Sex differences in oxytocin and vasopressin: Implications for autism spectrum disorders?

CARTER, C

doi:10.1016/j.bbr.2006.08.025

Cited by 432Neuroendocrine regulation and behaviorAutism Spectrum Disorder ResearchGenetics and Neurodevelopmental Disorders

Sex differences in oxytocin and vasopressin: Implications for autism spectrum disorders?

CARTER, C·2007·Behavioural Brain Research

DOI 10.1016/j.bbr.2006.08.025

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Abstract

Autism spectrum disorders (ASD) are male-biased and characterized by deficits in social behavior and social communication, excessive anxiety or hyperreactivity to stressful experiences, and a tendency toward repetitiveness. The purpose of this review is to consider evidence for a role for two sexually dimorphic neuropeptides, oxytocin (OT) and arginine vasopressin (VP), in these features of ASD. Both VP and OT play a role in normal development. VP is androgen-dependent and of particular importance to male behavior. Excess VP or disruptions in the VP system could contribute to the male vulnerability to ASD. Alternatively, protective processes mediated via OT or the OT receptor might help to explain the relatively rare occurrence of ASD in females. Disruptions in either OT or VP or their receptors could result from genetic variation or epigenetic modifications of gene expression, especially during early development. Deficits in other developmental growth factors, such as reelin, which may in turn regulate or be regulated by OT or VP, are additional candidates for a role in ASD.

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Both animal and recent human studies suggest that central and peripheral activity of the oxytocinergic system is coordinated.
“Although the relationship between central and peripheral OT levels is not fully understood, both animal (29,66) and recent human (39) studies suggest that central and peripheral activity of the oxytocinergic system is coordinated.”
From Oxytocin and the development of parenting in humans (2010) · cites this paper as [29]
Central and peripheral oxytocin activity is coordinated.
“both animal (71) and human studies (31) suggest that central and peripheral OT activity is coordinated”
From Oxytocin administration to parent enhances infant physiological and behavioral readiness for social engagement (2012) · cites this paper as [71]
OT, released endogenously or given exogenously, has been associated with positive social behaviors, reductions in anxiety, obsessiveness and stress reactivity, the central release of AVP and other peptides such as corticotropin-releasing factor, and may serve to counter the defensive behavioral strategies associated with stressful experiences.
“As described earlier OT, released endogenously or given exogenously, has been associated with positive social behaviors, reductions in anxiety, obses-siveness and stress reactivity, the central release of AVP and other peptides such as corticotropin-releasing factor, and may serve to counter the defensive behavioral strategies associated with stressful experiences (Carter, 2007).”
From Oxytocin and vasopressin systems in genetic syndromes and neurodevelopmental disorders (2014) · cites this paper as Carter, 2007

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Reelin and glutamic acid decarboxylase 67 promoter remodeling in an epigenetic methionine-induced mouse model of schizophrenia
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Selective Serotonin Reuptake Inhibitors in Autism
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Chapter 10 Alterations in behavioral and neuroendocrine stress coping strategies in pregnant, parturient and lactating rats
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Female oxytocin gene-knockout mice, in a semi-natural environment, display exaggerated aggressive behavior
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Oxytocin causes a sustained decrease in plasma levels of corticosterone in rats
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Neonatal oxytocin manipulations have long-lasting, sexually dimorphic effects on vasopressin receptors
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Estrogens and non-reproductive behaviors related to activity and fear.
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Chapter 22 Cardiovascular effects of oxytocin
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Non‐human primate models of childhood psychopathology: the promise and the limitations
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The Central Vasopressinergic System: Examining the Opportunities for Psychiatric Drug Development
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Maternal behavior and developmental psychopathology
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Oxytocin Protects Against Sepsis-Induced Multiple Organ Damage: Role of Neutrophils
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Search for autism loci by combined analysis of Autism Genetic Resource Exchange and Finnish families
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The role of central oxytocin in obsessive compulsive disorder and related normal behavior
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Voles and vasopressin: A review of molecular, cellular, and behavioral studies of pair bonding and paternal behaviors
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Vasopressin and Oxytocin Neurons of the Human Supraoptic and Paraventricular Nucleus; Size Changes in Relation to Age and Sex
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Oxytocin decreases carrageenan induced inflammation in rats
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Neuropeptides and the social brain: potential rodent models of autism
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Serotonin regulation of aggressive behavior in male golden hamsters (Mesocricetus auratus).
