Mitigation of sociocommunicational deficits of autism through oxytocin-induced recovery of medial prefrontal activity a randomized trial

JAMA Psychiatry

Volumn 71, Issue 2, 2014, Pages 166-175

  Watanabe, Takamitsu ^a   Abe, Osamu ^a,b   Kuwabara, Hitoshi ^a   Yahata, Noriaki ^c   Takano, Yosuke ^a   Iwashiro, Norichika ^a   Natsubori, Tatsunobu ^a   Aoki, Yuta ^a   Takao, Hidemasa ^a   Kawakubo, Yuki ^a   Kamio, Yoko ^d   Kato, Nobumasa ^e   Miyashita, Yasushi ^a   Kasai, Kiyoto ^a   Yamasue, Hidenori ^a,e,f  

^a UNIVERSITY OF TOKYO   (Japan)

^b NIHON UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d NATIONAL INSTITUTE OF MENTAL HEALTH   (Japan)

^e SHOWA UNIVERSITY   (Japan)

^f JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

OXYTOCIN; PLACEBO;

ABSENCE OF SIDE EFFECTS; ADULT; ARTICLE; AUTISM; CLINICAL ARTICLE; COMMUNICATION DISORDER; CONTROLLED STUDY; COORDINATION; CROSSOVER PROCEDURE; DECISION MAKING; DOUBLE BLIND PROCEDURE; DRUG EFFICACY; ELECTROENCEPHALOGRAM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; IMAGING SOFTWARE; MALE; NERVE POTENTIAL; NONVERBAL COMMUNICATION; NUCLEAR MAGNETIC RESONANCE SCANNER; PREFRONTAL CORTEX; PSYCHOSOCIAL DISORDER; RANDOMIZED CONTROLLED TRIAL; RESPONSE TIME; SINGLE DRUG DOSE; SOCIAL PSYCHOLOGY; SOCIOCOMMUNICATIONAL DEFICIT; YOUNG ADULT;

ADMINISTRATION, INTRANASAL; ADULT; CHILD DEVELOPMENT DISORDERS, PERVASIVE; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; OXYTOCIN; PLACEBO EFFECT; PREFRONTAL CORTEX; SOCIAL BEHAVIOR; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84893842512     PISSN: 2168622X     EISSN: None     Source Type: Journal    
DOI: 10.1001/jamapsychiatry.2013.3181     Document Type: Article

References (52)

