Convergence of Sex Differences and the Neuroimmune System in Autism Spectrum Disorder

Biological Psychiatry

Volumn 81, Issue 5, 2017, Pages 402-410

  McCarthy, Margaret M ^a   Wright, Christopher L ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Androgens; Autism spectrum disorder; Cerebellum; Estrogens; Masculinization; Microglia; Preoptic area; Prostaglandins

Indexed keywords

PROSTAGLANDIN E2;

ASTROCYTE; AUTISM; BOY; BRAIN DEVELOPMENT; BRAIN REGION; CEREBELLUM; GIRL; HUMAN; INNATE IMMUNITY; MICROGLIA; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SEX DIFFERENCE; SOCIAL BEHAVIOR; ANIMAL; ANIMAL BEHAVIOR; BRAIN; DISEASE MODEL; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; IMMUNOMODULATION; INFLAMMATION; MALE; METABOLISM; MOUSE; RAT; SEX DIFFERENTIATION; SEXUAL DEVELOPMENT;

ANIMALS; ASTROCYTES; AUTISM SPECTRUM DISORDER; BEHAVIOR, ANIMAL; BRAIN; CEREBELLUM; DINOPROSTONE; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; IMMUNITY, INNATE; INFLAMMATION; MALE; MICE; MICROGLIA; NEUROIMMUNOMODULATION; PREOPTIC AREA; RATS; RISK FACTORS; SEX CHARACTERISTICS; SEX DIFFERENTIATION; SEX FACTORS;

EID: 85007013718     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2016.10.004     Document Type: Review

References (110)

1. 1 Jacquemont, S., Coe, B.P., Hersch, M., Duyzend, M.H., Krumm, N., Bergmann, S., et al. A higher mutational burden in females supports a “female protective model” in neurodevelopmental disorders. Am J Human Genet 94 (2014), 415–425.
2. 2 Robinson, E.B., Lichtenstein, P., Anckarsater, H., Happe, F., Ronald, A., Examining and interpreting the female protective effect against autistic behavior. Proc Natl Acad Sci U S A 110 (2013), 5258–5262.
3. 3 Lai, M.C., Lombardo, M.V., Auyeung, B., Chakrabarti, B., Baron-Cohen, S., Sex/gender differences and autism: Setting the scene for future research. J Am Acad Child Adolesc Psychiatry 54 (2015), 11–24.
4. 4 Halladay, A.K., Bishop, S., Constantino, J.N., Daniels, A.M., Koenig, K., Palmer, K., et al. Sex and gender differences in autism spectrum disorder: Summarizing evidence gaps and identifying emerging areas of priority. Mol Autism, 6, 2015, 36.
5. 5 Gockley, J., Willsey, A.J., Dong, S., Dougherty, J.D., Constantino, J.N., Sanders, S.J., The female protective effect in autism spectrum disorder is not mediated by a single genetic locus. Mol Autism, 6, 2015, 25.
6. 6 Auyeung, B., Baron-Cohen, S., Ashwin, E., Knickmeyer, R., Taylor, K., Hackett, G., Fetal testosterone and autistic traits. Br J Psychol 100 (2009), 1–22.
7. 7 Rynkiewicz, A., Schuller, B., Marchi, E., Piana, S., Camurri, A., Lassalle, A., et al. An investigation of the ‘female camouflage effect׳ in autism using a computerized ADOS-2 and a test of sex/gender differences. Mol Autism, 7, 2016, 10.
8. 8 Cohly, H.H., Panja, A., Immunological findings in autism. Int Rev Neurobiol 71 (2005), 317–341.
9. 9 Masi, A., Quintana, D.S., Glozier, N., Lloyd, A.R., Hickie, I.B., Guastella, A.J., Cytokine aberrations in autism spectrum disorder: A systematic review and meta-analysis. Mol Psychiatry 20 (2015), 440–446.
10. 10 Patterson, P.H., Maternal infection and immune involvement in autism. Trends Mol Med 17 (2011), 389–394.
11. 11 Vargas, D.L., Nascimbene, C., Krishnan, C., Zimmerman, A.W., Pardo, C.A., Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol 57 (2005), 67–81.