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The Neurobiology of Social Affiliation and Pair Bonding
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The involvement of the vasopressin system in stress-related disorders
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Background
Sexually dimorphic expression of oxytocin binding sites in forebrain and spinal cord of the rat
Uhl-Bronner, S., Waltisperger, E., Martínez-Lorenzana, G., Condes Lara, M., & Freund-Mercier, M. J. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.05.025 · Cited by 123 · see citing works
Born to be anxious: neuroendocrine and genetic correlates of trait anxiety in HAB rats
Landgraf, R., & Wigger, A. (2003) · Stress · doi:10.1080/1025389031000104193 · Cited by 122 · see citing works
Left vagal nerve stimulation in six patients with hypothalamic hamartomas
Murphy, J. V., Wheless, J. W., & Schmoll, C. (2000) · Pediatric Neurology · doi:10.1016/s0887-8994(00)00170-3 · Cited by 121 · see citing works
Brain mechanisms underlying emotional alterations in the peripartum period in rats
Neumann, I. D. (2003) · Depression and Anxiety · doi:10.1002/da.10070 · Cited by 121 · see citing works
Receptor ontogeny and hormonal imprinting
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Extraordinary diversity in vasopressin (V1a) receptor distributions among wild prairie voles (Microtus ochrogaster): Patterns of variation and covariation
Phelps, S. M., & Young, L. J. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10902 · Cited by 116 · see citing works
Oxytocin mediates acquisition of maternally associated odor preferences in preweanling rat pups.
Nelson, E. E., & Panksepp, J. (1996) · Behavioral Neuroscience · doi:10.1037//0735-7044.110.3.583 · Cited by 113 · see citing works
Gonadal steroids have paradoxical effects on brain oxytocin receptors
Insel, T. R., Young, L., Witt, D. M., & Crews, D. (1993) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1993.tb00531.x · Cited by 113 · see citing works
The Maternal Brain
Kinsley, C. H., & Lambert, K. G. (2006) · Scientific American · doi:10.1038/scientificamerican0106-72 · Cited by 111 · see citing works
Orally active vasopressin V1a receptor antagonist, SRX251, selectively blocks aggressive behavior
Ferris, C. F., Lu, S., Messenger, T. L., Guillon, C. D., Heindel, N. D., Miller, M., KOPPEL, G. A., Bruns, F., & Simon, N. G. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.01.001 · Cited by 111 · see citing works
An Overview of SSR149415, a Selective Nonpeptide Vasopressin V1b Receptor Antagonist for the Treatment of Stress-Related Disorders
Gal, C. S., Wagnon, J., Tonnerre, B., Roux, R., Garcia, G., Griebel, G., & Aulombard, A. (2006) · CNS Drug Reviews · doi:10.1111/j.1527-3458.2005.tb00035.x · Cited by 110 · see citing works
Autism and 15q11‐q13 disorders: Behavioral, genetic, and pathophysiological issues
Dykens, E. M., Sutcliffe, J. S., & Levitt, P. R. (2004) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.20042 · Cited by 108 · see citing works
Sex differences and developmental effects of manipulations of oxytocin on alloparenting and anxiety in prairie voles
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Repetitive and ritualistic behaviour in children with Prader–Willi syndrome and children with autism
Greaves, N., Prince, E., Evans, D. W., & Charman, T. (2006) · Journal of Intellectual Disability Research · doi:10.1111/j.1365-2788.2005.00726.x · Cited by 107 · see citing works
Effects of oxytocin microinjected into the central amygdaloid nucleus and bed nucleus of stria terminalis on maternal aggressive behavior in rats
Consiglio, A. R., Borsoi, A., Pereira, G. A. M., & Lucion, A. B. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.05.002 · Cited by 106 · see citing works
Hormonal Basis of Social Conflict and Communication
Albers, H. E., Huhman, K. L., & Meisel, R. L. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50008-1 · Cited by 105 · see citing works
Postnatal oxytocin treatment and postnatal stroking of rats reduce blood pressure in adulthood
Holst, S., Uvnäs‐Moberg, K., & Petersson, M. (2002) · Autonomic Neuroscience · doi:10.1016/s1566-0702(02)00134-0 · Cited by 105 · see citing works
Molecular regulation of the oxytocin receptor in peripheral organs
