Oxytocin Administration to Parent Enhances Infant Physiological and Behavioral Readiness for Social Engagement

BACKGROUND The social milieu provides the context for the organism's survival, endurance, and adaptation. In mammals, social participation originates within the parent-infant bond and is supported by the oxytocin (OT) system, whose functioning is transmitted from parent to child through patterns of parental care. Human studies indicate that OT administration increases affiliative behavior, including trust, empathy, and social reciprocity. Here, we examine whether OT administration to parent can enhance physiological and behavioral processes that support parental social engagement but, moreover, can have parallel effects on the infant. METHODS Utilizing a double-blind, placebo-controlled crossover design, 35 fathers and their 5-month-old infants were observed twice following administration of OT or placebo to father in the face-to-face still-face paradigm. Parent and infant salivary OT were assessed at multiple time points, respiratory sinus arrhythmia (RSA) was measured in the three face-to-face still-face episodes, and social behaviors of the parent and child were micro-coded for indices of social engagement. RESULTS Oxytocin administration increased father salivary OT, RSA during free play, and key parenting behaviors that support parental-infant bonding. Parallel increases were also found in the infant's salivary OT, RSA response, and engagement behavior, including social gaze, exploration, and social reciprocity. CONCLUSIONS Results are the first to demonstrate that OT administration to one attachment partner can have parallel effects on the other and underscore the role of OT in the cross-generation transmission of human social participation. Findings have translational implications for conditions associated with early risk for social-emotional growth, including autism and prematurity, without the need to administer drugs to young infants.

[1]  K. Grewen,et al.  An investigation of plasma and salivary oxytocin responses in breast- and formula-feeding mothers of infants. , 2010, Psychophysiology.

[2]  Shaul Shalvi,et al.  References and Notes Supporting Online Material Materials and Methods Som Text Figs. S1 to S16 References the Neuropeptide Oxytocin Regulates Parochial Altruism in Intergroup Conflict among Humans , 2022 .

[3]  M. Bornstein,et al.  Physiological self-regulation and information processing in infancy: cardiac vagal tone and habituation. , 2000, Child development.

[4]  Michael E. Lamb,et al.  The role of the father in child development, 4th ed. , 2004 .

[5]  L. Young Being Human: Love: Neuroscience reveals all , 2009, Nature.

[6]  S. Calkins,et al.  Infants' vagal regulation in the still-face paradigm is related to dyadic coordination of mother-infant interaction. , 2004, Developmental psychology.

[7]  Caroline F. Zink,et al.  Human neuroimaging of oxytocin and vasopressin in social cognition , 2012, Hormones and Behavior.

[8]  Peter A. Bos,et al.  Acute effects of steroid hormones and neuropeptides on human social–emotional behavior: A review of single administration studies , 2012, Frontiers in Neuroendocrinology.

[9]  E. Cone,et al.  Comparison of heroin and cocaine concentrations in saliva with concentrations in blood and plasma. , 1995, Journal of analytical toxicology.

[10]  Orna Zagoory-Sharon,et al.  Evidence for a Neuroendocrinological Foundation of Human Affiliation , 2007, Psychological science.

[11]  L. Sroufe,et al.  Attachment and development: A prospective, longitudinal study from birth to adulthood , 2005, Attachment & human development.

[12]  S. Porges The polyvagal perspective , 2007, Biological Psychology.

[13]  Douglas A. Granger,et al.  Oxytocin is not a valid biomarker when measured in saliva by immunoassay , 2005, Physiology & Behavior.

[14]  James A. Levine,et al.  The Role of the Father in Child Development , 1985 .

[15]  C. Carter,et al.  Sex differences in oxytocin and vasopressin: Implications for autism spectrum disorders? , 2007, Behavioural Brain Research.

[16]  Michael X. Cohen,et al.  Oxytocin Enhances Amygdala-Dependent, Socially Reinforced Learning and Emotional Empathy in Humans , 2010, The Journal of Neuroscience.

[17]  W. Guo,et al.  Oxytocin is expressed by both intrinsic sensory and secretomotor neurons in the enteric nervous system of guinea pig , 2011, Cell and Tissue Research.