12. 12 Zimmerman, A.W., Jyonouchi, H., Comi, A.M., Connors, S.L., Milstien, S., Varsou, A., et al. Cerebrospinal fluid and serum markers of inflammation in autism. Pediatr Neurol 33 (2005), 195–201.
13. 13 Sanders, S.J., He, X., Willsey, A.J., Ercan-Sencicek, A.G., Samocha, K.E., Cicek, A.E., et al. Insights into autism spectrum disorder genomic architecture and biology from 71 risk loci. Neuron 87 (2015), 1215–1233.
14. 14 De Rubeis, S., He, X., Goldberg, A.P., Poultney, C.S., Samocha, K., Cicek, A.E., et al. Synaptic, transcriptional and chromatin genes disrupted in autism. Nature 515 (2014), 209–215.
15. 15 Iossifov, I., O'Roak, B.J., Sanders, S.J., Ronemus, M., Krumm, N., Levy, D., et al. The contribution of de novo coding mutations to autism spectrum disorder. Nature 515 (2014), 216–221.
16. 16 Chaste, P., Klei, L., Sanders, S.J., Hus, V., Murtha, M.T., Lowe, J.K., et al. A genome-wide association study of autism using the Simons Simplex Collection: Does reducing phenotypic heterogeneity in autism increase genetic homogeneity?. Biol Psychiatry 77 (2014), 775–784.
17. 17 Taniai, H., Nishiyama, T., Miyachi, T., Imaeda, M., Sumi, S., Genetic influences on the broad spectrum of autism: Study of proband-ascertained twins. Am J Med Genet B 147B (2008), 844–849.
18. 18 Lanz, T.A., Guilmette, E., Gosink, M.M., Fischer, J.E., Fitzgerald, L.W., Stephenson, D.T., et al. Transcriptomic analysis of genetically defined autism candidate genes reveals common mechanisms of action. Mol Autism, 4, 2013, 45.
19. 19 Mullins, C., Fishell, G., Tsien, R.W., Unifying views of autism spectrum disorders: A consideration of autoregulatory feedback loops. Neuron 89 (2016), 1131–1156.
20. 20 Jiang, H.Y., Xu, L.L., Shao, L., Xia, R.M., Yu, Z.H., Ling, Z.X., et al. Maternal infection during pregnancy and risk of autism spectrum disorders: A systematic review and meta-analysis. Brain Behav Immun 58 (2016), 165–172.
21. 21 McCarthy, M.M., Estradiol and the developing brain. Physiol Rev 88 (2008), 91–124.
22. 22 McCarthy, M., De Vries, G., Forger, N., Sexual differentiation of the brain: Mode, mechanisms and meaning. Pfaff, D., Arnold, A.P., Etgen, A.M., Fahrbach, S.E., Rubin, R.T., (eds.) Hormones, Brain and Behavior, 2009, Academic Press, San Diego, 1707–1744.
23. 23 McCarthy, M.M., Pickett, L.A., VanRyzin, J.W., Kight, K.E., Surprising origins of sex differences in the brain. Horm Behav 76 (2015), 3–10.
24. 24 Baron-Cohen, S., Empathizing, systemizing, and the extreme male brain theory of autism. Prog Brain Res 186 (2010), 167–175.
25. 25 Ingudomnukul, E., Baron-Cohen, S., Wheelwright, S., Knickmeyer, R., Elevated rates of testosterone-related disorders in women with autism spectrum conditions. Horm Behav 51 (2007), 597–604.
26. 26 Baron-Cohen, S., The extreme male brain theory of autism. Trends Cogn Sci 6 (2002), 248–254.
27. 27 Lai, M.C., Lombardo, M.V., Suckling, J., Ruigrok, A.N., Chakrabarti, B., Ecker, C., et al. Biological sex affects the neurobiology of autism. Brain 136 (2013), 2799–2815.
28. 28 Turner, T.N., Sharma, K., Oh, E.C., Liu, Y.P., Collins, R.L., Sosa, M.X., et al. Loss of delta-catenin function in severe autism. Nature 520 (2015), 51–56.
29. 29 Lai, M.C., Baron-Cohen, S., Buxbaum, J.D., Understanding autism in the light of sex/gender. Mol Autism, 6, 2015, 24.
30. 30 Silverman, J.L., Yang, M., Lord, C., Crawley, J.N., Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 11 (2010), 490–502.