Kimura, T., Saji, F., Nishimori, K., Ogita, K., Nakamura, H., Koyama, M., & Murata, Y. (2003) · Journal of Molecular Endocrinology · doi:10.1677/jme.0.0300109 · Cited by 103 · see citing works
Coping with stress in rats and mice: Differential peptidergic modulation of the amygdala-lateral septum complex
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Sex and species differences in plasma oxytocin using an enzyme immunoassay
Kramer, K. M., Cushing, B. S., Carter, C. S., Wu, J., & Ottinger, M. A. (2004) · Canadian Journal of Zoology · doi:10.1139/z04-098 · Cited by 99 · see citing works
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Chapter 19 Neural mediation of nursing and related maternal behaviors
Stern, J. M., & Lonstein, J. S. (2001) · Progress in brain research · doi:10.1016/s0079-6123(01)33020-0 · Cited by 98 · see citing works
Sex differences in the hypothalamus in the different stages of human life
Swaab, D. F., Chung, W. C. J., Kruijver, F. P. M., Hofman, M. A., & Hestiantoro, A. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(03)00059-9 · Cited by 97 · see citing works
Sexual dimorphism in the vasopressin system: Lack of an altered behavioral phenotype in female V1a receptor knockout mice
Bielsky, I. F., Hu, S.-B., & Young, L. J. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.06.005 · Cited by 92 · see citing works
Vasopressin administration modulates anxiety-related behavior in rats
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Oxytocin Receptor Binding in Female Prairie Voles: Endogenous and Exogenous Oestradiol Stimulation
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Neuropeptides and social behavior: animal models relevant to autism
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Cerebrospinal fluid levels of oxytocin in Prader–Willi syndrome: a preliminary report
Martin, A., State, M., Anderson, G. M., Kaye, W. M., Hanchett, J. M., McConaha, C. W., North, W. G., & Leckman, J. F. (1998) · Biological Psychiatry · doi:10.1016/s0006-3223(98)00190-5 · Cited by 89 · see citing works
Gender Effect on Purkinje Cell Loss in the Cerebellum of the Heterozygous Reeler Mouse
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Reelin down-regulation in mice and psychosis endophenotypes
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Neuroendocrine and behavioral response to social confrontation: residents versus intruders, active versus passive coping styles
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Axon-sparing lesions of the medial nucleus of the amygdala decrease affiliative behaviors in the prairie vole (Microtus ochrogaster): Behavioral and anatomical specificity.
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Vasopressin Release in Male and Female Rats: Effects of Gonadectomy and Treatment with Gonadal Steroid Hormones*
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Mutation screening and association analysis of six candidate genes for autism on chromosome 7q
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OXYTOCIN RECEPTOR mRNA EXPRESSION IN RAT BRAIN: IMPLICATIONS FOR BEHAVIORAL INTEGRATION AND REPRODUCTIVE SUCCESS
Ostrowski, N. L. (1998) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00070-5 · Cited by 81 · see citing works
Developmental effects of oxytocin on stress response: Single versus repeated exposure
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Androgenic Activity in Autism
Tordjman, S., Ferrari, P., Sulmont, V., Duyme, M., & Roubertoux, P. L. (1997) · American Journal of Psychiatry · doi:10.1176/ajp.154.11.1626-a · Cited by 79 · see citing works
Effects of stress on parental care are sexually dimorphic in prairie voles
Bales, K. L., Kramer, K. M., Lewis‐Reese, A. D., & Carter, C. S. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.11.002 · Cited by 78 · see citing works
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Remodeling of astrocytes, a prerequisite for synapse turnover in the adult brain? Insights from the oxytocin system of the hypothalamus
Theodosis, D. T., Trailin, A., & Poulain, D. A. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00755.2005 · Cited by 77 · see citing works
Arginine vasopressin, fever and temperature regulation
