The biology of mammalian parenting and its effect on offspring social development
Open accessAbstract
Parents know the transformative nature of having and caring for a child. Among many mammals, giving birth leads from an aversion to infant stimuli to irresistible attraction. Here, we review the biological mechanisms governing this shift in parental motivation in mammals. Estrogen and progesterone prepare the uterus for embryo implantation and placental development. Prolactin stimulates milk production, whereas oxytocin initiates labor and triggers milk ejection during nursing. These same molecules, interacting with dopamine, also activate specific neural pathways to motivate parents to nurture, bond with, and protect their offspring. Parenting in turn shapes the neural development of the infant social brain. Recent work suggests that many of the principles governing parental behavior and its effect on infant development are conserved from rodent to humans.
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Ewes form selective bonds based on olfactory recognition of their offspring within 30 min of birth and will reject foreign lambs from nursing.
“Ewes form selective bonds based on olfactory recognition of their offspring within 30 min of birth and will reject foreign lambs from nursing.”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [5]
The section “Oxytocin and parenting in rodents and sheep” states that sheep form strong, selective mother–infant bonds. It does not say that the bonds depend on olfactory recognition, form within 30 minutes of birth, or cause ewes to reject foreign lambs from nursing. Page numbers are unavailable in our copy. (LLM, conf=0.88)
Experimental — accuracy not yet measuredMother-infant bonding enables the ongoing maternal drive to care for young, improving long-term outcomes for offspring.
“Mother–infant bonding enables the ongoing maternal drive to care for one’s young, thus improving long-term outcomes for offspring [5,20].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [5]
The ‘Oxytocin and parenting in rodents and sheep’ section (page not provided) says oxytocin influences both maternal motivation and mother–infant attachment, but does not say that bonding itself sustains the drive to care. The Abstract (page not provided) says parental nurturing has long-term effects on offspring development; it does not establish that bonding improves long-term outcomes in general. (LLM, conf=0.85)
Experimental — accuracy not yet measuredAnimal models of pair bonding, particularly monogamous prairie voles, provide insights into the neurobiological processes underlying love.
“Considerable insights have been gained into the neural mechanisms driving the evolutionary antecedents of love by studies in animal models of pair bonding, particularly in monogamous species such as prairie voles (Microtus ochrogaster).”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [5]
Parental behaviors generally involve oxytocin, although some aspects such as nest building instead require vasopressin.
“Parental behaviors generally involve oxytocin (Rilling & Young 2014), although some aspects such as nest building instead require vasopressin”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Rilling & Young 2014
Rodents and primates exhibit behavioral mimicking, a precursor of human social synchrony.
“Social synchrony is an evolutionary-ancient mechanism that binds members into a social group; rodents15 and primates16,17 exhibit behavioral mimicking, a precursor of human social synchrony, and in both, familiarity with conspecific bolsters behavioral matching18.”
From Brain-to-Brain Synchrony during Naturalistic Social Interactions (2017) · cites this paper as [15]
Central oxytocin signalling is crucial for the onset of maternal nurturing behaviour in rats.
“Work in rats has demonstrated that central OT signalling is crucial for the onset of maternal nurturing behaviour (1,2).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [1]
Oxytocin receptor signaling influences several social behaviors in animals, including maternal care and bonding, social reward and gregariousness, social recognition, and pair bonding in monogamous species.
“OXTR affects a range of social behaviors in animals including maternal nurturing and bonding (1, 2), social reward and gregariousness (3, 4), social recognition (5), and pair bonding in monogamous species (6–8).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [1]
Noncoding SNPs in the human OXTR are associated with pair bonding, parenting, face recognition, and autism.
“Single nucleotide polymorphisms (SNPs) in noncoding regions of the human OXTR have been associated with pair bonding behaviors (19), parenting (1), face recognition skills (20), and autism (21).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [1]
Early-life OT signaling, likely influenced by parental nurturing and attachment behaviors, can help establish the neural networks needed later in life to form adult social bonds.
“early-life OT signaling, which is likely influenced by parental nurturing and attachment behaviors, can help establish the neural networks needed later in life to form adult social bonds”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Rilling and Young 2014
Some behavioral effects of oxytocin and vasopressin are functionally linked to their peripheral function: oxytocin promotes birth and nursing but also parental nurturing, while vasopressin modulates urine production and also territorial behavior involving urine and scent marking.
“Some of the behavioral effects of OXT and AVP are functionally linked to their peripheral function, as OXT promotes birth and nursing but also parental nurturing, while AVP modulates urine production and also territorial behavior, which often involves urine and scent marking (17,18).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [18]
Oxytocin is well known for its influence on social bonding and maternal behavior, and its role in parental behavior highlights the putative function of oxytocin as an attentional modulator.
“OXT is well known for its influence on social bonding and maternal behavior (9,18), and its role in parental behavior highlights the putative function of OXT as an attentional modulator (122).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [18]
Oxytocin may specifically facilitate the transition from avoidance of pups to caring for them.
