The oxytocin system in drug discovery for autism: Animal models and novel therapeutic strategies

Hormones and Behavior

Volumn 61, Issue 3, 2012, Pages 340-350

  Modi, Meera E ^a   Young, Larry J ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Animal models; Autism; Buspirone; Oxytocin; Prairie voles; Serotonin; Social cognition; Therapeutics

Indexed keywords

CD38 ANTIGEN; CYSTYL AMINOPEPTIDASE; MELANOCORTIN 4 RECEPTOR; OXYTOCIN; OXYTOCIN RECEPTOR;

ANXIETY; AUTISM; BEHAVIOR THERAPY; CHROMOSOME 3; CONSTRUCT VALIDITY; EMOTION; FACE VALIDITY; GENE; GENETIC LINKAGE; HUMAN; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; INBRED STRAIN; KNOCKOUT MOUSE; MOTIVATION; NONHUMAN; OXYTOCIN BLOOD LEVEL; OXYTOCIN RECEPTOR GENE; OXYTOCIN RELEASE; PHENOTYPIC VARIATION; PREDICTIVE VALIDITY; PRIORITY JOURNAL; RECEPTOR DENSITY; RECOGNITION; REINFORCEMENT; REVIEW; SEXUAL BEHAVIOR; SINGLE NUCLEOTIDE POLYMORPHISM; SOCIAL BEHAVIOR; SOCIAL COGNITION; SOCIAL DISCRIMINATION; SOCIAL INTERACTION; SOCIAL LEARNING; SUPRAOPTIC NUCLEUS;

ADMINISTRATION, INTRANASAL; ANIMALS; ANXIETY; ARVICOLINAE; AUTISTIC DISORDER; BEHAVIOR THERAPY; CYSTINYL AMINOPEPTIDASE; DISEASE MODELS, ANIMAL; DRUG DISCOVERY; GENOTYPE; HUMANS; MICE; MODELS, PSYCHOLOGICAL; OXYTOCIN; PHENOTYPE; RECEPTORS, OXYTOCIN; RECOGNITION (PSYCHOLOGY); SOCIAL BEHAVIOR;

EID: 84858674139     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2011.12.010     Document Type: Review

References (99)

1. Ahern T.H., Modi M.E., Burkett J.P., Young L.J. Evaluation of two automated metrics for analyzing partner preference tests. J. Neurosci. Methods 2009, 182:180-188.
2. Albiston A.L., Diwakarla S., Fernando R.N., Mountford S.J., Yeatman H.R., Morgan B., Pham V., Holien J.K., Parker M.W., Thompson P.E., Chai S.Y. Identification and development of specific inhibitors for insulin-regulated aminopeptidase as a new class of cognitive enhancers. Br. J. Pharmacol. 2011, 164:37-47.
3. Amico J.A., Cai H.M., Vollmer R.R. Corticosterone release in oxytocin gene deletion mice following exposure to psychogenic versus non-psychogenic stress. Neurosci. Lett. 2008, 442:262-266.
4. Andari E., Duhamel J., Zalla T., Herbrecht E., Leboyer M., Sirigu A. Promoting social behavior with oxytocin in high-functioning autism spectrum disorders. Proc. Natl. Acad. Sci. 2010, 107:4389-4394.
5. Ashworth D.M., Batt A.R., Baxter A.J., Broqua P., Haigh R.M., Hudson P., Heeney C.M., Laporte R., Penson A.M., Pitt G.R., Robson P.A., Rooker D.P., Tartar A.L., Yea C.M., Roe M.B. Nonpeptide oxytocin agonists. Drugs Future 2006, 31:345.
6. Bagdy G., Kalogeras K.T. Stimulation of 5-HT1A and 5-HT2/5-HT1C receptors induce oxytocin release in the male rat. Brain Res. 1993, 611:330-332.
7. Barrett S., Beck J.C., Bernier R., Bisson E., Braun T.A., Casavant T.L., Childress D., Folstein S.E., Garcia M., Gardiner M.B., Gilman S., Haines J.L., Hopkins K., Landa R., Meyer N.H., Mullane J.A., Nishimura D.Y., Palmer P., Piven J., Purdy J., Santangelo S.L., Searby C., Sheffield V., Singleton J., Slager S. An autosomal genomic screen for autism. Collaborative linkage study of autism. Am. J. Med. Genet. 1999, 88:609-615.
