Synchrony and specificity in the maternal and the paternal brain: relations to oxytocin and vasopressin
Abstract
Objective Research on the neurobiology of parenting has defined biobehavioral synchrony, the coordination of biological and behavioral responses between parent and child, as a central process underpinning mammalian bond formation. Bi-parental rearing, typically observed in monogamous species, is similarly thought to draw on mechanisms of mother-father synchrony.Method We examined synchrony in mothers' and fathers' brain response to ecologically valid infant cues. Thirty mothers and fathers, comprising 15 couples parenting 4- to 6-month-old infants, were visited at home, and infant play was videotaped. Parents then underwent functional magnetic resonance imaging scanning while observing own-infant compared with standard-infant videos. Coordination in brain response between mothers and fathers was assessed using a voxel-by-voxel algorithm, and gender-specific activations were also tested. Plasma oxytocin and arginine vasopressin, neuropeptides implicated in female and male bonding, were examined as correlates.Results Online coordination in maternal and paternal brain activations emerged in social-cognitive networks implicated in empathy and social cognition. Mothers showed higher amygdala activations and correlations between amygdala response and oxytocin. Fathers showed greater activations in social-cognitive circuits, which correlated with vasopressin.Conclusions Parents coordinate online activity in social-cognitive networks that support intuitive understanding of infant signals and planning of adequate caregiving, whereas motivational-limbic activations may be gender specific. Although preliminary, these findings demonstrate synchrony in the brain response of two individuals within an attachment relationship, and may suggest that human attachment develops within the matrix of biological attunement and brain-to-brain synchrony between attachment partners.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Plasma oxytocin is correlated with the activation of the amygdala and nucleus accumbens in mothers viewing their own infant.
“Additionally, plasma OT is correlated with the activation of the amygdala and NAc in mothers viewing their own infant [45].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [45]
Plasma levels of vasopressin in human fathers, but not mothers, are related to activation of the inferior frontal gyrus and insular cortex.
“Furthermore, plasma levels of AVP in human fathers, but not mothers, are related to activation of the inferior frontal gyrus and in the insular cortex (IC), both regions implicated in socio-cognitive function, suggesting a distinct role for AVP in promoting paternal behavior [45].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [45]
Among mothers, plasma OT levels correlated positively with activations in the ventral ACC, the left NAcc, the inferior parietal lobule, and the temporal and frontal gyri in response to videos of their own infants.
“In another study, the same group of researchers demonstrated that among mothers, plasma OT levels correlated positively with activations in the ventral ACC, the left NAcc, the inferior parietal lobule, and the temporal and frontal gyri in response to videos of their own infants (Atzil et al., 2012).”
From The maternal brain and its plasticity in humans (2016) · cites this paper as Atzil et al., 2012
When own vs other infant vignettes were compared, maternal synchrony was associated with significantly increased activity of left NAcc, while maternal intrusiveness was linked to activity of right amygdala (Atzil et al., 2012).
“In another study, when own vs. other infant vignettes were compared, maternal synchrony was associated with significantly increased activity of left NAcc, while maternal intrusiveness was linked to activity of right amygdala (Atzil et al., 2012).”
From Approaching the biology of human parental attachment: Brain imaging, oxytocin and coordinated assessments of mothers and fathers (2014) · cites this paper as Atzil et al., 2012
Cites
The Role of the Father in Child Development
Lamb, M. E., Pleck, J. H., & Levine, J. A. (1985) · Springer eBooks · doi:10.1007/978-1-4613-9820-2_7 · Cited by 2,488 · see citing works
Intersubject synchronization of cortical activity during natural vision
Hasson, U., Nir, Y., Levy, I., Fuhrmann, G., & Malach, R. (2004) · Science · doi:10.1126/science.1089506 · Cited by 1,839 · see citing works
Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine
Meyer-Lindenberg, A., Domes, G., Kirsch, P., & Heinrichs, M. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3044 · Cited by 1,688 · see citing works
Social effects of oxytocin in humans: context and person matter
Bartz, J. A., Zaki, J., Bolger, N., & Ochsner, K. N. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.05.002 · Cited by 1,572 · see citing works
Neuroendocrine perspectives on social attachment and love
Sue Carter, C. (1998) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00055-9 · Cited by 1,425 · see citing works
The role of the father in child development
Lewis, C. E. (2009) · Cited by 1,423 · see citing works
The mirror neuron system and the consequences of its dysfunction
Iacoboni, M., & Dapretto, M. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn2024 · Cited by 1,401 · see citing works
Type I and Type II error concerns in fMRI research: re-balancing the scale
Lieberman, M. D., & Cunningham, W. A. (2009) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsp052 · Cited by 1,342 · see citing works
The neurobiology of attachment
Insel, T. R., & Young, L. J. (2001) · Nature Reviews Neuroscience · doi:10.1038/35053579 · Cited by 1,173 · see citing works
The neural basis of romantic love
Bartels, A., & Zeki, S. (2000) · NeuroReport · doi:10.1097/00001756-200011270-00046 · Cited by 1,020 · see citing works
Evolution and proximate expression of human paternal investment.