“For instance, hypothalamic lesions block the initiation, but not the maintenance, of maternal behaviors in rats (18), suggesting that OXT may specifically facilitate the transition from avoidance of pups to caring for them (19,20).”
From Dissecting the Role of Oxytocin in the Formation and Loss of Social Relationships (2016) · cites this paper as [20]
Maternal care is critical for child survival and health.
“Maternal care is critical for child survival and health (Rilling and Young, 2014).”
From Neuromodulation of maternal circuits by oxytocin (2019) · cites this paper as Rilling and Young, 2014
OT is critical in the formation and maintenance of mother-infant bonds in mammals.
“OT has been shown to be critical in the formation and maintenance of mother-infant bonds in mammals (Rilling and Young, 2014)”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Rilling and Young, 2014
OT mediates mother-infant attachments via both physiological mechanisms (e.g., uterine contraction, milk-let down) and behavioral mechanisms (e.g., mother-infant bonding).
“OT mediates mother-infant attachments via both physiological mechanisms (e.g., uterine contraction, milk-let down) and also behavioral mechanisms (e.g., mother-infant bonding; (Rilling and Young, 2014).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Rilling and Young, 2014
Systemic loss of oxytocin or oxytocin receptors disrupts maternal nurturing behaviours in mice.
“Systemic loss of either oxytocin or oxytocin receptors (Oxt−/− and Oxtr−/−) disrupts maternal nurturing behaviours in mice7,8.”
From Vascular RAGE transports oxytocin into the brain to elicit its maternal bonding behaviour in mice (2019) · cites this paper as [8]
Clinical studies have linked autism and Asperger's disorders and attention-deficit/hyperactivity disorders to oxytocin deficiency.
“Clinical studies have linked autism and Asperger’s disorders and attention-deficit/hyperactivity disorders to oxytocin deficiency7,8,54, and the potential use of exogenous oxytocin to treat these conditions is being assessed in clinical trials10,11,54–57.”
From Vascular RAGE transports oxytocin into the brain to elicit its maternal bonding behaviour in mice (2019) · cites this paper as [8]
Intranasal oxytocin promotes affiliative behaviors.
“affiliative behaviors (Hurlemann and Scheele, 2015;Rilling and Young, 2014)”
From Oxytocin Facilitates Pavlovian Fear Learning in Males (2016) · cites this paper as Rilling and Young, 2014
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Cites
Feldman, R. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01701.x · Cited by 1,317 · see citing works
Early developmental emergence of human amygdala–prefrontal connectivity after maternal deprivation
Gee, D. G., Gabard-Durnam, L. J., Flannery, J., Goff, B., Humphreys, K. L., Telzer, E. H., Hare, T. A., Bookheimer, S. Y., & Tottenham, N. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1307893110 · Cited by 871 · see citing works
Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior
Ross, H. E., & Young, L. J. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.004 · Cited by 856 · see citing works
Self-citationAdult attachment predicts maternal brain and oxytocin response to infant cues.
Strathearn, L., Fonagy, P., Amico, J., & Montague, P. R. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.103 · Cited by 773 · see citing works
Oxytocin and social affiliation in humans
Feldman, R. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.01.008 · Cited by 767 · see citing works
Fries, A. B. W., Ziegler, T. E., Kurian, J. R., Jacoris, S., & Pollak, S. D. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504767102 · Cited by 570 · see citing works
Increased brain and plasma oxytocin after nasal and peripheral administration in rats and mice
Neumann, I. D., Maloumby, R., Beiderbeck, D. I., Lukas, M., & Landgraf, R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.03.003 · Cited by 511 · see citing works
Neural control of maternal and paternal behaviors
Dulac, C., O’Connell, L. A., & Wu, Z. (2014) · Science · doi:10.1126/science.1253291 · Cited by 457 · see citing works
Striepens, N., Kendrick, K. M., Hanking, V., Landgraf, R., Wüllner, U., Maier, W., & Hurlemann, R. (2013) · Scientific Reports · doi:10.1038/srep03440 · Cited by 452 · see citing works
Bosch, O. J., & Neumann, I. D. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.11.002 · Cited by 400 · see citing works
Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster).