8. Bartz J.A., Zaki J., Bolger N., Hollander E., Ludwig N.N., Kolevzon A., Ochsner K.N. Oxytocin selectively improves empathic accuracy. Psychol. Sci. 2010, 21:1426-1428.
9. Bartz J.A., Zaki J., Bolger N., Ochsner K.N. Social effects of oxytocin in humans: context and person matter. Trends Cogn. Sci. 2011, 15:301-309.
10. Bolivar V.J., Walters S.R., Phoenix J.L. Assessing autism-like behavior in mice: variations in social interctions among inbred strains. Behav. Brain Res. 2007, 176:21-26.
11. Born J., Lange T., Kern W., McGregor G.P., Bickel U., Fehm H.L. Sniffing neuropeptides: a transnasal approach to the human brain. Nat. Neurosci. 2002, 5:514-516.
12. Bos P.A., Panksepp J., Bluthe R.M., Honk J.V. Acute effects of steroid hormones and neuropeptides on human social-emotional behavior: a review of single administration studies. Front. Neuroendocrinol. 2011, (Electronic publication ahead of print).
13. Brodkin E.S. BALB/c mice: low sociability and other phenotypes that may be relevant to autism. Behav. Brain Res. 2007, 176:53-65.
14. Buchheim A., Heinrichs M., George C., Pokorny D., Koops E., Henningsen P., O'Connor M.F., Gundel H. Oxytocin enhances the experience of attachment security. Psychoneuroendocrinology 2009, 34:1417-1422.
15. Bukelis I., Porter F.D., Zimmerman A.W., Tierney E. Smith-Lemli-Opitz syndrome and autism spectrum disorder. Am. J. Psychiatry 2007, 164:1655-1661.
16. Campbell D.B., Datta D., Jones S.T., Batey Lee E., Sutcliffe J.S., Hammock E.A., Levitt P. Association of oxytocin receptor (OXTR) gene variants with multiple phenotypes domains of autism spectrum disorder. J. Neurodev. Disord. 2011, 3:101-112.
17. Chai S.Y., Yeatman H.R., Parker M.W., Ascher D.B., Thompson P.E., Mulvey H.T., Albiston A.L. Development of cognitive enhancers based on inhibition of insulin-regulated aminopeptidase. BMC Neurosci. 2008, 9(Suppl. 2):S14.
18. Dluzen D.E., Muraoka S., Engelmann M., Landgraf R. The effects of infusion of arginine vasopressin, oxytocin or their antagonists into the olfactory bulb upon social recognition responses in male rats. Peptides 1998, 19:999-1005.
19. Domes G., Lischke A., Berger C., Grossmann A., Hauenstein K., Heinrichs M., Herpertz S.C. Effects of intranasal oxytocin on emotional face processing in women. Psychoneuroendocrinology 2010, 35:83-93.
20. Ebstein R.P., Mankuta D., Yirmiya N., Malavasi F. Are retinoids potential therapeutic agents in disorders of social cognition including autism?. FEBS Lett. 2011, 585:1529-1536.
21. Ermisch A., Barth T., Ruhle H.J., Skopkova J., Hrbas P., Landgraf R. On the blood-brain barrier to peptides: accumulation of labelled vasopressin, DesGlyNH2-vasopressin and oxytocin by brain regions. Endocrinol. Exp. 1985, 19:29-37.
22. Ey E., Leblond C.S., Bourgeron T. Behavioral profiles of mouse models for autism spectrum disorders. Autism Res. 2011, 4:5-16.
23. Ferguson J.N., Young L.J., Hearn E.F., Matzuk M.M., Insel T.R., Winslow J.T. Social amnesia in mice lacking the oxytocin gene. Nat. Genet. 2000, 25:284-288.
24. Ferguson J.N., Aldag J.M., Insel T.R., Young L.J. Oxytocin in the medial amygdala is essential for social recognition in the mouse. J. Neurosci. 2001, 21:8278-8285.
25. Fernando R.N., Larm J., Albiston A.L., Chai S.Y. Distribution and cellular localization of insulin-regulated aminopeptidase in the rat central nervous system. J. Comp. Neurol. 2005, 487:372-390.
26. Gabis L., Pomeroy J., Andriola M.R. Autism and epilepsy: cause, consequence, comorbidity or coincidence?. Epilepsy Behav. 2005, 7:652-656.
27. Gregory S.G., Connelly J.J., Towers A.J., Johnson J., Biscocho D., Markunas C.A., Lintas C., Abramson R.K., Wright H.H., Ellis P., Langford C.F., Worley G., Delong G.R., Murphy S.K., Cuccaro M.L., Persico A., Pericak-Vance M.A. Genomic and epigenetic evidence for oxytocin receptor deficiency in autism. BMC Med. 2009, 7.