Geary, D. C. (2000) · Psychological Bulletin · doi:10.1037/0033-2909.126.1.55 · Cited by 812 · 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
Self-citationThe Simulation of Smiles (SIMS) model: Embodied simulation and the meaning of facial expression
Niedenthal, P. M., Mermillod, M., Maringer, M., & Hess, U. (2010) · Behavioral and Brain Sciences · doi:10.1017/s0140525x10000865 · Cited by 618 · see citing works
Cho, M. M., DeVries, A. C., Williams, J. R., & Carter, C. S. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.5.1071 · Cited by 529 · see citing works
Mother and infant coordinate heart rhythms through episodes of interaction synchrony
Feldman, R., Magori-Cohen, R., Galili, G., Singer, M., & Louzoun, Y. (2011) · Infant Behavior and Development · doi:10.1016/j.infbeh.2011.06.008 · Cited by 505 · see citing works
Self-citationSwain, J. E., Lorberbaum, J. P., Kose, S., & Strathearn, L. (2007) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2007.01731.x · Cited by 499 · 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
Self-citationKim, P., Leckman, J. F., Mayes, L. C., Feldman, R., Wang, X., & Swain, J. E. (2010) · Behavioral Neuroscience · doi:10.1037/a0020884 · Cited by 440 · see citing works
Self-citationAtzil, S., Hendler, T., & Feldman, R. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.172 · Cited by 399 · see citing works
Self-citationJean Decety, A. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06027.x · Cited by 389 · see citing works
Oxytocin–dopamine interactions mediate variations in maternal behavior in the rat
Shahrokh, D. K., Zhang, T.-Y., Diorio, J., Gratton, A., & Meaney, M. J. (2010) · Endocrinology · doi:10.1210/en.2009-1271 · Cited by 366 · see citing works
fMRI item analysis in a theory of mind task
Dodell‐Feder, D., Koster-Hale, J., Bedny, M., & Saxe, R. R. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.12.040 · Cited by 322 · see citing works
Sex-specific influences of vasopressin on human social communication
Thompson, R. R., George, K., Walton, J. C., Orr, S. P., & Benson, J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600406103 · Cited by 312 · see citing works
Maternal neglect: oxytocin, dopamine and the neurobiology of attachment
Strathearn, L. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02228.x · Cited by 268 · see citing works
Pereira, M., & Morrell, J. I. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02200.x · Cited by 146 · see citing works
Maternal 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
Zink, C. F., Stein, J. L., Kempf, L., Hakimi, S., & Meyer‐Lindenberg, A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4899-09.2010 · Cited by 131 · see citing works
Fathers and the Well-Child Visit
Garfield, C. F., & Isacco, A. J. (2006) · PEDIATRICS · doi:10.1542/peds.2005-1612 · Cited by 130 · see citing works
Intranasal Arginine Vasopressin Enhances the Encoding of Happy and Angry Faces in Humans
Guastella, A. J., Kenyon, A. R., Alvares, G. A., Carson, D. S., & Hickie, I. B. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.03.014 · Cited by 130 · see citing works
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
Bielsky, I. F., Hu, S.-B., & Young, L. J. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.06.005 · Cited by 91 · see citing works
Cocaine addiction in mothers: Potential effects on maternal care and infant development
Strathearn, L., & Mayes, L. C. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.05142.x · Cited by 80 · see citing works
Kinsley, C. H., & Amory, E. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02194.x · Cited by 71 · see citing works
Luo, J., Wang, L., & Gao, W. (2011) · Child Care Health and Development · doi:10.1111/j.1365-2214.2011.01304.x · Cited by 53 · see citing works
Effects of father participation in child rearing: Twenty-year follow-up.
Williams, E. M., & Radin, N. (1999) · American Journal of Orthopsychiatry · doi:10.1037/h0080407 · Cited by 45 · see citing works
Biosocial Foundations of Family Processes
Booth, A. D., Landale, N. S., & McHale, S. M. (2010) · National symposium on family issues · doi:10.1007/978-1-4419-7361-0 · Cited by 37 · see citing works
Fatherhood Alters Behavioural and Neural Responsiveness in a Spatial Task
Franssen, C. L., Bardi, M., Shea, E. A., Hampton, J. E., Franssen, R. A., Kinsley, C. H., & Lambert, K. G. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02225.x · Cited by 36 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Toward a second-person neuroscience
Schilbach, L., Timmermans, B., Reddy, V., Costall, A., Bente, G., Schlicht, T., & Vogeley, K. (2013) · Behavioral and Brain Sciences · doi:10.1017/s0140525x12000660 · Cited by 1,510 · see citing works
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
Self-citationOxytocin 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
Self-citationPanter‐Brick, C., Burgess, A., Eggerman, M., McAllister, F., Pruett, K., & Leckman, J. F. (2014) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12280 · Cited by 737 · see citing works
Mirror neurons: from origin to function
Cook, R., Bird, G., Catmur, C., Press, C., & Heyes, C. (2014) · Behavioral and Brain Sciences · doi:10.1017/s0140525x13000903 · Cited by 632 · see citing works
Emotion regulation in parenthood
Rutherford, H. J. V., Wallace, N. S., Laurent, H. K., & Mayes, L. C. (2015) · Developmental Review · doi:10.1016/j.dr.2014.12.008 · Cited by 485 · see citing works
“…is suggested by studies relating maternal and paternal observed sensitivity during parent–infant interaction to differential prefrontal and subcortical (nucleus accumbens, amygdala, hippocampus) activation to infant cues (Atzil et al., 2012; Kuo et al., 2012; Musser, Kaiser-Laurent, & Ablow, 2012).”
