O. V., Bergman, M. Y., Friez, M., Haiman, C. A., Levitt, P., & Aldinger, K. A. (2013). Transcriptional regulation of the MET receptor tyrosine kinase gene by MeCP2 and sex-specific expression in autism and Rett syndrome. Transcultural Psychiatry, 3, e316.

    Article  CAS  Google Scholar 

  • Posthuma, D., & Polderman, T. J. (2013). What have we learned from recent twin studies about the etiology of neurodevelopmental disorders? Current Opinion in Neurology, 26(2), 111–121.

    Article  PubMed  Google Scholar 

  • Redcay, E., & Courchesne, E. (2005). When is the brain enlarged in autism? A meta-analysis of all brain size reports. Biological Psychiatry, 58(1), 1–9.

    Article  PubMed  Google Scholar 

  • Reinhardt, V. P., Wetherby, A. M., Schatschneider, C., & Lord, C. (2015). Examination of sex differences in a large sample of young children with autism spectrum disorder and typical development. Journal of Autism and Developmental Disorders, 45(3), 697–706.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ritvo, E. R., Freeman, B. J., Mason-Brothers, A., Mo, A., & Ritvo, A. M. (1985). Concordance for the syndrome of autism in 40 pairs of afflicted twins. The American Journal of Psychiatry, 142(1), 74–77.

    Article  CAS  PubMed  Google Scholar 

  • Rivet, T. T., & Matson, J. L. (2011). Review of gender differences in core symptomatology in autism spectrum disorders. Research in Autism Spectrum Disorders, 5(3), 957–976.

    Article  Google Scholar 

  • Robinson, E. B., Koenen, K. C., McCormick, M. C., Munir, K., Hallett, V., Happe, F., Plomin, R., & Ronald, A. (2012). A multivariate twin study of autistic traits in 12-year-olds: testing the fractionable autism triad hypothesis. Behavior Genetics, 42(2), 245–255.

    Article  PubMed  Google Scholar 

  • Robinson, E. B., Lichtenstein, P., Anckarsäter, H., Happé, F., & Ronald, A. (2013). Examining and interpreting the female protective effect against autistic behavior. Proceedings of the National Academy of Sciences of the United States of America, 110(13), 5258–5262.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ronald, A., & Hoekstra, R. A. (2011). Autism spectrum disorders and autistic traits: a decade of new twin studies. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 156B(3), 255–274.

    Article  Google Scholar 

  • Ronald, A., Happe, F., & Plomin, R. (2005). The genetic relationship between individual differences in social and nonsocial behaviours characteristic of autism. Developmental Science, 8(5), 444–458.

    Article  PubMed  Google Scholar 

  • Ronald, A., Happe, F., Bolton, P., Butcher, L. M., Price, T. S., Wheelwright, S., Baron-Cohen, S., & Plomin, R. (2006). Genetic heterogeneity between the three components of the autism spectrum: a twin study. Journal of the American Academy of Child and Adolescent Psychiatry, 45(6), 691–699.

    Article  PubMed  Google Scholar 

  • Rosenberg, R. E., Law, J. K., Yenokyan, G., McGready, J., Kaufmann, W. E., & Law, P. A. (2009). Characteristics and concordance of autism spectrum disorders among 277 twin pairs. Archives of Pediatrics & Adolescent Medicine, 163(10), 907–914.

    Article  Google Scholar 

  • Ross, J. L., Roeltgen, D. P., Kushner, H., Zinn, A. R., Reiss, A., Bardsley, M. Z., McCauley, E., & Tartaglia, N. (2012). Behavioral and social phenotypes in boys with 47, XYY syndrome or 47, XXY Klinefelter syndrome. Pediatrics, 129(4), 769–778.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rudie, J. D., & Dapretto, M. (2013). Convergent evidence of brain overconnectivity in children with autism? Cell Reports, 5(3), 565–566.

    Article  CAS  PubMed  Google Scholar 

  • Rudie, J. D., Hernandez, L. M., Brown, J. A., Beck-Pancer, D., Colich, N. L., Gorrindo, P., Thompson, P. M., Geschwind, D. H., Bookheimer, S. Y., Levitt, P., & Dapretto, M. (2012). Autism-associated promoter variant in MET impacts functional and structural brain networks. Neuron, 75(5), 904–915.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sajan, S. A., Fernandez, L., Nieh, S. E., Rider, E., Bukshpun, P., Wakahiro, M., Christian, S. L., Rivière, J. B., Sullivan, C. T., Sudi, J., Herriges, M. J., Paciorkowski, A. R., Barkovich, A. J., Glessner, J. T., Millen, K. J., Hakonarson, H., Dobyns, W. B., & Sherr, E. H. (2013). Both rare and de novo copy number variants are prevalent in agenesis of the corpus callosum but not in cerebellar hypoplasia or polymicrogyria. PLoS Genetics, 9(10), e1003823.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Samadi, S. A., Mahmoodizadeh, A., & McConkey, R. (2012). A national study of the prevalence of autism among five-year-old children in Iran. Autism, 16(1), 5–14.