28. Guastella A.J., Mitchell P.B., Dadds M.R. Oxytocin increases gaze to the eye region of human faces. Biol. Psychiatry 2008, 63:3-5.
29. Guastella A.J., Einfeld S.L., Gray K.M., Rinehart N.J., Tonge B.J., Lambert T.J., Hickie I.B. Intranasal oxytocin improves emotion recognition for youth with autism spectrum disorders. Biol. Psychiatry 2010, 67:692-694.
30. Hall S.S., Lightbody A.A., McCarthy B.E., Parker K.J., Reiss A.L. Effects of intranasal oxytocin on social anxiety in males with fragile X syndrome. Psychoneuroendocrinology 2011, (Electronic publication ahead of print).
31. Hawtin S.R., Howard H.C., Wheatley M. Identification of an extracellular segment of the oxytocin receptor providing agonist-specific binding epitopes. Biochemistry 2001, 354:465-472.
32. Higashida H., Yokoyama S., Kikuchi M. CD38 and its role in oxytocin secretion and social behavior. Horm. Behav. 2011.
33. Higashida H., Yokoyama S., Munesue T., Kikuchi M., Minabe Y., Lopatina O. Cd38 gene knock-out juvenile mice: a model of oxytocin signal defects in autism. Biol. Pharmacol. Bull. 2011, 34:1369-1372.
34. Hollander E., Novotny S., Hanratty M., Yaffe R., DeCaria C.M., Aronowitz B.R., Mosovich S. Oxytocin infusion reduces repetitive behaviors in adults with autistic and Asperger's disorders. Neuropsychopharmacology 2003, 28:193-198.
35. Hollander E., Bartz J., Chaplin W., Phillips A., Sumner J., Soorya L., Anagnostou E., Wasserman S. Oxytocin increases retention of social cognition in autism. Biol. Psychiatry 2007, 61:498-503.
36. Hurlemann R., Patin A., Onur O.A., Cohen M.X., Baumgartner T., Metzler S., Dziobek I., Gallinat J., Wagner M., Maier W., Kendrick K.M. Oxytocin enhances amygdala-dependent, socially reinforced learning and emotional empathy in humans. J. Neurosci. 2010, 30:4999-5007.
37. Illum L. Transport of drugs from the nasal cavity to the central nervous system. Eur. J. Pharm. Sci. 2000, 11:1-18.
38. Insel T.R., Shapiro L.E. Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc. Natl. Acad. Sci. U. S. A. 1992, 89:5981-5985.
39. Jacob S., Brune C.W., Carter C.S., Leventhal B.L., Lord C., Cook E.H. Association of the oxytocin receptor gene (OXTR) in Caucasian children and adolescents with autism. Neurosci. Lett. 2007, 417:6-9.
40. Jansen L.M., Gispen-de Wied C.C., Wiegant V.M., Westenberg H.G., Lahuis B.E., van Engeland H. Autonomic and neuroendocrine responses to a psychosocial stressor in adults with autistic spectrum disorder. J. Autism Dev. Disord. 2006, 36:891-899.
41. Jin D., Liu H.X., Hirai H., Torashima T., Nagai T., Lopatina O., Shnayder N.A., Yamada K., Noda M., Seike T., Fujita K., Takasawa S., Yokoyama S., Koizumi K., Shiraishi Y., Tanaka S., Hashii M., Yoshihara T., Higashida K., Islam M.S., Yamada N., Hayashi K., Noguchi N., Kato I., Okamoto H., Matsushima A., Salmina A., Munesue T., Shimizu N., Mochida S., Asano M., Higashida H. CD38 is critical for social behaviour by regulating oxytocin secretion. Nature 2007, 446:41-45.
42. Jorgensen H., Riis M., Knigge U., Kjaer A., Warberg J. Serotonin receptors involved in vasopressin and oxytocin secretion. J. Neuroendocrinol. 2003, 15:242-249.
43. Keebaugh A.C., Young L.J. Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults. Horm. Behav. 2011, 60:498-504.
44. Keri S., Benedek G. Oxytocin enhances the perception of biological motion in humans. Cogn. Affect. Behav. Neurosci. 2009, 9:237-241.