Pittman, Q. J., Chen, X., Mouihate, A., Hirasawa, M., & Martin, S. M. (1999) · Progress in brain research · doi:10.1016/s0079-6123(08)61582-4 · Cited by 75 · see citing works
Functional Genomics of Social Recognition
Choleris, E., Kavaliers, M., & Pfaff, D. W. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.0953-8194.2004.01178.x · Cited by 75 · see citing works
Oxytocin receptors in brain cortical regions are reduced in haploinsufficient (+/−) reeler mice
Liu, W., Pappas, G. D., & Carter, C. S. (2005) · Neurological Research · doi:10.1179/016164105x35602 · Cited by 73 · see citing works
Self-citation
Differing concentrations of corticotropin-releasing factor and oxytocin in the cerebrospinal fluid of bonnet and pigtail macaques
Rosenblum, L. A. (2002) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00056-7 · Cited by 73 · see citing works
Peptides associated with hyperphagia in adults with Prader–Willi syndrome before and during GH treatment
Höybye, C., Barkeling, B., Espelund, U. S., Petersson, M., & Thorén, M. C. (2003) · Growth Hormone & IGF Research · doi:10.1016/s1096-6374(03)00077-7 · Cited by 71 · see citing works
Neuronal nicotinic acetylcholine receptor subunits in autism: an immunohistochemical investigation in the thalamus
Ray, M. A., Graham, A. J., Lee, M. H., Perry, R. H., COURT, J. A., & Perry, E. K. (2005) · Neurobiology of Disease · doi:10.1016/j.nbd.2005.01.017 · Cited by 71 · see citing works
Neonatal manipulation of oxytocin affects expression of estrogen receptor alpha
Yamamoto, Y., Carter, C. S., & Cushing, B. S. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.08.065 · Cited by 70 · see citing works
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Vasopressin Differentially Modulates Non-NMDA Receptors in Vasopressin and Oxytocin Neurons in the Supraoptic Nucleus
Hirasawa, M., Mouginot, D., Kozoriz, M. G., Kombian, S. B., & Pittman, Q. J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-10-04270.2003 · Cited by 69 · see citing works
Enhanced Up‐Regulation of Corticotropin‐Releasing Hormone Gene Expression in Response to Restraint Stress in the Hypothalamic Paraventricular Nucleus of Oxytocin Gene‐Deficient Male Mice
Nomura, M., Saito, J., Ueta, Y., Muglia, L. J., Pfaff, D. W., & Ogawa, S. (2003) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2003.01095.x · Cited by 69 · see citing works
Oxytocinergic regulation of cardiovascular function: studies in oxytocin-deficient mice
Michelini, L. C., Marcelo, M. C., Amico, J. A., & Morris, M. (2003) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00774.2002 · Cited by 69 · see citing works
Release of vasopressin and oxytocin by paraventricular stimulation in rats
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Brain Sexual Dimorphism and Sex Differences in Parental and Other Social Behaviorsa
Vries, G. J. D., & Villalba, C. (1997) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1997.tb51926.x · Cited by 68 · see citing works
Vasopressin interactions with oxytocin in the control of female sexual behavior
Pedersen, C. A., & Boccia, M. L. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.01.002 · Cited by 68 · see citing works
Neuropeptides in Hypothalamic Neuronal Disorders
Swaab, D. F. (2004) · International review of cytology · doi:10.1016/s0074-7696(04)40003-5 · Cited by 68 · see citing works
Vasopressin and pair-bond formation: genes to brain to behavior.
Nair, H. P., & Young, L. J. (2006) · Physiology · doi:10.1152/physiol.00049.2005 · Cited by 68 · see citing works
Adolescent stress and neural plasticity in hamsters: a vasopressin‐serotonin model of inappropriate aggressive behaviour
Ferris, C. F. (2000) · Experimental Physiology · doi:10.1111/j.1469-445x.2000.tb00011.x · Cited by 65 · see citing works
Brief Report: Non-Random X Chromosome Inactivation in Females with Autism
Talebizadeh, Z., Bittel, D. C., Veatch, O. J., Kibiryeva, N., & Butler, M. G. (2005) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-005-0011-z · Cited by 65 · see citing works
Receptor‐mediated uterine effects of vasopressin and oxytocin in nonpregnant women
Bossmar, T., Åkerlund, M., Szamatowicz, J., LAUDAŃSKI, T., Fantoni, G., & Maggi, M. (1995) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1995.tb10880.x · Cited by 64 · see citing works
Sex differences among oxytocin-immunoreactive neuronal systems in the mouse hypothalamus.