1. Autism and Developmental Disabilities Monitoring Network Surveillance Year 2008 Principal Investigators; Centers for Disease Control and Prevention. Prevalence of autism spectrum disorders: Autism and Developmental Disabilities Monitoring Network, 14 sites, United States, 2008. MMWR Surveill Summ. 2012;61(3):1-19.
2. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders. 4th ed, text revision. Washington, DC: American Psychiatric Association; 2000.
3. Kuehn BM. Scientists probe oxytocin therapy for social deficits in autism, schizophrenia. JAMA. 2011;305(7):659-661.
4. Frith U, Happé F. Language and communication in autistic disorders. Philos Trans R Soc Lond B Biol Sci. 1994;346(1315):97-104.
5. Pelphrey KA, Morris JP, McCarthy G. Neural basis of eye gaze processing deficits in autism. Brain. 2005;128(pt 5):1038-1048.
6. Wang AT, Lee SS, Sigman M, Dapretto M. Neural basis of irony comprehension in children with autism: the role of prosody and context. Brain. 2006;129(pt 4):932-943.
7. Wang AT, Lee SS, Sigman M, Dapretto M. Reading affect in the face and voice: neural correlates of interpreting communicative intent in children and adolescents with autism spectrum disorders. Arch Gen Psychiatry. 2007;64(6): 698-708.
8. Watanabe T, Yahata N, Abe O, et al. Diminished medial prefrontal activity behind autistic social judgments of incongruent information. PLoS One. 2012;7(6):e39561.
9. Happé FG. Communicative competence and theory ofmind in autism: a test of relevance theory. Cognition. 1993;48(2):101-119.
10. Leekam SR, PriorM. Can autistic children distinguish lies from jokes? a second look at second-order belief attribution. J Child Psychol Psychiatry. 1994;35(5):901-915.
11. Shamay-Tsoory SG, Tomer R, Aharon-Peretz J. The neuroanatomical basis of understanding sarcasm and its relationship to social cognition. Neuropsychology. 2005;19(3):288-300.
12. Bartz JA, Zaki J, Bolger N, Ochsner KN. Social effects of oxytocin in humans: context and person matter. Trends Cogn Sci. 2011;15(7):301-309.
13. Meyer-Lindenberg A, Domes G, Kirsch P, Heinrichs M. Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine. Nat Rev Neurosci. 2011;12(9):524-538.
14. KosfeldM, Heinrichs M, Zak PJ, Fischbacher U, Fehr E. Oxytocin increases trust in humans. Nature. 2005;435(7042):673-676.
15. Domes G, Heinrichs M, Michel A, Berger C, Herpertz SC. Oxytocin improves "mind-reading" in humans. Biol Psychiatry. 2007;61(6):731-733.
16. Donaldson ZR, Young LJ. Oxytocin, vasopressin, and the neurogenetics of sociality. Science. 2008;322(5903):900-904.
17. Petrovic P, Kalisch R, Singer T, Dolan RJ. Oxytocin attenuates affective evaluations of conditioned faces and amygdala activity. J Neurosci. 2008;28(26):6607-6615.
18. Van IJzendoorn MH, Bakermans-Kranenburg MJ. A sniff of trust:meta-analysis of the effects of intranasal oxytocin administration on face recognition, trust to in-group, and trust to out-group. Psychoneuroendocrinology. 2012;37(3):438-443.
19. Yamasue H, Yee JR, Hurlemann R, et al. Integrative approaches utilizing oxytocin to enhance prosocial behavior: from animal and human social behavior to autistic social dysfunction. J Neurosci. 2012;32(41):14109-14117.
20. Carter CS. Sex differences in oxytocin and vasopressin: implications for autism spectrum disorders? Behav Brain Res. 2007;176(1):170-186.
21. Jin D, Liu H-X, Hirai H, et al. CD38 is critical for social behaviour by regulating oxytocin secretion. Nature. 2007;446(7131):41-45.
22. Petrovic P, Kalisch R, Pessiglione M, Singer T, Dolan RJ. Learning affective values for faces is expressed in amygdala and fusiform gyrus. Soc Cogn Affect Neurosci. 2008;3(2):109-118.
23. Bethlehem RAI, van Honk J, Auyeung B, Baron-Cohen S. Oxytocin, brain physiology, and functional connectivity: a review of intranasal oxytocin fMRI studies. Psychoneuroendocrinology. 2013;38(7):962-974.
24. Hollander E, Novotny S, Hanratty M, et al. Oxytocin infusion reduces repetitive behaviors in adults with autistic and Asperger's disorders. Neuropsychopharmacology. 2003;28(1):193-198.
25. Hollander E, Bartz J, ChaplinW, et al. Oxytocin increases retention of social cognition in autism. Biol Psychiatry. 2007;61(4):498-503.