45. Kishimoto H., Hoshino S., Ohori M., Kontani K., Nishina H., Suzawa M., Kato S., Katada T. Molecular mechanism of human CD38 gene expression by retinoic acid. Identification of retinoic acid response element in the first intron. J. Biol. Chem. 1998, 273:465-483.
46. Kosfeld M., Heinrichs M., Zak P.J., Fischbacher U., Fehr E. Oxytocin increases trust in humans. Nature 2005, 435:673-676.
47. Kotulska K., Jozwiak S. Autism in monogenic disorders. Eur. J. Paediatr. Neurol. 2011, 15:177-180.
48. Landgraf R., Neumann I.D. Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front. Neuroendocrinol. 2004, 25:150-176.
49. Lauritsen M.B., Als T.D., Dahl H.A., Flint T.J., Wang A.G., Vang M., Kruse T.A., Ewald H., Mors O. A genome-wide search for alleles and haplotypes associated with autism and related pervasive developmental disorders on the Faroe Islands. Mol. Psychiatry 2006, 11:37-46.
50. Lerer E., Levi S., Salomon S., Darvasi A., Yirmiya N., Ebstein R.P. Association between the oxytocin receptor (OXTR) gene and autism: relationship to Vineland adaptive behavior scales and cognition. Mol. Psychiatry 2008, 13:980-988.
51. Lerer E., Levi S., Israel S., Yaari M., Nemanov L., Mankuta D., Nurit Y., Ebstein R.P. Low CD38 expression in lymphoblastoid cells and haplotypes are both associated with autism in a family-based study. Autism Res. 2010, 3:293-302.
52. Levine T.P., Sheinkopf S.J., Pescosolido M., Rodino A., Elia G., Lester B. Physiologic arousal to social stress in children with autism spectrum disorders: a pilot study. Res. Autism Spectr. Disord. 2012, 6:177-183.
53. Lew R.A., Mustafa T., Ye S., McDowall S.G., Chai S.Y., Albiston A.L. Angiotensin AT4 ligands are potent, competitive inhibitors of insulin regulated aminopeptidase (IRAP). J. Neurochem. 2003, 86:344-350.
54. Liu H.X., Lopatina O., Higashida C., Tsuji T., Kato I., Takasawa S., Okamoto H., Yokoyama S., Higashida H. Locomotor activity, ultrasonic vocalization and oxytocin levels in infant CD38 knockout mice. Neurosci. Lett. 2008, 448:67-70.
55. Liu X., Kawamura Y., Shimada T., Otowa T., Koishi S., Sugiyama T., Nishida H., Hashimoto O., Nakagami R., Tochigi M., Umekage T., Kano Y., Miyagawa T., Kato N., Tokunaga K., Sasaki T. Association of the oxytocin receptor (OXTR) gene polymorphisms with autism spectrum disorder (ASD) in the Japanese population. J. Hum. Genet. 2010, 55:137-141.
56. Macbeth A.H., Lee H.J., Edds J., Young W.S. Oxytocin and the oxytocin receptor underlie intra-strain but not inter-strain, social recognition. Genes Brain Behav. 2009, 8:558-567.
57. Mantella R.C., Vollmer R.R., Li X., Amico J.A. Female oxytocin-deficient mice display enhanced anxiety-related behavior. Endocrinology 2003, 144:2291-2296.
58. Matsumoto H., Nagasaka T., Hattori A., Rogi T., Tsuruoka N., Mizutani S., Tsujimoto M. Expression of placental leucine aminopeptidase/oxytocinase in neuronal cells and its action on neuronal peptides. Eur. J. Biochem. 2001, 268:3259-3266.
59. McCauley J.L., Li C., Jiang L., Olson L.M., Crockett G., Gainer K., Folstein S.E., Haines J.L., Sutcliffe J.S. Genome-wide and ordered-subset linkage analyses provide support for autism loci on 17q and 19p with evidence of phenotypic and interlocus genetic correlates. BMC Med. Genet. 2005, 6.
60. Mens W.B., Witter A., van Wilmersma Greidanus T.B. Penetration of neurophyophyseal hormones from plasma into cerebrospinal fluid: half-times of disappearance of these neuropeptides from CSF. Brain Res. 1983, 262:143-149.
61. Mizutani S., Yokosawa H., Tomoda Y. Degradation of oxytocin by the human placenta: effect of selective inhibitors. Acta Endocrinol. (Copenh.) 1992, 127:76-80.
62. Modahl C., Green L., Fein D., Morris M., Waterhouse L., Feinstein C., Levin H. Plasma oxytocin levels in autistic children. Biol. Psychiatry 1998, 43:270-277.