Hu, H., Gf, J., & Jd, C. (1990) · PubMed · Cited by 63 · see citing works
Suppression of Proinflammatory Cytokines Interleukin-1β and Tumor Necrosis Factor-α in Astrocytes by a V1Vasopressin Receptor Agonist: A cAMP Response Element-Binding Protein-Dependent Mechanism
Zhao, L., & Brinton, R. D. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4922-03.2004 · Cited by 62 · see citing works
The oxytocin receptor: a target for steroid hormones
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Neuropeptides and non‐human primate social deficits associated with pathogenic rearing experience
Winslow, J. (2004) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2004.03.003 · Cited by 56 · see citing works

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Autism spectrum disorder
Lord, C., Brugha, T. S., Charman, T., Cusack, J., Dumas, G., Frazier, T., Jones, E. J. H., Jones, R. M., Pickles, A., State, M. W., et al. (2020) · Nature Reviews Disease Primers · doi:10.1038/s41572-019-0138-4 · Cited by 1,859 · see citing works
Autism‐like behavioral phenotypes in BTBR T+tf/J mice
McFarlane, H. G., Kusek, G. K., Yang, M., Phoenix, J. L., Bolivar, V. J., & Crawley, J. N. (2008) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2007.00330.x · Cited by 812 · see citing works
Oxytocin, vasopressin, and human social behavior
Heinrichs, M., von Dawans, B., & Domes, G. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.005 · Cited by 799 · see citing works
Psychobiological mechanisms underlying the social buffering of the hypothalamic-pituitary-adrenocortical axis: a review of animal models and human studies across development
Hostinar, C. E., Sullivan, R. M., & Gunnar, M. R. (2014) · Psychological Bulletin · doi:10.1037/a0032671 · Cited by 739 · see citing works
Oxytocin pathways and the evolution of human behavior
Carter, C. S. (2014) · Annual Review of Psychology · doi:10.1146/annurev-psych-010213-115110 · Cited by 714 · see citing works
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Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent–infant contact
Feldman, R., Gordon, I., Schneiderman, I., Weisman, O., & Zagoory-Sharon, O. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.01.013 · Cited by 638 · see citing works
The Peptide That Binds: A Systematic Review of Oxytocin and its Prosocial Effects in Humans
MacDonald, K., & MacDonald, T. M. (2010) · Harvard Review of Psychiatry · doi:10.3109/10673220903523615 · Cited by 585 · see citing works
Genomic and epigenetic evidence for oxytocin receptor deficiency in autism
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., et al. (2009) · BMC Medicine · doi:10.1186/1741-7015-7-62 · Cited by 576 · see citing works
Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior
Dumais, K. M., & Veenema, A. H. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.04.003 · Cited by 520 · see citing works
“Even so, these studies overall suggest a correlation between OTR SNPs and differences in social processing, social behaviors, and social functioning in both sexes, with some important sex differences that perhaps may be informative in understanding the potential role of the OTR in mediating sex differences in the susc…”
Background
Effects of intranasal oxytocin on emotional face processing in women
Domes, G., Lischke, A., Berger, C., Grossmann, A., Hauenstein, K., Heinrichs, M., & Herpertz, S. C. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.06.016 · Cited by 521 · see citing works
Vasopressin: Behavioral roles of an “original” neuropeptide
Caldwell, H. K., Lee, H.-J., Macbeth, A. H., & Young, W. S. (2008) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.10.007 · Cited by 504 · see citing works
Neuropeptides and social behaviour: effects of oxytocin and vasopressin in humans
HEINRICHS, M., & DOMES, G. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00428-7 · Cited by 479 · see citing works
Oxytocin and the development of parenting in humans
Gordon, I., Zagoory-Sharon, O., Leckman, J. F., & Feldman, R. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.02.005 · Cited by 469 · see citing works
Acute effects of steroid hormones and neuropeptides on human social-emotional behavior: A review of single administration studies
Bos, P. A., Panksepp, J., Bluthé, R.-M., & Honk, J. V. (2012) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2011.01.002 · Cited by 429 · see citing works
Coregulation, Dysregulation, Self-Regulation: An Integrative Analysis and Empirical Agenda for Understanding Adult Attachment, Separation, Loss, and Recovery
Sbarra, D. A., & Hazan, C. (2008) · Personality and Social Psychology Review · doi:10.1177/1088868308315702 · Cited by 427 · see citing works
Oxytocin Attenuates Affective Evaluations of Conditioned Faces and Amygdala Activity
Petrovic, P., Kalisch, R., Singer, T., & Dolan, R. J. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4572-07.2008 · Cited by 424 · see citing works
“It has been suggested that an underlying cause for deficits in social interaction in autistics is a malfunctioning oxytocin system (Bartz and Hollander, 2006; Hammock and Young, 2006; Carter, 2007; Heinrichs and Gaab, 2007), evidenced in lower oxytocin levels than in normal controls (Modahl et al.”