31. 31 Hamilton, S.M., Green, J.R., Veeraragavan, S., Yuva, L., McCoy, A., Wu, Y., et al. Fmr1 and Nlgn3 knockout rats: novel tools for investigating autism spectrum disorders. Behav Neurosci 128 (2014), 103–109.
32. 32 Esclassan, F., Francois, J., Phillips, K.G., Loomis, S., Gilmour, G., Phenotypic characterization of nonsocial behavioral impairment in neurexin 1alpha knockout rats. Behav Neurosci 129 (2015), 74–85.
33. 33 Grayton, H.M., Missler, M., Collier, D.A., Fernandes, C., Altered social behaviours in neurexin 1alpha knockout mice resemble core symptoms in neurodevelopmental disorders. PloS One, 8, 2013, e67114.
34. 34 Laarakker, M.C., Reinders, N.R., Bruining, H., Ophoff, R.A., Kas, M.J., Sex-dependent novelty response in neurexin-1alpha mutant mice. PloS One, 7, 2012, e31503.
35. 35 Lo, S.C., Scearce-Levie, K., Sheng, M., Characterization of social behaviors in caspase-3 deficient mice. Sci Rep, 6, 2016, 18335.
36. 36 Curtis, J.T., Hood, A.N., Chen, Y., Cobb, G.P., Wallace, D.R., Chronic metals ingestion by prairie voles produces sex-specific deficits in social behavior: An animal model of autism. Behav Brain Res 213 (2010), 42–49.
37. 37 Werling, D.M., Parikshak, N.N., Geschwind, D.H., Gene expression in human brain implicates sexually dimorphic pathways in autism spectrum disorders. Nat Commun, 7, 2016, 10717.
38. 38 Voineagu, I., Wang, X., Johnston, P., Lowe, J.K., Tian, Y., Horvath, S., et al. Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature 474 (2011), 380–384.
39. 39 Gupta, S., Ellis, S.E., Ashar, F.N., Moes, A., Bader, J.S., Zhan, J., et al. Transcriptome analysis reveals dysregulation of innate immune response genes and neuronal activity-dependent genes in autism. Nat Commun, 5, 2014, 5748.
40. 40 Suzuki, K., Sugihara, G., Ouchi, Y., Nakamura, K., Futatsubashi, M., Takebayashi, K., et al. Microglial activation in young adults with autism spectrum disorder. JAMA Psychiatry 70 (2013), 49–58.
41. 41 Puelles, L., Harrison, M., Paxinos, G., Watson, C., A developmental ontology for the mammalian brain based on the prosomeric model. Trends Neurosci 36 (2013), 570–578.
42. 42 Raisman, G., Field, P.M., Sexual dimorphism in the preoptic area of the rat. Science 173 (1971), 731–733.
43. 43 Gorski, R.A., Harlan, R.E., Jacobson, C.D., Shryne, J.E., Southam, A.M., Evidence for the existence of a sexually dimorphic nucleus in the preoptic area of the rat. J Comp Neurol 193 (1980), 529–539.
44. 44 Roselli, C.E., Larkin, K., Resko, J.A., Stellflug, J.N., Stormshak, F., The volume of a sexually dimorphic nucleus in the ovine medial preoptic area/anterior hypothalamus varies with sexual partner preference. Endocrinology 145 (2004), 478–483.
45. 45 Davis, E.C., Popper, P., Gorski, R.A., The role of apoptosis in sexual differentiation of the rat sexually dimorphic nucleus of the preoptic area. Brain Res 734 (1996), 10–18.
46. 46 Simerly, R.B., Wired for reproduction: Organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 25 (2002), 507–536.
47. 47 Amateau, S.K., McCarthy, M.M., A novel mechanism of dendritic spine plasticity involving estradiol induction of prostglandin-E2. J Neurosci 22 (2002), 8586–8596.
48. 48 Wright, C.L., Burks, S.R., McCarthy, M.M., Identification of prostaglandin E2 receptors mediating perinatal masculinization of adult sex behavior and neuroanatomical correlates. Dev Neurobiol 68 (2008), 1406–1419.