[18]  R. Ebstein,et al.  Sensitive Parenting Is Associated with Plasma Oxytocin and Polymorphisms in the OXTR and CD38 Genes , 2012, Biological Psychiatry.

[19]  S. Herpertz,et al.  Oxytocin Improves “Mind-Reading” in Humans , 2007, Biological Psychiatry.

[20]  Thomas R Insel,et al.  The Challenge of Translation in Social Neuroscience: A Review of Oxytocin, Vasopressin, and Affiliative Behavior , 2010, Neuron.

[21]  S. Pollak,et al.  Early experience in humans is associated with changes in neuropeptides critical for regulating social behavior. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[22]  R. Feldman From biological rhythms to social rhythms: Physiological precursors of mother-infant synchrony. , 2006, Developmental psychology.

[23]  Ruth Feldman,et al.  Parent-infant synchrony and the social-emotional development of triplets. , 2004, Developmental psychology.

[24]  W. Malarkey,et al.  Marital behavior, oxytocin, vasopressin, and wound healing , 2010, Psychoneuroendocrinology.

[25]  S. Porges Cardiac vagal tone: A physiological index of stress , 1995, Neuroscience & Biobehavioral Reviews.

[26]  S. Porges,et al.  Mechanisms, mediators, and adaptive consequences of caregiving , 2011 .

[27]  Ilanit Gordon,et al.  Natural variations in maternal and paternal care are associated with systematic changes in oxytocin following parent–infant contact , 2010, Psychoneuroendocrinology.

[28]  P. Churchland,et al.  Modulating social behavior with oxytocin: How does it work? What does it mean? , 2012, Hormones and Behavior.

[29]  U. Fischbacher,et al.  Oxytocin increases trust in humans , 2005, Nature.

[30]  Orna Zagoory-Sharon,et al.  Intranasal oxytocin administration is reflected in human saliva , 2012, Psychoneuroendocrinology.

[31]  A. Serretti,et al.  Influence of postpartum onset on the course of mood disorders , 2006, BMC psychiatry.

[32]  Ruth Feldman,et al.  Neonatal State Organization, Neuromaturation, Mother-Infant Interaction, and Cognitive Development in Small-for-Gestational-Age Premature Infants , 2006, Pediatrics.

[33]  Bar-Ilan Parent–Infant Synchrony Biological Foundations and Developmental Outcomes , 2007 .

[34]  Larry J. Young,et al.  Oxytocin and the neural mechanisms regulating social cognition and affiliative behavior , 2009, Frontiers in Neuroendocrinology.

[35]  N. Bolger,et al.  Social effects of oxytocin in humans: context and person matter , 2011, Trends in Cognitive Sciences.

[36]  K. Light,et al.  Salivary levels of oxytocin remain elevated for more than two hours after intranasal oxytocin administration. , 2012, Neuro endocrinology letters.

[37]  Carol Carter Porges Neuroendocrine perspectives on social attachment and love , 1998 .

[38]  D. Hellhammer,et al.  Plasma Oxytocin Concentration during Pregnancy is associated with Development of Postpartum Depression , 2011, Neuropsychopharmacology.

[39]  R. Feldman Oxytocin and social affiliation in humans , 2012, Hormones and Behavior.

[40]  Peter Kirsch,et al.  Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine , 2011, Nature Reviews Neuroscience.

[41]  Bar-Ilan,et al.  INFANT – MOTHER AND INFANT – FATHER SYNCHRONY : THE COREGULATION OF POSITIVE AROUSAL , 2003 .

[42]  Jan Born,et al.  Sniffing neuropeptides: a transnasal approach to the human brain , 2002, Nature Neuroscience.

[43]  M. Lamb,et al.  Attachment and bonding: a new synthesis , 2005 .

[44]  Toni E Ziegler,et al.  Oxytocin: behavioral associations and potential as a salivary biomarker. , 2007, Annals of the New York Academy of Sciences.

[45]  Talma Hendler,et al.  Specifying the Neurobiological Basis of Human Attachment: Brain, Hormones, and Behavior in Synchronous and Intrusive Mothers , 2011, Neuropsychopharmacology.