    Article  PubMed  Google Scholar 

  • Sanders, S. J., Murtha, M. T., Gupta, A. R., Murdoch, J. D., Raubeson, M. J., Willsey, A. J., Ercan-Sencicek, A. G., DiLullo, N. M., Parikshak, N. N., Stein, J. L., Walker, M. F., Ober, G. T., Teran, N. A., Song, Y., El-Fishawy, P., Murtha, R. C., Choi, M., Overton, J. D., Bjornson, R. D., Carriero, N. J., Meyer, K. A., Bilguvar, K., Mane, S. M., Sestan, N., Lifton, R. P., Günel, M., Roeder, K., Geschwind, D. H., Devlin, B., & State, M. W. (2012). De novo mutations revealed by whole-exome sequencing are strongly associated with autism. Nature, 485(7397), 237–241.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarachana, T., Xu, M., Wu, R. C., & Hu, V. W. (2011). Sex hormones in autism: androgens and estrogens differentially and reciprocally regulate RORA, a novel candidate gene for autism. PLoS ONE, 6(2), e17116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato, D., Lionel, A. C., Leblond, C. S., Prasad, A., Pinto, D., Walker, S., O’Connor, I., Russell, C., Drmic, I. E., Hamdan, F. F., Michaud, J. L., Endris, V., Roeth, R., Delorme, R., Huguet, G., Leboyer, M., Rastam, M., Gillberg, C., Lathrop, M., Stavropoulos, D. J., Anagnostou, E., Weksberg, R., Fombonne, E., Zwaigenbaum, L., Fernandez, B. A., Roberts, W., Rappold, G. A., Marshall, C. R., Bourgeron, T., Szatmari, P., & Scherer, S. W. (2012). SHANK1 deletions in males with autism spectrum disorder. American Journal of Human Genetics, 90(5), 879–887.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schaafsma, S. M., & Pfaff, D. W. (2014). Etiologies underlying sex differences in autism spectrum disorders. Frontiers in Neuroendocrinology, 35(3), 255–271.

    Article  PubMed  Google Scholar 

  • Schellenberg, G.D., Dawson, G., Sung, Y.J., Estes, A., Munson, J., Rosenthal, E., Rothstein, J., Flodman, P., Smith, M., Coon, H., Leong, L., Yu, C.E., Stodgell, C., Rodier, P.M., Spence, M.A., Minshew, N., McMahon, W.M., & Wijsman, E.M. (2006). Evidence for multiple loci from a genome scan of autism kindreds. Molecular Psychiatry, 11(11), 1049–1060, 1979.

  • 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. (2010). Longitudinal magnetic resonance imaging study of cortical development through early childhood in autism. Journal of Neuroscience, 30(12), 4419–4427.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scourfield, J., Martin, N., Lewis, G., & McGuffin, P. (1999). Heritability of social cognitive skills in children and adolescents. British Journal of Psychiatry, 175, 559–564.

    Article  CAS  PubMed  Google Scholar 

  • Sebat, J., Lakshmi, B., Malhotra, D., Troge, J., Lese-Martin, C., Walsh, T., Yamrom, B., Yoon, S., Krasnitz, A., Kendall, J., Leotta, A., Pai, D., Zhang, R., Lee, Y. H., Hicks, J., Spence, S. J., Lee, A. T., Puura, K., Lehtimäki, T., Ledbetter, D., Gregersen, P. K., Bregman, J., Sutcliffe, J. S., Jobanputra, V., Chung, W., Warburton, D., King, M. C., Skuse, D., Geschwind, D. H., Gilliam, T. C., Ye, K., & Wigler, M. (2007). Strong association of de novo copy number mutations with autism. Science, 316(5823), 445–449.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheen, V. L., Wheless, J. W., Bodell, A., Braverman, E., Cotter, P. D., Rauen, K. A., Glenn, O., Weisiger, K., Packman, S., Walsh, C. A., & Sherr, E. H. (2003). Periventricular heterotopia associated with chromosome 5p anomalies. Neurology, 60(6), 1033–1036.