63. Modi M.E., Young L.J. D-cycloserine facilitates socially reinforced learning in an animal model relevant to autism spectrum disorders. Biol. Psychiatry 2011, 70:298-304.
64. Moy S.S., Nadler J.J., Young N.B., Perez A., Holloway L.P., Barbaro R.P., Barbaro J.R., Wilson L.M., Threadgill D.W., Lauder J.M., Magnuson T.R., Crawley J.N. Mouse behavioral tasks relevant to autism: phenotypes of 10 inbred strains. Behav. Brain Res. 2007, 176:4-20.
65. Olazabal D.E., Young L.J. Oxytocin receptors in the nucleus accumbens facilitate "spontaneous" maternal behavior in adult female prairie voles. Neuroscience 2006, 141:559-568.
66. Olazabal D.E., Young L.J. Species and individual differences in juvenile female alloparental care are associated with oxytocin receptor density in the striatum and the lateral septum. Horm. Behav. 2006, 49:681-687.
67. Page E.W. The usefulness of intravenous pitocin infusions in obstetrics. West. J. Surg. Obstet. Gynecol. 1954, 62:125-135.
68. Philippe A., Martinez M., Guilloud-Bataille M., Gilberg C., Rastam M., Sponheim E., Coleman M., Zappella M., Aschauer H., Van Maldergem L., Penet C., Feingold J., Brice A., Leboyer M. Genome-wide scan for autism susceptibility genes. Paris Autism Research International Sibpair Study. Hum. Mol. Genet. 1999, 8:805-812.
69. Pitt G.R., Batt A.R., Haigh R.M., Penson A.M., Robson P.A., Rooker D.P., Tartar A.L., Trim J.E., Yea C.M., Roe M.B. Non-peptide agonists. Bioorg. Med. Chem. Lett. 2004, 14:4585-4589.
70. Popik P., van Ree J.M. Oxytocin but not vasopressin facilitates social recognition following injection into the medial preoptic area of the rat brain. Eur. J. Pharmacol. 1991, 1:555-560.
71. Popik P., Vos P.E., van Ree J.M. Neurohypophyseal hormone receptors in the septum are implicated in social recognition in the rat. Behav. Pharmacol. 1992, 3:351-358.
72. Rilling J.K., Demarco A.C., Hackett P.D., Thompson R., Ditzen B., Patel R., Pagnoni G. Effects of intranasal oxytocin and vasopressin on cooperative behavior and associated brain activity in men. Psychoneuroendocrinology 2011, (Electronic publication ahead of print).
73. Rimmele U., Hediger K., Heinrichs M., Klaver P. Oxytocin makes a face in memory familiar. J. Neurosci. 2009, 29:38-42.
74. Ring R.H. A complicated picture of oxytocin action in the central nervous system revealed. Biol. Psychiatry 2011, 69:818-819.
75. Ring R.H., Malberg J.E., Potestio L., Ping J., Boikess S., Luo B., Schechter L.E., Rizzo S., Rahman Z., Rosenzweig-Lipson S. Anxiolytic-like activity of oxytocin in male mice: behavioral and autonomic evidence, therapeutic implications. Psychopharmacology (Berl) 2006, 185:218-225.
76. Ring R.H., Schechter L.E., Leonard S.K., Dwyer J.M., Platt B.J., Graf R., Grauer S., Pulicicchio C., Resnick L., Rahman Z., Sukoff Rizzo S.J., Luo B., Beyer C.E., Logue S.F., Marquis K.L., Hughes Z.A., Rosenzweig-Lipson S. Receptor and behavioral pharmacology of WAY-267464, a non-peptide oxytocin receptor agonist. Neuropharmacology 2010, 58:69-77.
77. Ross H.E., Young L.J. Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior. Front. Neuroendocrinol. 2009, 30:534-547.
78. Ross H.E., Cole C.D., Smith Y., Neumann I.D., Landgraf R., Murphy A.Z., Young L.J. Characterization of the oxytocin system regulating affiliative behavior in female prairie voles. Neuroscience 2009, 162:892-903.
79. Ross H.E., Freeman S.M., Spiegel L.L., Ren X., Terwilliger E.F., Young L.J. Variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviors in monogamous and polygamous voles. J. Neurosci. 2009, 29:1312-1318.
80. Sabatier N. alpha-Melanocyte-stimulating hormone and oxytocin: a peptide signaling cascade in the hypothalamus. J. Neuroendocrinol. 2006, 18:703-710.