Wang, Z., Ferris, C. F., & De Vries, G. J. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.1.400 · Cited by 381 · see citing works
Riem, M. M. E., Bakermans-Kranenburg, M. J., Pieper, S., Tops, M., Boksem, M. A. S., Vermeiren, R. R. J. M., van IJzendoorn, M. H., & Rombouts, S. A. R. B. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.02.006 · Cited by 366 · see citing works
Baby schema modulates the brain reward system in nulliparous women
Glocker, M. L., Langleben, D. D., Ruparel, K., Loughead, J. W., Valdez, J. N., Griffin, M. D., Sachser, N., & Gur, R. C. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811620106 · Cited by 365 · see citing works
Early neglect is associated with alterations in white matter integrity and cognitive functioning
Hanson, J. L., Adluru, N., Chung, M. K., Alexander, A. L., Davidson, R. J., & Pollak, S. D. (2013) · Child Development · doi:10.1111/cdev.12069 · Cited by 276 · see citing works
Apter-Levy, Y., Feldman, M., Vakart, A., Ebstein, R. P., & Feldman, R. (2013) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2013.12121597 · Cited by 260 · see citing works
Weisman, O., Zagoory-Sharon, O., & Feldman, R. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.06.011 · Cited by 240 · see citing works
The neural and hormonal bases of human parentalcare
Rilling, J. K. (2013) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2012.12.017 · Cited by 230 · see citing works
Self-citationA cry in the dark: depressed mothers show reduced neural activation to their own infant’s cry
Laurent, H. K., & Ablow, J. C. (2012) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsq091 · Cited by 224 · see citing works
Oxytocin administration, salivary testosterone, and father–infant social behavior
Weisman, O., Zagoory‐Sharon, O., & Feldman, R. (2013) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2013.11.006 · Cited by 160 · see citing works
McQuaid, R. J., McInnis, O. A., Stead, J. D. H., Matheson, K., & Anisman, H. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00128 · Cited by 158 · see citing works
Testicular volume is inversely correlated with nurturing-related brain activity in human fathers
Mascaro, J. S., Hackett, P. D., & Rilling, J. K. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305579110 · Cited by 153 · see citing works
Self-citationMaternal neural responses to infant cries and faces: relationships with substance use
Landi, N., Montoya, J., Kober, H., Rutherford, H. J. V., Mencl, W. E., Worhunsky, P. D., Potenza, M. N., & Mayes, L. C. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00032 · Cited by 146 · see citing works
Bradley, B., Davis, T. A., Wingo, A. P., Mercer, K. B., & Ressler, K. J. (2013) · European Journal of Psychotraumatology · doi:10.3402/ejpt.v4i0.21659 · Cited by 137 · see citing works
Stolzenberg, D. S., & Numan, M. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.10.003 · Cited by 137 · see citing works
Aerosolized oxytocin increases cerebrospinal fluid oxytocin in rhesus macaques
Modi, M. E., Connor-Stroud, F., Landgraf, R., Young, L. J., & Parr, L. A. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.02.011 · Cited by 129 · see citing works
Self-citationBarr, R. G. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1121267109 · Cited by 121 · see citing works
Peña, C. J., Neugut, Y. D., Calarco, C. A., & Champagne, F. A. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12479 · Cited by 120 · see citing works
Oxytocin and vasopressin support distinct configurations of social synchrony
Apter-Levi, Y., Zagoory-Sharon, O., & Feldman, R. (2014) · Brain Research · doi:10.1016/j.brainres.2013.10.052 · Cited by 116 · see citing works
Riem, M. M. E., Pieper, S., Out, D., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2011) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsq035 · Cited by 113 · see citing works
Ahern, T. H., Hammock, E. A. D., & Young, L. J. (2011) · Developmental Psychobiology · doi:10.1002/dev.20498 · Cited by 113 · see citing works
Self-citationMah, B. L., Bakermans‐Kranenburg, M. J., van IJzendoorn, M. H., & Smith, R. (2014) · Depression and Anxiety · doi:10.1002/da.22245 · Cited by 93 · see citing works
Tottenham, N., Shapiro, M., Telzer, E. H., & Humphreys, K. L. (2012) · Developmental Science · doi:10.1111/j.1467-7687.2011.01128.x · Cited by 91 · see citing works
Behavioral and genetic correlates of the neural response to infant crying among human fathers
Mascaro, J. S., Hackett, P. D., Gouzoules, H., Lori, A., & Rilling, J. K. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst166 · Cited by 89 · see citing works
Self-citationMascaro, J. S., Hackett, P. D., & Rilling, J. K. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.04.014 · Cited by 84 · see citing works
Self-citationThe missing link: Mothers’ neural response to infant cry related to infant attachment behaviors
Laurent, H. K., & Ablow, J. C. (2012) · Infant Behavior and Development · doi:10.1016/j.infbeh.2012.07.007 · Cited by 82 · see citing works
Michalska, K. J., Decety, J., Liu, C., Chen, Q., Martz, M. E., Jacob, S., Hipwell, A. E., Lee, S. S., Chronis-Tuscano, A., Waldman, I. D., et al. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00021 · Cited by 76 · see citing works
Maternal imprints and the origins of variation
Champagne, F. A. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.02.016 · Cited by 74 · see citing works