BackgroundInfluential
An investigation of the ‘female camouflage effect’ in autism using a computerized ADOS-2 and a test of sex/gender differences
Rynkiewicz, A., Schuller, B., Marchi, E., Piana, S., Camurri, A., Lassalle, A., & Baron-Cohen, S. (2016) · Molecular Autism · doi:10.1186/s13229-016-0073-0 · Cited by 404 · see citing works
Specifying the Neurobiological Basis of Human Attachment: Brain, Hormones, and Behavior in Synchronous and Intrusive Mothers
Atzil, S., Hendler, T., & Feldman, R. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.172 · Cited by 399 · see citing works
Is oxytocin “nature’s medicine”
Carter, C. S., Kenkel, W. M., MacLean, E. L., Wilson, S. R., Perkeybile, A. M., Yee, J. R., Ferris, C. F., Nazarloo, H. P., Porges, S. W., Davis, J. M., et al. (2020) · Pharmacological Reviews · doi:10.1124/pr.120.019398 · Cited by 394 · see citing works
Self-citation
Sex differences in autism spectrum disorder: a review
Ferri, S. L., Abel, T., & Brodkin, E. S. (2018) · Current Psychiatry Reports · doi:10.1007/s11920-018-0874-2 · Cited by 392 · see citing works
Oxytocin, vasopressin and sociality
CARTER, C., GRIPPO, A., POURNAJAFINAZARLOO, H., RUSCIO, M., & PORGES, S. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00427-5 · Cited by 380 · see citing works
Self-citation
Pharmacologic rescue of impaired cognitive flexibility, social deficits, increased aggression, and seizure susceptibility in oxytocin receptor null mice: a neurobehavioral model of autism
Sala, M., Braida, D., Lentini, D., Busnelli, M., Bulgheroni, E., Capurro, V., Finardi, A., Donzelli, A., Pattini, L., Rubino, T., et al. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.12.022 · Cited by 375 · see citing works
Association between the oxytocin receptor (OXTR) gene and autism: relationship to Vineland Adaptive Behavior Scales and cognition
Lerer, E., Levi, S., Salomon, S., Darvasi, A., Yirmiya, N., & Ebstein, R. P. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002087 · Cited by 349 · see citing works
Why Does Writing About Important Values Reduce Defensiveness?: Self-Affirmation and the Role of Positive Other-Directed Feelings
Crocker, J., Niiya, Y., & Mischkowski, D. (2008) · Psychological Science · doi:10.1111/j.1467-9280.2008.02150.x · Cited by 345 · see citing works
Oxytocin enhances brain function in children with autism
Gordon, I., Vander Wyk, B. C., Bennett, R. H., Cordeaux, C., Lucas, M. V., Eilbott, J. A., Zagoory-Sharon, O., Leckman, J. F., Feldman, R., & Pelphrey, K. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1312857110 · Cited by 336 · see citing works
Dopaminergic-neuropeptide interactions in the social brain
Skuse, D. H., & Gallagher, L. (2009) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2008.09.007 · Cited by 340 · see citing works
Autism Symptoms and Internalizing Psychopathology in Girls and Boys with Autism Spectrum Disorders
Solomon, M., Miller, M., Taylor, S. L., Hinshaw, S. P., & Carter, C. S. (2012) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-011-1215-z · Cited by 326 · see citing works
Self-citation
Oxytocin: Behavioral Associations and Potential as a Salivary Biomarker
SUE CARTER, C., POURNAJAFI‐NAZARLOO, H., KRAMER, K. M., ZIEGLER, T. E., WHITE‐TRAUT, R., BELLO, D., & SCHWERTZ, D. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1384.006 · Cited by 323 · see citing works
The Steroid/Peptide Theory of Social Bonds: Integrating testosterone and peptide responses for classifying social behavioral contexts
van Anders, S. M., Goldey, K. L., & Kuo, P. X. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.06.001 · Cited by 321 · see citing works
The oxytocin receptor (OXTR) contributes to prosocial fund allocations in the dictator game and the social value orientations task
Israel, S., Lerer, E., Shalev, I., Uzefovsky, F., Riebold, M., Laiba, E., Bachner-Melman, R., Maril, A., Bornstein, G., Knafo, A., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005535 · Cited by 278 · see citing works
Associations between the oxytocin receptor gene (OXTR) and affect, loneliness and intelligence in normal subjects
Lucht, M. J., Barnow, S., Sonnenfeld, C., Rosenberger, A., Grabe, H. J., Schroeder, W., Völzke, H., Freyberger, H. J., Herrmann, F. H., Kroemer, H., et al. (2009) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2009.04.004 · Cited by 271 · see citing works
Review of gender differences in core symptomatology in autism spectrum disorders
Rivet, T. T., & Matson, J. L. (2011) · Research in Autism Spectrum Disorders · doi:10.1016/j.rasd.2010.12.003 · Cited by 258 · see citing works
Effects of intranasal oxytocin on the neural basis of face processing in autism spectrum disorder
Domes, G., Heinrichs, M., Kumbier, E., Grossmann, A., Hauenstein, K., & Herpertz, S. C. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.02.007 · Cited by 255 · see citing works
The cross-generation transmission of oxytocin in humans
Feldman, R., Gordon, I., & Zagoory-Sharon, O. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.06.005 · Cited by 256 · see citing works
Oxytocin increases eye contact during a real-time, naturalistic social interaction in males with and without autism