81. Sabatier N., Caquineau C., Dayanithi G., Bull P., Douglas A.J., Guan X.M., Jiang M., Van der Ploeg L., Leng G. Alpha-melanocyte-stimulating hormone stimulates oxytocin release from the dendrites of hypothalamic neurons while inhibiting oxytocin release from their terminals in the neurohypophysis. J. Neurosci. 2003, 23:10351-10358.
82. Sala M., Braida D., Lentini D., Busnelli M., Bulgheroni E., Capurro V., Finardi A., Donzelli A., Pattini L., Rubino T., Parolaro D., Nishimori K., Parenti M., Chini B. Pharmacologic rescue of impaired cognitive flexibility, social decifics, increased aggression, and seizure susceptibility in oxytocin receptor null mice: a neurobehavioral model of autism. Biol. Psychiatry 2011, 69:875-882.
83. Scattoni M.L., Gandhy S.U., Ricceri L., Crawley J.N. Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism. PLoS One 2008, 3:e3067.
84. 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. Strong association of de novo copy number mutations with autism. Science 2007, 316:445-449.
85. Silverman J.L., Yang M., Turner S.M., Katz A.M., Bell D.B., Koenig J.I., Crawley J.N. Low stress reactivity and neuroendocrine factors in the BTBR T+tf/J mouse model of autism. Neuroscience 2010, 171:1197-1208.
86. Takayanagi Y., Yoshida M., Bielsky I.F., Ross H.E., Kawamata M., Onaka T., Yanagisawa T., Kimura T., Matzuk M.M., Young L.J., Nishimori K. Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc. Natl. Acad. Sci. 2005, 102:16096-16101.
87. Thompson M.R., Callaghan P.D., Hunt G.E., Cornish J.L., McGregor I.S. A role for oxytocin and 5-HT(1A) receptors in the prosocial effects of 3,4 methylenedioxymethamphetamine ("ecstasy"). Neuroscience 2007, 146:509-514.
88. Tsujimoto M., Hattori A. The oxytocinase subfamily of M1 aminopeptidases. Biochim. Biophys. Acta 2005, 1751:9-18.
89. Uvnas-Moberg K., Hillegaart V., Alster P., Ahlenius S. Effects of 5-HT agonists, selective for different receptor subtypes, on oxytocin, CCK, gastrin and somatostatin plasma levels in the rat. Neuropharmacology 1996, 35:1635-1640.
90. Van Ijzendoorn M.H., Bakermans-Kranenburg M.J. 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 2011, (Electronic publication ahead of print).
91. Wermter A.K., Kamp-Becker I., Hesse P., Schulte-Korne G., Strauch K., Remschmidt H. Evidence for the involvement of genetic variation in the oxytocin receptor gene (OXTR) in the etiology of autistic disorders on high-functioning level. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2010, 153B:629-639.
92. Williams J.R., Insel T.R., Harbaugh C.R., Carter C.S. Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). J. Neuroendocrinol. 1994, 6:247-250.
93. Winslow J.T., Camacho F. Cholinergic modulation of a decrement in social investigation following repeated contacts between mice. Psychopharmacology 1995, 121:164-172.
94. Winslow J.T., Hearn E.F., Ferguson J., Young L.J., Matzuk M.M., Insel T.R. Infant vocalization, adult aggression and fear behavior of an oxytocin null mutant mouse. Horm. Behav. 2000, 37:145-155.
95. Wohr M., Roullet F.I., Crawley J.N. Reduced scent marking and ultrasonic vocalizations in the BTBR T+tf/J mouse model of autism. Genes Brain Behav. 2011, 10:35-43.
96. Wu S., Jia M., Ruan Y., Liu J., Guo Y., Shuang M., Gong X., Zhang Y., Yang X., Zhang D. Positive association of the oxytocin receptor gene (OXTR) with autism in the Chinese Han population. Biol. Psychiatry 2005, 58:74-77.
97. Ylisaukko-oja T., Alarcón M., Cantor R.M., Auranen M., Vanhala R., Kempas E., von Wendt L., Järvelä I., Geschwind D.H., Peltonen L. Search for autism loci by combines analysis of autism genetic resource exchange and Finish families. Ann. Neurol. 2006, 59:145-155.
98. Young L.J., Wang Z. The neurobiology of pair bonding. Nat. Neurosci. 2004, 7:1048-1054.
99. Young L.J., Lim M.M., Gingrich B., Insel T.R. Cellular mechanisms of social attachment. Horm. Behav. 2001, 40:133-138.