Ziegler, T. E., Prudom, S. L., Zahed, S. R., Parlow, A. F., & Wegner, F. H. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.07.012 · Cited by 73 · see citing works
Gettler, L. T., McDade, T. W., Agustin, S. S., Feranil, A. B., & Kuzawa, C. W. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.08.019 · Cited by 63 · see citing works
Oxytocin shapes parental motion during father-infant interaction
Weisman, O., Delaherche, E., Rondeau, M., Chetouani, M., Cohen, D., & Feldman, R. (2013) · Biology Letters · doi:10.1098/rsbl.2013.0828 · Cited by 63 · see citing works
Gleason, E. D., & Marler, C. A. (2013) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.0824 · Cited by 41 · see citing works
Barrett, C. E., Modi, M. E., Zhang, B. C., Walum, H., Inoue, K., & Young, L. J. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.05.041 · Cited by 34 · see citing works
Self-citationYu, P., An, S.-C., Tai, F., Wang, J., Wu, R., & Wang, B. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.09.012 · Cited by 32 · see citing works
Kryski, K. R., Smith, H. J., Sheikh, H. I., Singh, S. M., & Hayden, E. P. (2014) · Personality and Individual Differences · doi:10.1016/j.paid.2014.02.028 · Cited by 24 · see citing works
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The Neurobiology of Human Attachments
Feldman, R. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.11.007 · Cited by 839 · see citing works
Paradise lost: the neurobiological and clinical consequences of child abuse and neglect
Nemeroff, C. B. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.019 · Cited by 768 · see citing works
Oxytocin-gaze positive loop and the coevolution of human-dog bonds
Nagasawa, M., Mitsui, S., En, S., Ohtani, N., Ohta, M., Sakuma, Y., Onaka, T., Mogi, K., & Kikusui, T. (2015) · Science · doi:10.1126/science.1261022 · Cited by 753 · see citing works
Oxytocin enables maternal behaviour by balancing cortical inhibition
Marlin, B. J., Mitre, M., D’amour, J. A., Chao, M. V., & Froemke, R. C. (2015) · Nature · doi:10.1038/nature14402 · Cited by 744 · see citing works
Oxytocin, Neural Plasticity, and Social Behavior
Froemke, R. C., & Young, L. J. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-102320-102847 · Cited by 487 · see citing works
Self-citationNeural control of maternal and paternal behaviors
Dulac, C., O’Connell, L. A., & Wu, Z. (2014) · Science · doi:10.1126/science.1253291 · Cited by 457 · see citing works
The adaptive human parental brain: implications for children's social development
Feldman, R. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.04.004 · Cited by 419 · see citing works
Brain-to-Brain Synchrony during Naturalistic Social Interactions
Kinreich, S., Djalovski, A., Kraus, L., Louzoun, Y., & Feldman, R. (2017) · Scientific Reports · doi:10.1038/s41598-017-17339-5 · Cited by 402 · see citing works
The neural mechanisms and circuitry of the pair bond
Walum, H., & Young, L. J. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0072-6 · Cited by 353 · see citing works
Self-citationNuman, M., & Young, L. J. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.05.015 · Cited by 355 · see citing works
Self-citationNeuroendocrine regulation of maternal behavior
Bridges, R. S. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2014.11.007 · Cited by 346 · see citing works
A distributed network for social cognition enriched for oxytocin receptors
Mitre, M., Marlin, B. J., Schiavo, J. K., Morina, E., Norden, S. E., Hackett, T. A., Aoki, C. J., Chao, M. V., & Froemke, R. C. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.2409-15.2016 · Cited by 305 · see citing works
Hormonal gain control of a medial preoptic area social reward circuit
McHenry, J. A., Otis, J. M., Rossi, M. A., Robinson, J. E., Kosyk, O., Miller, N. W., McElligott, Z. A., Budygin, E. A., Rubinow, D. R., & Stuber, G. D. (2017) · Nature Neuroscience · doi:10.1038/nn.4487 · Cited by 304 · see citing works
De Dreu, C. K. W., & Kret, M. E. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.03.020 · Cited by 297 · see citing works
van IJzendoorn, M. H., Bakermans‐Kranenburg, M. J., Coughlan, B., & Reijman, S. (2020) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.13147 · Cited by 262 · see citing works
A sexually dimorphic hypothalamic circuit controls maternal care and oxytocin secretion
Scott, N., Prigge, M., Yizhar, O., & Kimchi, T. (2015) · Nature · doi:10.1038/nature15378 · Cited by 261 · see citing works
Guastella, A. J., & Hickie, I. B. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.06.028 · Cited by 223 · see citing works
A Cortical Circuit for Sexually Dimorphic Oxytocin-Dependent Anxiety Behaviors
Li, K., Nakajima, M., Ibañez-Tallon, I., & Heintz, N. (2016) · Cell · doi:10.1016/j.cell.2016.08.067 · Cited by 234 · see citing works
Fragmentation and high entropy of neonatal experience predict adolescent emotional outcome
Molet, J., Heins, K., Zhuo, X., Mei, Y., Regev, L., Baram, T. Z., & Stern, H. S. (2016) · Translational Psychiatry · doi:10.1038/tp.2015.200 · Cited by 230 · see citing works
Pace-Schott, E. F., Amole, M. C., Aue, T., Balconi, M., Bylsma, L. M., Critchley, H., Demaree, H. A., Friedman, B. H., Gooding, A. E. K., Gosseries, O., et al. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.05.002 · Cited by 221 · see citing works
“Oxytocin is thought to promote attachment and is critical for early survival of neonates (Rilling and Young, 2014).”