Auyeung, B., Lombardo, M. V., Heinrichs, M., Chakrabarti, B., Sule, A., Deakin, J. B., Bethlehem, R. A. I., Dickens, L., Mooney, N., Sipple, J. A. N., et al. (2015) · Translational Psychiatry · doi:10.1038/tp.2014.146 · Cited by 234 · see citing works
Oxytocin administration to parent enhances infant physiological and behavioral readiness for social engagement
Weisman, O., Zagoory-Sharon, O., & Feldman, R. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.06.011 · Cited by 240 · see citing works
Methylation of the oxytocin receptor gene and oxytocin blood levels in the development of psychopathy
Dadds, M. R., Moul, C., Cauchi, A., Dobson-Stone, C., Hawes, D. J., Brennan, J., & Ebstein, R. E. (2014) · Development and Psychopathology · doi:10.1017/s0954579413000497 · Cited by 230 · see citing works
The biology of paternal care in human and nonhuman primates
Fernandez-Duque, E., Valeggia, C. R., & Mendoza, S. P. (2009) · Annual Review of Anthropology · doi:10.1146/annurev-anthro-091908-164334 · Cited by 232 · see citing works
Oxytocin enhances processing of positive versus negative emotional information in healthy male volunteers
Di Simplicio, M., Massey-Chase, R., Cowen, P., & Harmer, C. (2009) · Journal of Psychopharmacology · doi:10.1177/0269881108095705 · Cited by 229 · see citing works
Intranasal oxytocin enhances emotion recognition from dynamic facial expressions and leaves eye-gaze unaffected
Lischke, A., Berger, C., Prehn, K., Heinrichs, M., Herpertz, S. C., & Domes, G. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.07.015 · Cited by 221 · see citing works
Is stress affecting our ability to tune into others? Evidence for gender differences in the effects of stress on self-other distinction
Tomova, L., von Dawans, B., Heinrichs, M., Silani, G., & Lamm, C. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.02.006 · Cited by 224 · see citing works
Oxytocin and social motivation
Gordon, I., Martin, C., Feldman, R., & Leckman, J. F. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.07.007 · Cited by 211 · see citing works
Mitigation of Sociocommunicational Deficits of Autism Through Oxytocin-Induced Recovery of Medial Prefrontal Activity: A Randomized Trial
Watanabe, T., Abe, O., Kuwabara, H., Yahata, N., Takano, Y., Iwashiro, N., Natsubori, T., Aoki, Y., Takao, H., Kawakubo, Y., et al. (2014) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.3181 · Cited by 183 · see citing works
Consequences of Early Experiences and Exposure to Oxytocin and Vasopressin Are Sexually Dimorphic
Carter, C. S., Boone, E. M., Pournajafi-Nazarloo, H., & Bales, K. L. (2009) · Developmental Neuroscience · doi:10.1159/000216544 · Cited by 176 · see citing works
Self-citation
Human neuroimaging of oxytocin and vasopressin in social cognition
Zink, C. F., & Meyer-Lindenberg, A. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.016 · Cited by 176 · see citing works
From ultrasocial to antisocial: A role for oxytocin in the acute reinforcing effects and long-term adverse consequences of drug use?
McGregor, I. S., Callaghan, P. D., & Hunt, G. E. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.132 · Cited by 171 · see citing works
The extreme male brain revisited: gender coherence in adults with autism spectrum disorder
Bejerot, S., Eriksson, J. M., Bonde, S., Carlström, K., Humble, M. B., & Eriksson, E. (2012) · British Journal of Psychiatry · doi:10.1192/bjp.bp.111.097899 · Cited by 161 · see citing works
Association between the oxytocin receptor gene and amygdalar volume in healthy adults
Inoue, H., Yamasue, H., Tochigi, M., Abe, O., Liu, X., Kawamura, Y., Takei, K., Suga, M., Yamada, H., Rogers, M. A., et al. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.07.019 · Cited by 164 · see citing works
Oxytocin, cortisol, and triadic family interactions
Gordon, I., Zagoory-Sharon, O., Leckman, J. F., & Feldman, R. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.08.008 · Cited by 158 · see citing works
Brief report: theatre as therapy for children with autism spectrum disorder
Corbett, B. A., Gunther, J. R., Comins, D., Price, J., Ryan, N., Simon, D., Schupp, C. W., & Rios, T. (2011) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-010-1064-1 · Cited by 160 · see citing works
Oxytocin Promotes Facial Emotion Recognition and Amygdala Reactivity in Adults with Asperger Syndrome
Domes, G., Kumbier, E., Heinrichs, M., & Herpertz, S. C. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2013.254 · Cited by 160 · see citing works
Sex-specific modulation of juvenile social play behavior by vasopressin and oxytocin depends on social context
Bredewold, R., Smith, C. J. W., Dumais, K. M., & Veenema, A. H. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00216 · Cited by 157 · see citing works
Oxytocin and Vasopressin in Children and Adolescents With Autism Spectrum Disorders: Sex Differences and Associations With Symptoms
Miller, M., Bales, K. L., Taylor, S. L., Yoon, J., Hostetler, C. M., Carter, C. S., & Solomon, M. (2013) · Autism Research · doi:10.1002/aur.1270 · Cited by 151 · see citing works
Self-citation
Personality and self-insight in individuals with autism spectrum disorder.