49. 49 Amateau, S.K., McCarthy, M.M., Sexual differentiation of astrocyte morphology in the developing rat preoptic area. J Neuroendocrinol 14 (2002), 904–910.
50. 50 Lenz, K.M., Nugent, B.M., Haliyur, R., McCarthy, M.M., Microglia are essential to masculinization of brain and behavior. J Neurosci 33 (2013), 2761–2772.
51. 51 Hull, E.M., Dominguez, J.M., Sexual behavior in male rodents. Horm Behav 52 (2007), 45–55.
52. 52 Numan, M., Maternal behavior. Knobil, E., Neill, J.D., (eds.) Physiology of Reproduction, 1994, Raven Press, New York, 108–302.
53. 53 Dölen, G., Autism: Oxytocin, serotonin, and social reward. Soc Neurosci 10 (2015), 450–465.
54. 54 Shamay-Tsoory, S., Young, L.J., Understanding the oxytocin system and its relevance to psychiatry. Biol Psychiatry 79 (2016), 150–152.
55. 55 Hollander, E., Novotny, S., Hanratty, M., Yaffe, R., DeCaria, C.M., Aronowitz, B.R., et al. Oxytocin infusion reduces repetitive behaviors in adults with autistic and Asperger's disorders. Neuropsychopharmacology 28 (2003), 193–198.
56. 56 Champagne, F., Diorio, J., Sharma, S., Meaney, M.J., Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci U S A 98 (2001), 12736–12741.
57. 57 Insel, T.R., Shapiro, L.E., Oxytocin receptors and maternal behavior. Ann N Y Acad Sci 652 (1992), 122–141.
58. 58 de Vries, G.J., Sex differences in vasopressin and oxytocin innervation of the brain. Prog Brain Res 170 (2008), 17–27.
59. 59 Burkett, J.P., Andari, E., Johnson, Z.V., Curry, D.C., de Waal, F.B., Young, L.J., Oxytocin-dependent consolation behavior in rodents. Science 351 (2016), 375–378.
60. 60 Guastella, A.J., Hickie, I.B., Oxytocin treatment, circuitry, and autism: A critical review of the literature placing oxytocin into the autism context. Biol Psychiatry 79 (2016), 234–242.
61. 61 Saper, C.B., Scammell, T.E., Lu, J., Hypothalamic regulation of sleep and circadian rhythms. Nature 437 (2005), 1257–1263.
62. 62 Romanovsky, A., Almeida, M., Aronoff, D., Ivanov, A., Konsman, J., Steiner, A., et al. Fever and hypothermia in systemic inflammation: Recent discoveries and revisions. Front Biosci 10 (2005), 2193–2216.
63. 63 Devnani, P.A., Hegde, A.U., Autism and sleep disorders. J Pediatr Neurosci 10 (2015), 304–307.
64. 64 Curran, L.K., Newschaffer, C.J., Lee, L.C., Crawford, S.O., Johnston, M.V., Zimmerman, A.W., Behaviors associated with fever in children with autism spectrum disorders. Pediatrics 120 (2007), e1386–e1392.
65. 65 Toufexis, D., Region- and sex-specific modulation of anxiety behaviours in the rat. J Neuroendocrinol 19 (2007), 461–473.
66. 66 Auger, A.P., Olesen, K.M., Brain sex differences and the organisation of juvenile social play behaviour. J Neuroendocrinol 21 (2009), 519–525.
67. 67 Gungor, N.Z., Yamamoto, R., Paré, D., Optogenetic study of the projections from the bed nucleus of the stria terminalis to the central amygdala. J Neurophysiol 114 (2015), 2903–2911.
68. 68 Koutcherov, Y., Paxinos, G., Mai, J.K., Organization of the human medial preoptic nucleus. J Comp Neurol 503 (2007), 392–406.
69. 69 Avery, S.N., Clauss, J.A., Winder, D.G., Woodward, N., Heckers, S., Blackford, J.U., BNST neurocircuitry in humans. Neuroimage 91 (2014), 311–323.
70. 70 Kruger, O., Shiozawa, T., Kreifelts, B., Scheffler, K., Ethofer, T., Three distinct fiber pathways of the bed nucleus of the stria terminalis to the amygdala and prefrontal cortex. Cortex 66 (2015), 60–68.