    Article  CAS  PubMed  Google Scholar 

  • Sipes, M., Matson, J. L., Worley, J. A., & Kozlowski, A. M. (2011). Gender differences in symptoms of autism spectrum disorders in toddlers. Research in Autism Spectrum Disorders, 5(4), 1465–1470.

    Article  Google Scholar 

  • Sisk, C. L., & Zehr, J. L. (2005). Pubertal hormones organize the adolescent brain and behavior. Frontiers in Neuroendocrinology, 26(3–4), 163–174.

    Article  CAS  PubMed  Google Scholar 

  • Skuse, D. H., James, R. S., Bishop, D. V., Coppin, B., Dalton, P., Aamodt-Leeper, G., Bacarese-Hamilton, M., Creswell, C., McGurk, R., & Jacobs, P. A. (1997). Evidence from Turner’s syndrome of an imprinted X-linked locus affecting cognitive function. Nature, 387(6634), 705–708.

    Article  CAS  PubMed  Google Scholar 

  • Skuse, D. H., Mandy, W. P., & Scourfield, J. (2005). Measuring autistic traits: heritability, reliability and validity of the social and communication disorders checklist. British Journal of Psychiatry, 187, 568–572.

    Article  PubMed  Google Scholar 

  • Solomon, M., Miller, M., Taylor, S. L., Hinshaw, S. P., & Carter, C. S. (2012). Autism symptoms and internalizing psychopathology in girls and boys with autism spectrum disorders. Journal of Autism and Developmental Disorders, 42(1), 48–59.

    Article  PubMed  Google Scholar 

  • 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. (2002). Brain structural abnormalities in young children with autism spectrum disorder. Neurology, 59(2), 184–192.

    Article  CAS  PubMed  Google Scholar 

  • Stacy, M. E., Zablotsky, B., Yarger, H. A., Zimmerman, A., Makia, B., & Lee, L. C. (2014). Sex differences in co-occurring conditions of children with autism spectrum disorders. Autism, 18(8), 965–974.

    Article  PubMed  Google Scholar 

  • Steffenburg, S., Gillberg, C., Hellgren, L., Andersson, L., Gillberg, I. C., Jakobsson, G., & Bohman, M. (1989). A twin study of autism in Denmark, Finland, Iceland, Norway and Sweden. Journal of Child Psychology and Psychiatry, 30(3), 405–416.

    Article  CAS  PubMed  Google Scholar 

  • Stone, J. L., Merriman, B., Cantor, R. M., Yonan, A. L., Gilliam, T. C., Geschwind, D. H., & Nelson, S. F. (2004). Evidence for sex-specific risk alleles in autism spectrum disorder. American Journal of Human Genetics, 75(6), 1117–1123.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szatmari, P., Paterson, A. D., Zwaigenbaum, L., Roberts, W., Brian, J., Liu, X. Q., Vincent, J. B., Skaug, J. L., Thompson, A. P., Senman, L., Feuk, L., Qian, C., Bryson, S. E., Jones, M. B., Marshall, C. R., Scherer, S. W., Vieland, V. J., Bartlett, C., Mangin, L. V., Goedken, R., Segre, A., Pericak-Vance, M. A., Cuccaro, M. L., Gilbert, J. R., Wright, H. H., Abramson, R. K., Betancur, C., Bourgeron, T., Gillberg, C., Leboyer, M., Buxbaum, J. D., Davis, K. L., Hollander, E., Silverman, J. M., Hallmayer, J., Lotspeich, L., Sutcliffe, J. S., Haines, J. L., Folstein, S. E., Piven, J., Wassink, T. H., Sheffield, V., Geschwind, D. H., Bucan, M., Brown, W. T., Cantor, R. M., Constantino, J. N., Gilliam, T. C., Herbert, M., Lajonchere, C., Ledbetter, D. H., Lese-Martin, C., Miller, J., Nelson, S., Samango-Sprouse, C. A., Spence, S., State, M., Tanzi, R. E., Coon, H., Dawson, G., Devlin, B., Estes, A., Flodman, P., Klei, L., McMahon, W. M., Minshew, N., Munson, J., Korvatska, E., Rodier, P. M., Schellenberg, G. D., Smith, M., Spence, M. A., Stodgell, C., Tepper, P. G., Wijsman, E. M., Yu, C. E., Rogé, B., Mantoulan, C., Wittemeyer, K., Poustka, A., Felder, B., Klauck, S. M., Schuster, C., Poustka, F., Bölte, S., Feineis-Matthews, S., Herbrecht, E., Schmötzer, G., Tsiantis, J., Papanikolaou, K., Maestrini, E., Bacchelli, E., Blasi, F., Carone, S., Toma, C., Van Engeland, H., de Jonge, M., Kemner, C., Koop, F., Langemeijer, M., Hijmans, C., Hijimans, C., Staal, W. G., Baird, G., Bolton, P. F., Rutter, M. L., Weisblatt, E., Green, J., Aldred, C., Wilkinson, J. A., Pickles, A., Le Couteur, A., Berney, T., McConachie, H., Bailey, A. J., Francis, K., Honeyman, G., Hutchinson, A., Parr, J. R., Wallace, S., Monaco, A. P., Barnby, G., Kobayashi, K., Lamb, J. A., Sousa, I., Sykes, N., Cook, E. H., Guter, S. J., Leventhal, B. L., Salt, J., Lord, C., Corsello, C., Hus, V., Weeks, D. E., Volkmar, F., Tauber, M., Fombonne, E., Shih, A., Meyer, K. J., & Consortium, A. G. P. (2007). Mapping autism risk loci using genetic linkage and chromosomal rearrangements. Nature Genetics, 39(3), 319–328.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szatmari, P., Liu, X. Q., Goldberg, J., Zwaigenbaum, L., Paterson, A. D., Woodbury-Smith, M., Georgiades, S., Duku, E., & Thompson, A. (2012). Sex differences in repetitive stereotyped behaviors in autism: implications for genetic liability. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 159B(1), 5–12.