Schriber, R. A., Robins, R. W., & Solomon, M. (2014) · Journal of Personality and Social Psychology · doi:10.1037/a0034950 · Cited by 150 · see citing works
Integrative Approaches Utilizing Oxytocin to Enhance Prosocial Behavior: From Animal and Human Social Behavior to Autistic Social Dysfunction
Yamasue, H., Yee, J. R., Hurlemann, R., Rilling, J. K., Chen, F. S., Meyer-Lindenberg, A., & Tost, H. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3327-12.2012 · Cited by 149 · see citing works
Oxytocin and vasopressin receptor distributions in a solitary and a social species of tuco‐tuco ( Ctenomys haigi and Ctenomys sociabilis )
Beery, A. K., Lacey, E. A., & Francis, D. D. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21638 · Cited by 144 · see citing works
An investigation of plasma and salivary oxytocin responses in breast- and formula-feeding mothers of infants
Grewen, K. M., Davenport, R. E., & Light, K. C. (2010) · Psychophysiology · doi:10.1111/j.1469-8986.2009.00968.x · Cited by 146 · see citing works
The oxytocin analogue carbetocin prevents emotional impairment and stress-induced reinstatement of opioid-seeking in morphine-abstinent mice
Zanos, P., Georgiou, P., Wright, S. R., Hourani, S. M., Kitchen, I., Winsky-Sommerer, R., & Bailey, A. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2013.285 · Cited by 133 · see citing works
Oxytocin and experimental therapeutics in autism spectrum disorders
BARTZ, J., & HOLLANDER, E. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00435-4 · Cited by 139 · see citing works
A psychobiological rationale for oxytocin in the treatment of posttraumatic stress disorder
Olff, M., Langeland, W., Witteveen, A., & Denys, D. (2010) · CNS Spectrums · doi:10.1017/s109285290000047x · Cited by 135 · see citing works
The role of oxytocin and oxytocin receptor gene variants in childhood‐onset aggression
Malik, A. I., Zai, C. C., Abu, Z., Nowrouzi, B., & Beitchman, J. H. (2012) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2012.00776.x · Cited by 128 · see citing works
Oxytocin and vasopressin are dysregulated in Williams Syndrome, a genetic disorder affecting social behavior
Dai, L., Carter, C. S., Ying, J., Bellugi, U., Pournajafi-Nazarloo, H., & Korenberg, J. R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038513 · Cited by 119 · see citing works
Self-citation
Intranasal oxytocin in the treatment of autism spectrum disorders: A multilevel meta-analysis
Huang, Y., Huang, X., Ebstein, R. P., & Yu, R. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.12.028 · Cited by 119 · see citing works
Impact of prosocial neuropeptides on human brain function
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Authors: CARTER, C.
Affiliations: University of Illinois Chicago (US)
Corresponding author: CARTER, C
ORCID: CARTER, C
Venue: Behavioural Brain Research
Publisher: Elsevier BV
Published: 2007-01-10
Volume: 176
Issue: 1
Pages: 170-186
ISSN: 0166-4328 (ISSN-L)
DOI: 10.1016/j.bbr.2006.08.025
OpenAlex: W2170760423
Cited by: 432
References: 238
Citations by year: 2026: 6 · 2025: 11 · 2024: 8 · 2023: 13 · 2022: 9 · 2021: 16 · 2020: 15 · 2019: 24 · 2018: 23 · 2017: 21 · 2016: 31 · 2015: 31 · 2014: 32 · 2013: 39 · 2012: 25
FWCI: 28.42
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Behavioural Brain Research (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health
National Institute of Mental Health (R01MH073022, MH073022, MH 072935, R01MH072935)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (P01HD038490, HD38490)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
Keywords: autism spectrum disorder, oxytocin, vasopressin, sex differences, androgen dependence, oxytocin receptor, reelin, epigenetic gene expression, social behavior deficits, anxiety, female autism
MeSH terms: Reelin Protein, Amygdala, Animals, Arginine Vasopressin, Autistic Disorder, Female, Humans, Male, Oxytocin, Sex Factors

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Sex differences in oxytocin and vasopressin: Implications for autism spectrum disorders?

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