26. Andari E, Duhamel J-R, Zalla T, Herbrecht E, LeboyerM, Sirigu A. Promoting social behavior with oxytocin in high-functioning autism spectrum disorders. Proc Natl Acad Sci U S A. 2010;107(9):4389-4394.
27. Guastella AJ, Einfeld SL, Gray KM, et al. Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biol Psychiatry. 2010;67(7):692-694.
28. Anagnostou E, Soorya L, ChaplinW, et al. Intranasal oxytocin versus placebo in the treatment of adults with autism spectrum disorders: a randomized controlled trial. Mol Autism. 2012;3(1):16.
29. Senju A, Southgate V, White S, Frith U. Mindblind eyes: an absence of spontaneous theory of mind in Asperger syndrome. Science. 2009;325(5942):883- 885.
30. Hurlemann R, Patin A, Onur OA, et al. Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans. J Neurosci. 2010;30(14):4999-5007.
31. Theodoridou A, Rowe AC, Penton-Voak IS, Rogers PJ. Oxytocin and social perception: oxytocin increases perceived facial trustworthiness and attractiveness. Horm Behav. 2009;56(1):128-132.
32. Lord C, RutterM, Le Couteur A. Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord. 1994;24(5):659-685.
33. Lord C, Risi S, Lambrecht L, et al. 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(3):205-223.
34. Wechsler D. Wechsler Adult Intelligence Scale-Revised. New York, NY: Psychological Corp; 1981.
35. Born J, Lange T, KernW, McGregor GP, Bickel U, Fehm HL. Sniffing neuropeptides: a transnasal approach to the human brain. Nat Neurosci. 2002;5(6):514-516.
36. Gamer M, Zurowski B, Büchel C. Different amygdala subregions mediate valence-related and attentional effects of oxytocin in humans. Proc Natl Acad Sci U S A. 2010;107(20):9400-9405.
37. Watanabe T, Yahata N, Kawakubo Y, et al. Network structure underlying resolution of conflicting nonverbal and verbal social information [published onlineMay 18, 2013]. Soc Cogn Affect Neurosci. doi:10. 1093/scan/nst046.
38. Cocosco CA, Kollokian V, Kwan RKS, Pike GB, Evans AC. BrainWeb: online interface to a 3D MRI simulated brain database. Neuroimage. 1997;5(4):425.
39. Friston KJ, Buechel C, Fink GR, Morris J, Rolls ET, Dolan RJ. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage. 1997;6(3):218-229.
40. Watanabe T, Kimura HM, Hirose S, et al. Functional dissociation between anterior and posterior temporal cortical regions during retrieval of remote memory. J Neurosci. 2012;32(28):9659-9670.
41. Kirsch P, Esslinger C, Chen Q, et al. Oxytocin modulates neural circuitry for social cognition and fear in humans. J Neurosci. 2005;25(49):11489-11493.
42. Singer T, Snozzi R, Bird G, et al. Effects of oxytocin and prosocial behavior on brain responses to direct and vicariously experienced pain. Emotion. 2008;8(6):781-791.
43. Baumgartner T, Heinrichs M, Vonlanthen A, Fischbacher U, Fehr E. Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron. 2008;58(4):639-650.
44. Viviani D, Charlet A, van den Burg E, et al. Oxytocin selectively gates fear responses through distinct outputs from the central amygdala. Science. 2011;333(6038):104-107.
45. Knobloch HS, Charlet A, Hoffmann LC, et al. Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron. 2012;73(3):553-566.
46. Striepens N, Scheele D, Kendrick KM, et al. Oxytocin facilitates protective responses to aversive social stimuli in males. Proc Natl Acad Sci U S A. 2012;109(44):18144-18149.
47. Scheele D, Striepens N, Güntürkün O, et al. Oxytocin modulates social distance between males and females. J Neurosci. 2012;32(46):16074-16079.
48. Young LJ, Wang Z. The neurobiology of pair bonding. Nat Neurosci. 2004;7(10):1048-1054.
49. Insel TR. The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron. 2010;65(6): 768-779.
50. Tost H, Kolachana B, Hakimi S, et al. A common allele in the oxytocin receptor gene (OXTR) impacts prosocial temperament and human hypothalamic-limbic structure and function. Proc Natl Acad Sci U S A. 2010;107(31):13936-13941.
51. Furman DJ, Chen MC, Gotlib IH. Variant in oxytocin receptor gene is associated with amygdala volume. Psychoneuroendocrinology. 2011;36(6):891-897.
52. Tost H, Kolachana B, Verchinski BA, et al. Neurogenetic effects of OXTR rs2254298 in the extended limbic system of healthy Caucasian adults. Biol Psychiatry. 2011;70(9):e37-e39, author reply e41-e42.