Ko, J. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00041 · Cited by 212 · see citing works
Freeman, S. M., & Young, L. J. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12382 · Cited by 196 · see citing works
“Work in rats has demonstrated that central OT signalling is crucial for the onset of maternal nurturing behaviour (1,2).”
BackgroundSelf-citationKing, L. B., Walum, H., Inoue, K., Eyrich, N. W., & Young, L. J. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.12.008 · Cited by 191 · see citing works
“The OXTR affects a range of social behaviors in animals, including maternal nurturing and bonding (1,2), social reward and gregariousness (3,4), social recognition (5), and pair bonding in monogamous species (6–8).”
InfluentialSelf-citationOxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities
Rigney, N., de Vries, G. J., Petrulis, A., & Young, L. J. (2022) · Endocrinology · doi:10.1210/endocr/bqac111 · Cited by 191 · see citing works
Self-citationJohnson, Z. V., Walum, H., Jamal, Y. A., Xiao, Y., Keebaugh, A. C., Inoue, K., & Young, L. J. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.11.011 · Cited by 190 · see citing works
Self-citationBrown, S. L., & Brown, R. M. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.04.004 · Cited by 190 · see citing works
Vascular RAGE transports oxytocin into the brain to elicit its maternal bonding behaviour in mice
Yamamoto, Y., Liang, M., Munesue, S., Deguchi, K., Harashima, A., Furuhara, K., Yuhi, T., Zhong, J., Akther, S., Goto, H., et al. (2019) · Communications Biology · doi:10.1038/s42003-019-0325-6 · Cited by 171 · see citing works
Neurobiological mechanisms of social attachment and pair bonding
Johnson, Z. V., & Young, L. J. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.01.009 · Cited by 169 · see citing works
Self-citationThe neural mechanisms and consequences of paternal caregiving
Feldman, R., Braun, K., & Champagne, F. A. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-019-0124-6 · Cited by 168 · see citing works
Oxytocin and Social Relationships: From Attachment to Bond Disruption
Bosch, O. J., & Young, L. J. (2017) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2017_10 · Cited by 162 · see citing works
Self-citationMolecular Basis of Oxytocin Receptor Signalling in the Brain: What We Know and What We Need to Know
Busnelli, M., & Chini, B. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_6 · Cited by 161 · see citing works
Pet Face: Mechanisms Underlying Human-Animal Relationships
Borgi, M., & Cirulli, F. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.00298 · Cited by 161 · see citing works
Keebaugh, A. C., Barrett, C. E., Laprairie, J. L., Jenkins, J. J., & Young, L. J. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1040893 · Cited by 150 · see citing works
Self-citationMüller, L. E., Schulz, A., Andermann, M., Gäbel, A., Gescher, D. M., Spohn, A., Herpertz, S. C., & Bertsch, K. (2015) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2015.1252 · Cited by 141 · see citing works
Early Life Experiences and Exercise Associate with Canine Anxieties
Tiira, K., & Lohi, H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0141907 · Cited by 147 · see citing works
Child gender influences paternal behavior, language, and brain function.