71. 71 Kaufmann, W., Andreasson, K., Isakson, P., Worley, P., Cyclooxygenases and the central nervous system. Prostaglandins 54 (1997), 601–624.
72. 72 Shi, J., Johansson, J., Woodling, N.S., Wang, Q., Montine, T.J., Andreasson, K., The prostaglandin E2 E-prostanoid 4 receptor exerts anti-inflammatory effects in brain innate immunity. J Immunol 184 (2010), 7207–7218.
73. 73 Yokoyama, U., Iwatsubo, K., Umemura, M., Fujita, T., Ishikawa, Y., The prostanoid EP4 receptor and its signaling pathway. Pharmacol Rev 65 (2013), 1010–1052.
74. 74 Amateau, S.K., McCarthy, M.M., Induction of PGE(2) by estradiol mediates developmental masculinization of sex behavior. Nat Neurosci 7 (2004), 643–650.
75. 75 Wright, C.L., McCarthy, M.M., Prostaglandin E2-induced masculinization of brain and behavior requires protein kinase A, AMPA/kainate, and metabotropic glutamate receptor signaling. J Neurosci 29 (2009), 13274–13282.
76. 76 Ginhoux, F., Lim, S., Hoeffel, G., Low, D., Huber, T., Origin and differentiation of microglia. Front Cell Neurosci, 7, 2013, 45.
77. 77 Nayak, D., Roth, T.L., McGavern, D.B., Microglia development and function. Annu Rev Immunol 32 (2014), 367–402.
78. 78 Streit, W.J., Microglial response to brain injury: A brief synopsis. Toxicol Pathol 28 (2000), 28–30.
79. 79 Schafer, D.P., Lehrman, E.K., Kautzman, A.G., Koyama, R., Mardinly, A.R., Yamasaki, R., et al. Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74 (2012), 691–705.
80. 80 Ekdahl, C.T., Kokaia, Z., Lindvall, O., Brain inflammation and adult neurogenesis: the dual role of microglia. Neuroscience 158 (2009), 1021–1029.
81. 81 Sierra, A., Encinas, J.M., Deudero, J.J., Chancey, J.H., Enikolopov, G., Overstreet-Wadiche, L.S., et al. Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis. Cell Stem Cell 7 (2010), 483–495.
82. 82 Ueno, M., Fujita, Y., Tanaka, T., Nakamura, Y., Kikuta, J., Ishii, M., et al. Layer V cortical neurons require microglial support for survival during postnatal development. Nat Neurosci 16 (2013), 543–551.
83. 83 Brown, G.C., Neher, J.J., Eaten alive! Cell death by primary phagocytosis: ‘Phagoptosis’. Trends Biochem Sci 37 (2012), 325–332.
84. 84 Lenz, K.M., Wright, C.L., Martin, R.C., McCarthy, M.M., Prostaglandin E regulates AMPA receptor phosphorylation and promotes membrane insertion in preoptic area neurons and glia during sexual differentiation. PloS One, 6, 2011, e18500.
85. 85 Bezzi, P., Carmignoto, G., Pasti, L., Vesce, S., Rossi, D., Rizzini, B.L., et al. Prostaglandins stimulate calcium-dependent glutamate release in astrocytes. Nature 391 (1998), 281–285.
86. 86 Reeber, S.L., Otis, T.S., Sillitoe, R.V., New roles for the cerebellum in health and disease. Front Syst Neurosci, 7, 2013, 83.
87. 87 Dean, S.L., McCarthy, M.M., Steroids, sex and the cerebellar cortex: Implications for human disease. Cerebellum 7 (2008), 38–47.
88. 88 Durisko, C., Fiez, J.A., Functional activation in the cerebellum during working memory and simple speech tasks. Cortex 46 (2010), 896–906.
89. 89 Crispino, L., Bullock, T.H., Cerebellum mediates modality-specific modulation of sensory responses of midbrain and forebrain in rat. Proc Natl Acad Sci U S A 81 (1984), 2917–2920.
90. 90 Konarski, J.Z., McIntyre, R.S., Grupp, L.A., Kennedy, S.H., Is the cerebellum relevant in the circuitry of neuropsychiatric disorders?. J Psychiatry Neurosci 30 (2005), 178–186.