[46]  S. Calkins,et al.  Mother-infant vagal regulation in the face-to-face still-face paradigm is moderated by maternal sensitivity. , 2009, Child development.

[47]  Ian B. Hickie,et al.  Intranasal Oxytocin Improves Emotion Recognition for Youth with Autism Spectrum Disorders , 2010, Biological Psychiatry.

[48]  R. Feldman,et al.  Mother and infant coordinate heart rhythms through episodes of interaction synchrony. , 2011, Infant behavior & development.

[49]  Orna Zagoory-Sharon,et al.  The cross-generation transmission of oxytocin in humans , 2010, Hormones and Behavior.

[50]  B. McEwen Brain-fluid barriers: relevance for theoretical controversies regarding vasopressin and oxytocin memory research. , 2004, Advances in pharmacology.

[51]  A. Fleming,et al.  Neurobiology of mother–infant interactions: experience and central nervous system plasticity across development and generations , 1999, Neuroscience & Biobehavioral Reviews.

[52]  A. Stein,et al.  Paternal depression in the postnatal period and child development: a prospective population study , 2005, The Lancet.

[53]  C. Feinstein,et al.  Plasma oxytocin levels in autistic children , 1998, Biological Psychiatry.

[54]  M. Meaney,et al.  Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. , 2001, Annual review of neuroscience.

[55]  Jaak Panksepp,et al.  Brain Substrates of Infant–Mother Attachment: Contributions of Opioids, Oxytocin, and Norepinephrine , 1998, Neuroscience & Biobehavioral Reviews.

[56]  Michael J Meaney,et al.  Epigenetics and the biological definition of gene x environment interactions. , 2010, Child development.

[57]  Orna Zagoory-Sharon,et al.  Maternal and paternal plasma, salivary, and urinary oxytocin and parent-infant synchrony: considering stress and affiliation components of human bonding. , 2011, Developmental science.

[58]  D. Watson,et al.  Development and validation of brief measures of positive and negative affect: the PANAS scales. , 1988, Journal of personality and social psychology.

[59]  Ulrike Ehlert,et al.  Intranasal Oxytocin Increases Positive Communication and Reduces Cortisol Levels During Couple Conflict , 2009, Biological Psychiatry.

[60]  M. Heinrichs,et al.  The acute effects of intranasal oxytocin administration on endocrine and sexual function in males , 2008, Psychoneuroendocrinology.

[61]  Ruth Feldman,et al.  Touch attenuates infants' physiological reactivity to stress. , 2010, Developmental science.

[62]  L. Adamson,et al.  The Still Face: A History of a Shared Experimental Paradigm , 2003 .

[63]  M. Meaney,et al.  Naturally Occurring Differences in Maternal Care are Associated with the Expression of Oxytocin and Vasopressin (V1a) Receptors: Gender Differences , 2002, Journal of neuroendocrinology.

[64]  R. White-Traut,et al.  Detection of salivary oxytocin levels in lactating women. , 2009, Developmental psychobiology.

[65]  Ilanit Gordon,et al.  Oxytocin and the Development of Parenting in Humans , 2010, Biological Psychiatry.

[66]  M. Bakermans-Kranenburg,et al.  Oxytocin receptor (OXTR) and serotonin transporter (5-HTT) genes associated with observed parenting. , 2008, Social cognitive and affective neuroscience.

[67]  S. Porges,et al.  Social Engagement and Attachment , 2003, Annals of the New York Academy of Sciences.

[68]  H. Engeland,et al.  Intranasal oxytocin increases fathers’ observed responsiveness during play with their children: A double-blind within-subject experiment , 2010, Psychoneuroendocrinology.

[69]  I. Neumann Brain Oxytocin: A Key Regulator of Emotional and Social Behaviours in Both Females and Males , 2008, Journal of neuroendocrinology.

[70]  Ruth Feldman,et al.  Infant-mother and infant-father synchrony: The coregulation of positive arousal. , 2003 .

[71]  G. J. Vries,et al.  Sex differences in the parental behavior of rodents , 2000, Neuroscience & Biobehavioral Reviews.

[72]  Jamil Zaki,et al.  Oxytocin Selectively Improves Empathic Accuracy , 2010, Psychological science.