Mascaro, J. S., Rentscher, K. E., Hackett, P. D., Mehl, M. R., & Rilling, J. K. (2017) · Behavioral Neuroscience · doi:10.1037/bne0000199 · Cited by 149 · see citing works
Self-citationSocial bonds facilitate cooperative resource sharing in wild chimpanzees
Samuni, L., Preis, A., Mielke, A., Deschner, T., Wittig, R. M., & Crockford, C. (2018) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2018.1643 · Cited by 143 · see citing works
The influence of unpredictable, fragmented parental signals on the developing brain
Glynn, L. M., & Baram, T. Z. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.01.002 · Cited by 146 · see citing works
Oxytocin and postpartum depression: A systematic review
Thul, T. A., Corwin, E. J., Carlson, N. S., Brennan, P. A., & Young, L. J. (2020) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2020.104793 · Cited by 142 · see citing works
Self-citationOxytocin and the Neurobiology of Prosocial Behavior
Marsh, N., Marsh, A. A., Lee, M. R., & Hurlemann, R. (2020) · The Neuroscientist · doi:10.1177/1073858420960111 · Cited by 149 · see citing works
Yu, H., Miao, W., Ji, E., Huang, S., Jin, S., Zhu, X., Liu, M.-Z., Sun, Y.-G., Xu, F., & Yu, X. (2022) · Neuron · doi:10.1016/j.neuron.2021.12.022 · Cited by 144 · see citing works
Herpertz, S. C., & Bertsch, K. (2015) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2015.15020216 · Cited by 139 · see citing works
Dissecting the Role of Oxytocin in the Formation and Loss of Social Relationships
Hurlemann, R., & Scheele, D. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.05.013 · Cited by 136 · see citing works
Reward of labor coordination and hunting success in wild chimpanzees
Samuni, L., Preis, A., Deschner, T., Crockford, C., & Wittig, R. M. (2018) · Communications Biology · doi:10.1038/s42003-018-0142-3 · Cited by 135 · see citing works
<scp>O</scp>xytocin modulation of neural circuits for social behavior
Marlin, B. J., & Froemke, R. C. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22452 · Cited by 130 · see citing works
Ontogenesis of oxytocin pathways in the mammalian brain: late maturation and psychosocial disorders
Grinevich, V., Desarménien, M. G., Chini, B., Tauber, M., & Muscatelli, F. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00164 · Cited by 121 · see citing works
Bisphenol A and phthalate endocrine disruption of parental and social behaviors
Rosenfeld, C. S. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00057 · Cited by 119 · see citing works
Barrett, C. E., Arambula, S. E., & Young, L. J. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.73 · Cited by 115 · see citing works
Self-citationHormonal contraceptives suppress oxytocin-induced brain reward responses to the partner’s face
Scheele, D., Plota, J., Stoffel-Wagner, B., Maier, W., & Hurlemann, R. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsv157 · Cited by 116 · see citing works
“Consistent with OXT’s well-established reproductive functions, including the induction of uterine contraction during labor and milk ejection during lactation (Gimpl and Fahrenholz, 2001), its role as a key underlying factor of the mother–infant attachment system has often been documented (Rilling and Young, 2014; Feld…”
BackgroundOxytocin pathways in the intergenerational transmission of maternal early life stress
Töpfer, P., Heim, C. C., Entringer, S., Binder, E. B., Wadhwa, P. D., & Buß, C. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.12.026 · Cited by 114 · see citing works
Hormonal Physiology of Childbearing: Evidence and Implications for Women, Babies, and Maternity Care
Buckley, S. J. (2015) · Issue Lab (Candid) · Cited by 113 · see citing works
Neural circuitry for maternal oxytocin release induced by infant cries
Valtcheva, S., Issa, H. A., Bair-Marshall, C. J., Martin, K. A., Jung, K., Zhang, Y., Kwon, H.-B., & Froemke, R. C. (2023) · Nature · doi:10.1038/s41586-023-06540-4 · Cited by 115 · see citing works
The birth of new neurons in the maternal brain: Hormonal regulation and functional implications
Leuner, B., & Sabihi, S. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.02.004 · Cited by 110 · see citing works
RDoC-based categorization of amygdala functions and its implications in autism
Hennessey, T., Andari, E., & Rainnie, D. G. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2018.04.007 · Cited by 105 · see citing works
Intranasal oxytocin, but not vasopressin, augments neural responses to toddlers in human fathers
Li, T., Chen, X., Mascaro, J., Haroon, E., & Rilling, J. K. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.01.006 · Cited by 105 · see citing works
Self-citationRAGE regulates oxytocin transport into the brain
Yamamoto, Y., & Higashida, H. (2020) · Communications Biology · doi:10.1038/s42003-020-0799-2 · Cited by 102 · see citing works
Andari, E., Nishitani, S., Gopinath, K., Caceres, G. A., Morrier, M. J., Ousley, O., Smith, A. K., Cubells, J. F., & Young, L. J. (2020) · Neuropsychopharmacology · doi:10.1038/s41386-020-0610-6 · Cited by 97 · see citing works
Self-citationBiological Functions of Rat Ultrasonic Vocalizations, Arousal Mechanisms, and Call Initiation
Brudzyński, S. M. (2021) · Brain Sciences · doi:10.3390/brainsci11050605 · Cited by 103 · see citing works
Kroll‐Desrosiers, A., Nephew, B. C., Babb, J. A., Guilarte-Walker, Y., Simas, T. A. M., & Deligiannidis, K. M. (2017) · Depression and Anxiety · doi:10.1002/da.22599 · Cited by 99 · see citing works
Oxytocin and Parental Behaviors
Yoshihara, C., Numan, M., & Kuroda, K. O. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_11 · Cited by 102 · see citing works
Towards a neural model of infant cry perception