    Article  PubMed  Google Scholar 

  • Taniai, H., Nishiyama, T., Miyachi, T., Imaeda, M., & Sumi, S. (2008). Genetic influences on the broad spectrum of autism: study of proband-ascertained twins. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 147B(6), 844–849.

    Article  Google Scholar 

  • Taylor, B., Jick, H., & Maclaughlin, D. (2013). Prevalence and incidence rates of autism in the UK: time trend from 2004 to 2010 in children aged 8 years. BMJ Open, 3(10), e003219.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tepest, R., Jacobi, E., Gawronski, A., Krug, B., Möller-Hartmann, W., Lehnhardt, F. G., & Vogeley, K. (2010). Corpus callosum size in adults with high-functioning autism and the relevance of gender. Psychiatry Research, 183(1), 38–43.

    Article  PubMed  Google Scholar 

  • Thomas, N. S., Sharp, A. J., Browne, C. E., Skuse, D., Hardie, C., & Dennis, N. R. (1999). Xp deletions associated with autism in three females. Human Genetics, 104(1), 43–48.

    Article  CAS  PubMed  Google Scholar 

  • Tsai, L. Y., & Beisler, J. M. (1983). The development of sex differences in infantile autism. British Journal of Psychiatry, 142, 373–378.

    Article  CAS  PubMed  Google Scholar 

  • Tsai, L., Stewart, M. A., & August, G. (1981). Implication of sex differences in the familial transmission of infantile autism. Journal of Autism and Developmental Disorders, 11(2), 165–173.

    Article  CAS  PubMed  Google Scholar 

  • van Rijn, S., Bierman, M., Bruining, H., & Swaab, H. (2012). Vulnerability for autism traits in boys and men with an extra X chromosome (47, XXY): the mediating role of cognitive flexibility. Journal of Psychiatric Research, 46(10), 1300–1306.

    Article  PubMed  Google Scholar 

  • van Steensel, M. A., Vreeburg, M., Engelen, J., Ghesquiere, S., Stegmann, A. P., Herbergs, J., van Lent, J., Smeets, B., & Vles, J. H. (2008). Contiguous gene syndrome due to a maternally inherited 8.41 Mb distal deletion of chromosome band Xp22.3 in a boy with short stature, ichthyosis, epilepsy, mental retardation, cerebral cortical heterotopias and Dandy-Walker malformation. American Journal of Medical Genetics Part A, 146A(22), 2944–2949.

    Article  PubMed  Google Scholar 

  • Van Wijngaarden-Cremers, P. J., van Eeten, E., Groen, W. B., Van Deurzen, P. A., Oosterling, I. J., & Van der Gaag, R. J. (2014). Gender and age differences in the core triad of impairments in autism spectrum disorders: a systematic review and meta-analysis. Journal of Autism and Developmental Disorders, 44(3), 627–635.

    Article  PubMed  Google Scholar 

  • Verma, D., Chakraborti, B., Karmakar, A., Bandyopadhyay, T., Singh, A. S., Sinha, S., Chatterjee, A., Ghosh, S., Mohanakumar, K. P., Mukhopadhyay, K., & Rajamma, U. (2014). Sexual dimorphic effect in the genetic association of monoamine oxidase A (MAOA) markers with autism spectrum disorder. Progress in Neuropsychopharmacology and Biological Psychiatry, 50, 11–20.