91. 91 Stoodley, C.J., Valera, E.M., Schmahmann, J.D., Functional topography of the cerebellum for motor and cognitive tasks: An fMRI study. Neuroimage 59 (2012), 1560–1570.
92. 92 Ramnani, N., The primate cortico-cerebellar system: Anatomy and function. Nat Rev Neurosci 7 (2006), 511–522.
93. 93 D'Angelo, E., Casali, S., Seeking a unified framework for cerebellar function and dysfunction: from circuit operations to cognition. Front Neural Circuits, 6, 2012, 116.
94. 94 Hibi, M., Shimizu, T., Development of the cerebellum and cerebellar neural circuits. Dev Neurobiol 72 (2012), 282–301.
95. 95 D'Mello, A.M., Stoodley, C.J., Cerebro-cerebellar circuits in autism spectrum disorder. Front Neurosci, 9, 2015, 408.
96. 96 Mitchell, S.R., Reiss, A.L., Tatusko, D.H., Ikuta, I., Kazmerski, D.B., Botti, J.A., et al. Neuroanatomic alterations and social and communication deficits in monozygotic twins discordant for autism disorder. Am J Psychiatry 166 (2009), 917–925.
97. 97 Haist, F., Adamo, M., Westerfield, M., Courchesne, E., Townsend, J., The functional neuroanatomy of spatial attention in autism spectrum disorder. Dev Neuropsychol 27 (2005), 425–458.
98. 98 Courchesne, E., Pierce, K., Schumann, C.M., Redcay, E., Buckwalter, J.A., Kennedy, D.P., et al. Mapping early brain development in autism. Neuron 56 (2007), 399–413.
99. 99 Fatemi, S.H., Aldinger, K.A., Ashwood, P., Bauman, M.L., Blaha, C.D., Blatt, G.J., et al. Consensus paper: Pathological role of the cerebellum in autism. Cerebellum 11 (2012), 777–807.
100. 100 Limperopoulos, C., Bassan, H., Gauvreau, K., Robertson, R.L. Jr, Sullivan, N.R., Benson, C.B., et al. Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors?. Pediatrics 120 (2007), 584–593.
101. 101 Abel, K.M., Drake, R., Goldstein, J.M., Sex differences in schizophrenia. Int Rev Psychiatry 22 (2010), 417–428.
102. 102 Werling, D.M., Geschwind, D.H., Sex differences in autism spectrum disorders. Curr Opin Neurol 26 (2013), 146–153.
103. 103 Dean, S.L., Wright, C.L., Hoffman, J.F., Wang, M., Alger, B.E., McCarthy, M.M., Prostaglandin E2 stimulates estradiol synthesis in the cerebellum postnatally with associated effects on purkinje neuron dendritic arbor and electrophysiological properties. Endocrinology 153 (2012), 5415–5427.
104. 104 Dean, S.L., Knutson, J.F., Krebs-Kraft, D.L., McCarthy, M.M., Prostaglandin E2 is an endogenous modulator of cerebellar development and complex behavior during a sensitive postnatal period. Eur J Neurosci 35 (2012), 1218–1229.
105. 105 Hoffman, J.F., Wright, C.L., McCarthy, M.M., A critical period in Purkinje cell development is mediated by local estradiol synthesis, disrupted by inflammation, and has enduring consequences only for males. J Neurosci 36 (2016), 10039–10049.
106. 106 Constantino, J.N., Przybeck, T., Friesen, D., Todd, R.D., Reciprocal social behavior in children with and without pervasive developmental disorders. J Dev Behav Pediatr 21 (2000), 2–11.
107. 107 Constantino, J.N., Todd, R.D., Genetic structure of reciprocal social behavior. Am J Psychiatry 157 (2000), 2043–2045.
108. 108 Williams White, S., Keonig, K., Scahill, L., Social skills development in children with autism spectrum disorders: A review of the intervention research. J Autism Dev Disord 37 (2007), 1858–1868.
109. 109 Siviy, S.M., Panksepp, J., In search of the neurobiological substrates for social playfulness in mammalian brains. Neurosci Biobehav Rev 35 (2011), 1821–1830.
110. 110 Argue, K.J., McCarthy, M.M., Characterization of juvenile play in rats: Importance of sex of self and sex of partner. Biol Sex Differ, 6, 2015, 16.