Witteman, J., Van IJzendoorn, M. H., Rilling, J. K., Bos, P. A., Schiller, N. O., & Bakermans-Kranenburg, M. J. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.01.026 · Cited by 94 · see citing works
Self-citationDevelopments in Amphibian Parental Care Research: History, Present Advances, and Future Perspectives
Schulte, L. M., Ringler, E., Rojas, B., & Stynoski, J. L. (2020) · Herpetological Monographs · doi:10.1655/herpmonographs-d-19-00002.1 · Cited by 94 · see citing works
Abraham, E., Hendler, T., Zagoory‐Sharon, O., & Feldman, R. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw090 · Cited by 90 · see citing works
Oxytocin Facilitates Pavlovian Fear Learning in Males
Eckstein, M., Scheele, D., Patin, A., Preckel, K., Becker, B., Walter, A., Domschke, K., Grinevich, V., Maier, W., & Hurlemann, R. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2015.245 · Cited by 87 · see citing works
Dietz, L., Arnold, A. K., Goerlich, V. C., & Vinke, C. M. (2018) · Behaviour · doi:10.1163/1568539x-00003486 · Cited by 88 · see citing works
Oxytocin receptor DNA methylation and alterations of brain volumes in maltreated children
Fujisawa, T. X., Nishitani, S., Takiguchi, S., Shimada, K., Smith, A. K., & Tomoda, A. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0414-8 · Cited by 85 · see citing works
Group Cooperation, Carrying-Capacity Stress, and Intergroup Conflict
Dreu, C. K. W. D., Gross, J., Fariña, A., & Ma, Y. (2020) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2020.06.005 · Cited by 85 · see citing works
Pohl, T. T., Young, L. J., & Bosch, O. J. (2019) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2017.12.011 · Cited by 83 · see citing works
Self-citationHe, Z., Young, L., Ma, X.-M., Guo, Q., Wang, L., Yang, Y., Luo, L., Yuan, W., Li, L., Zhang, J., et al. (2019) · eLife · doi:10.7554/elife.44026 · Cited by 81 · see citing works
Lebowitz, E. R., Leckman, J. F., Feldman, R., Zagoory‐Sharon, O., McDonald, N. M., & Silverman, W. K. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.12.007 · Cited by 79 · see citing works
Abraham, E., & Feldman, R. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2017.12.034 · Cited by 90 · see citing works
Cohen, L., & Mizrahi, A. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.1786-14.2015 · Cited by 82 · see citing works
Raison, C. L., Hale, M. W., Williams, L. E., Wager, T. D., & Lowry, C. A. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.01580 · Cited by 76 · see citing works
Abraham, E., Raz, G., Zagoory‐Sharon, O., & Feldman, R. (2017) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2017.04.015 · Cited by 78 · see citing works
Oxytocin Modulation of Neural Circuits
Mitre, M., Minder, J. L., Morina, E., Chao, M. V., & Froemke, R. C. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_7 · Cited by 76 · see citing works
Psychobiology of Attachment and Trauma—Some General Remarks From a Clinical Perspective
Lahousen, T., Unterrainer, ., & Kapfhammer, H. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00914 · Cited by 83 · see citing works
Plasticity of neural connections underlying oxytocin-mediated parental behaviors of male mice
Inada, K., Hagihara, M., Tsujimoto, K., Abe, T., Konno, A., Hirai, H., Kiyonari, H., & Miyamichi, K. (2022) · Neuron · doi:10.1016/j.neuron.2022.03.033 · Cited by 79 · see citing works
Zhang, R., Zhang, H.-F., Han, J., & Han, S. (2017) · Neuroscience Bulletin · doi:10.1007/s12264-017-0120-7 · Cited by 76 · see citing works
Social Monogamy in Nonhuman Primates: Phylogeny, Phenotype, and Physiology
French, J. A., Cavanaugh, J., Mustoe, A. C., Carp, S. B., & Womack, S. L. (2017) · The Journal of Sex Research · doi:10.1080/00224499.2017.1339774 · Cited by 72 · see citing works
Specific maternal brain responses to their own child’s face: An fMRI meta-analysis
Rigo, P., Kim, P., Esposito, G., Putnick, D. L., Venuti, P., & Bornstein, M. H. (2018) · Developmental Review · doi:10.1016/j.dr.2018.12.001 · Cited by 76 · see citing works
Modification of feeding circuits in the evolution of social behavior
Fischer, E. K., & O’Connell, L. A. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.143859 · Cited by 70 · see citing works
Perry, R. E., Finegood, E. D., Braren, S. H., DeJoseph, M. L., Putrino, D. F., Wilson, D. A., Sullivan, R. M., Raver, C. C., Blair, C., & Family Life Project Key Investigators (2018) · Development and Psychopathology · doi:10.1017/s095457941800007x · Cited by 74 · see citing works
The maternal reward system in postpartum depression
Goodpaster, C. M., & Leuner, B. (2018) · Archives of Women s Mental Health · doi:10.1007/s00737-018-0926-y · Cited by 73 · see citing works
Mothers with substance addictions show reduced reward responses when viewing their own infant's face
Kim, S., Iyengar, U., Mayes, L. C., Potenza, M. N., Rutherford, H. J. V., & Strathearn, L. (2017) · Human Brain Mapping · doi:10.1002/hbm.23731 · Cited by 71 · see citing works
Oxytocin promotes intuitive rather than deliberated cooperation with the in-group
Ten Velden, F. S., Daughters, K., & De Dreu, C. K. W. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.06.005 · Cited by 66 · see citing works
The endocrinology of human caregiving and its intergenerational transmission
Bos, P. A. (2016) · Development and Psychopathology · doi:10.1017/s0954579416000973 · Cited by 70 · see citing works
Neuropeptide diversity and the regulation of social behavior in New World primates
French, J. A., Taylor, J. H., Mustoe, A. C., & Cavanaugh, J. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.03.004 · Cited by 66 · see citing works
Young, K. S., Parsons, C. E., Stein, A. L., Vuust, P., Craske, M. G., & Kringelbach, M. L. (2016) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.09.012 · Cited by 65 · see citing works
Oxytocin: Parallel Processing in the Social Brain?