    Article  CAS  Google Scholar 

  • Volkmar, F. R., Szatmari, P., & Sparrow, S. S. (1993). Sex differences in pervasive developmental disorders. Journal of Autism and Developmental Disorders, 23(4), 579–591.

    Article  CAS  PubMed  Google Scholar 

  • Weiss, L. (2011). Fair representation for the fairer sex in autism research. Simons Foundation Spectrum Newsletter, (https://spectrumnews.org/opinion/viewpoint/fair-representation-forthe-fairer-sex-in-autism-research/). Accessed 16 Aug 2011.

  • Werling, D. M., & Geschwind, D. H. (2013a). Sex differences in autism spectrum disorders. Current Opinion in Neurology, 26(2), 146–153.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Werling, D. M., & Geschwind, D. H. (2013b). Understanding sex bias in autism spectrum disorder. Proceedings of the National Academy of Sciences of the United States of America, 110(13), 4868–4869.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Werling, D. M., & Geschwind, D. H. (2015). Recurrence rates provide evidence for sex-differential, familial genetic liability for autism spectrum disorders in multiplex families and twins. Molecular Autism, 6, 27.

    Article  PubMed  PubMed Central  Google Scholar 

  • Werling, D. M., Lowe, J. K., Luo, R., Cantor, R. M., & Geschwind, D. H. (2014). Replication of linkage at chromosome 20p13 and identification of suggestive sex-differential risk loci for autism spectrum disorder. Molecular Autism, 5(1), 13.

    Article  PubMed  PubMed Central  Google Scholar 

  • Worley, J. A., & Matson, J. L. (2011). Psychiatric symptoms in children diagnosed with an autism spectrum disorder: an examination of gender differences. Research in Autism Spectrum Disorders, 5(3), 1086–1091.

    Article  Google Scholar 

  • Yeargin-Allsopp, M., Rice, C., Karapurkar, T., Doernberg, N., Boyle, C., & Murphy, C. (2003). Prevalence of autism in a US metropolitan area. JAMA, 289(1), 49–55.

    Article  PubMed  Google Scholar 

  • Yu, J., He, X., Yao, D., Li, Z., Li, H., & Zhao, Z. (2011). A sex-specific association of common variants of neuroligin genes (NLGN3 and NLGN4X) with autism spectrum disorders in a Chinese Han cohort. Behavioral and Brain Functions, 7, 13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zettergren, A., Jonsson, L., Johansson, D., Melke, J., Lundström, S., Anckarsäter, H., Lichtenstein, P., & Westberg, L. (2013). Associations between polymorphisms in sex steroid related genes and autistic-like traits. Psychoneuroendocrinology, 38(11), 2575–2584.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, X., Leotta, A., Kustanovich, V., Lajonchere, C., Geschwind, D. H., Law, K., Law, P., Qiu, S., Lord, C., Sebat, J., Ye, K., & Wigler, M. (2007). A unified genetic theory for sporadic and inherited autism. Proceedings of the National Academy of Sciences of the United States of America, 104(31), 12831–12836.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ziats, M. N., & Rennert, O. M. (2013). Sex-biased gene expression in the developing brain: implications for autism spectrum disorders. Molecular Autism, 4(1), 10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zwaigenbaum, L., Bryson, S. E., Szatmari, P., Brian, J., Smith, I. M., Roberts, W., Vaillancourt, T., & Roncadin, C. (2012). Sex differences in children with autism spectrum disorder identified within a high-risk infant cohort. Journal of Autism and Developmental Disorders, 42(12), 2585–2596.

    Article  PubMed  Google Scholar 

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Acknowledgments

This research for and preparation of this article was performed with the support from the National Institutes of Mental Health (grant #5R01MH100028-03; sub-award, JDVH). The authors wish to thank Dr. Elizabeth Aylward of the Seattle Children’s Research Institute for constructive comments on an earlier draft of this article. We also acknowledge the members of the USC Mark and Mary Stevens Neuroimaging and Informatics Institute.

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  1. Neuroscience Graduate Program, University of Southern California, Los Angeles, CA, USA

    Christina Chen

  2. USC Mark and Mary Stevens Neuroimaging and Informatics Institute and Laboratory of Neuro Imaging, Keck School of Medicine of USC, University of Southern California, 2001 North Soto Street – SSB1-Room 102, Los Angeles, CA, 90032, USA

    John Darrell Van Horn

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Chen, C., Van Horn, J.D. & GENDAAR Research Consortium. Developmental neurogenetics and multimodal neuroimaging of sex differences in autism. Brain Imaging and Behavior 11, 38–61 (2017). https://doi.org/10.1007/s11682-015-9504-3

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