Dölen, G. (2015) · Journal of Neuroendocrinology · doi:10.1111/jne.12284 · Cited by 65 · see citing works
Oxytocin, social cognition and psychiatry
Young, L. J. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.186 · Cited by 64 · see citing works
Self-citationThalamic integration of social stimuli regulating parental behavior and the oxytocin system
Dobolyi, A., Cservenák, M., & Young, L. J. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2018.05.002 · Cited by 64 · see citing works
Self-citationThe Anorexigenic Neural Pathways of Oxytocin and Their Clinical Implication
Maejima, Y., Yokota, S., Nishimori, K., & Shimomura, K. (2018) · Neuroendocrinology · doi:10.1159/000489263 · Cited by 65 · see citing works
Cross-fostering: Elucidating the effects of gene×environment interactions on phenotypic development
McCarty, R. C. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.12.025 · Cited by 61 · see citing works
Sexually dimorphic role of oxytocin in medaka mate choice
Yokoi, S., Naruse, K., Kamei, Y., Ansai, S., Kinoshita, M., Mito, M., Iwasaki, S., Inoue, S., Okuyama, T., Nakagawa, S., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1921446117 · Cited by 62 · see citing works
Self-citationGestational hormone profiles predict human maternal behavior at 1-year postpartum
Glynn, L. M., Davis, E. P., Sandman, C. A., & Goldberg, W. A. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.07.002 · Cited by 62 · see citing works
Krol, K. M., Monakhov, M. V., Lai, P. S., Ebstein, R. P., & Großmann, T. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1506352112 · Cited by 62 · see citing works
Oxytocin selectively modulates brain response to stimuli probing social synchrony
Lévy, J., Goldstein, A., Zagoory‐Sharon, O., Weisman, O., Schneiderman, I., Eidelman-Rothman, M., & Feldman, R. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.09.066 · Cited by 61 · see citing works
Murgatroyd, C., Peña, C. J., Podda, G., Nestler, E. J., & Nephew, B. C. (2015) · Neuropeptides · doi:10.1016/j.npep.2015.05.002 · Cited by 61 · see citing works
Leblanc, É., Dégeilh, F., Daneault, V., Beauchamp, M. H., & Bernier, A. (2017) · Frontiers in Psychology · doi:10.3389/fpsyg.2017.02141 · Cited by 61 · see citing works
The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives
Blumenthal, S. A., & Young, L. J. (2023) · Biology · doi:10.3390/biology12060844 · Cited by 59 · see citing works
“neural mechanisms driving evolutionary antecedents of love [4,5].”
BackgroundInfluentialSelf-citation
- Authors
- Rilling, J. K., & Young, L. J.
- Affiliations
- Emory University (US)
- Corresponding author
- Young, Larry J.
- Venue
- Science
- Published
- 2014-08-15
- Volume
- 345
- Issue
- 6198
- Pages
- 771-776
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC4306567
- OpenAlex
- W2119333871
- Cited by
- 452
- References
- 44
- Citations by year
- 2026: 22 · 2025: 26 · 2024: 19 · 2023: 25 · 2022: 45 · 2021: 43 · 2020: 31 · 2019: 38 · 2018: 50 · 2017: 50 · 2016: 45 · 2015: 53 · 2014: 4
- FWCI
- 7.20
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- John Templeton Foundation
- National Institutes of Health (UL1TR000454, P51OD011132)
- National Institute of Mental Health (R01MH096983, P50MH100023)
- National Center for Advancing Translational Sciences
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Health Sciences › Health Professions › Pharmacy › Infant Health and Development
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Keywords
- parental motivation, maternal behavior, estrogen, progesterone, prolactin, oxytocin, dopamine, maternal-infant bonding, social brain development, lactation, placental development
- MeSH terms
- Animals, Brain, Child Development, Dopamine, Female, Hormones, Humans, Infant, Male, Mammals, Maternal Behavior, Oxytocin, Paternal Behavior, Social Change, Parenting
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