BackgroundThe 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
Self-citationReindl, V., Gerloff, C., Scharke, W., & Konrad, K. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.05.060 · Cited by 411 · see citing works
Father’s brain is sensitive to childcare experiences
Abraham, E., Hendler, T., Shapira-Lichter, I., Kanat-Maymon, Y., Zagoory-Sharon, O., & Feldman, R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1402569111 · Cited by 343 · see citing works
Self-citationOxytocin 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
Self-citationSwain, J. E., Kim, P., Spicer, J., Ho, S. S., Dayton, C. J., Elmadih, A., & Abel, K. M. (2014) · Brain Research · doi:10.1016/j.brainres.2014.03.007 · Cited by 290 · see citing works
The maternal brain and its plasticity in humans
Kim, P., Strathearn, L., & Swain, J. E. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.08.001 · Cited by 278 · see citing works
Feldman, R. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000048 · Cited by 271 · see citing works
Self-citationTimmons, A. C., Margolin, G., & Saxbe, D. E. (2015) · Journal of Family Psychology · doi:10.1037/fam0000115 · Cited by 255 · see citing works
Kagerbauer, S. M., Martin, J., Schuster, T., Blobner, M., Kochs, E. F., & Landgraf, R. (2013) · Journal of Neuroendocrinology · doi:10.1111/jne.12038 · Cited by 212 · see citing works
Paloyelis, Y., Doyle, O. M., Zelaya, F. O., Maltezos, S., Williams, S. C., Fotopoulou, A., & Howard, M. A. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.10.005 · Cited by 187 · see citing works
Neural plasticity in fathers of human infants
Kim, P., Rigo, P., Mayes, L. C., Feldman, R., Leckman, J. F., & Swain, J. E. (2014) · Social Neuroscience · doi:10.1080/17470919.2014.933713 · Cited by 164 · see citing works
Self-citationPhysiological and Behavioral Synchrony Predict Group Cohesion and Performance
Gordon, I., Gilboa, A., Cohen, S., Milstein, N., Haimovich, N., Pinhasi, S., & Siegman, S. (2020) · Scientific Reports · doi:10.1038/s41598-020-65670-1 · Cited by 146 · see citing works
Positive maternal mental health, parenting, and child development
Phua, D. Y., Kee, M. Z. L., & Meaney, M. J. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.09.028 · Cited by 124 · 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
Self-citationSex differences in depression during pregnancy and the postpartum period
Sundström Poromaa, I., Comasco, E., Georgakis, M. K., & Skalkidou, A. (2017) · Journal of Neuroscience Research · doi:10.1002/jnr.23859 · Cited by 96 · see citing works
Rocchetti, M., Radua, J., Paloyelis, Y., Xenaki, L., Frascarelli, M., Caverzasi, E., Politi, P., & Fusar‐Poli, P. (2014) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12185 · Cited by 83 · see citing works
Early adverse experience and substance addiction: Dopamine, oxytocin, and glucocorticoid pathways
Kim, S., Kwok, S., Mayes, L. C., Potenza, M. N., Rutherford, H. J. V., & Strathearn, L. (2017) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13140 · Cited by 85 · see citing works
A review of infants’ and children’s facial cues’ influence on adults’ perceptions and behaviors.
Franklin, P., & Volk, A. A. (2018) · Evolutionary Behavioral Sciences · doi:10.1037/ebs0000108 · Cited by 66 · 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
“Furthermore, plasma levels of AVP in human fathers, but not mothers, are related to activation of the inferior frontal gyrus and in the insular cortex (IC), both regions implicated in socio-cognitive function, suggesting a distinct role for AVP in promoting paternal behavior [45].”
BackgroundChallenging the challenge hypothesis on testosterone in fathers: Limited meta-analytic support
Meijer, W. M., van IJzendoorn, M. H., & Bakermans - Kranenburg, M. J. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.104435 · Cited by 49 · see citing works
Cohen-Bendahan, C. C. C., Beijers, R., van Doornen, L. J. P., & de Weerth, C. (2015) · Infant Behavior and Development · doi:10.1016/j.infbeh.2015.06.007 · Cited by 50 · see citing works
Abraham, E., Hendler, T., Zagoory-Sharon, O., & Feldman, R. (2019) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2018.02.001 · Cited by 38 · see citing works
Self-citationPaternina-Die, M., Martínez-García, M., Pretus, C., Hoekzema, E., Barba-Müller, E., Martín de Blas, D., Pozzobon, C., Ballesteros, A., Vilarroya, Ó., Desco, M., et al. (2020) · Cerebral Cortex Communications · doi:10.1093/texcom/tgaa082 · Cited by 29 · see citing works
van ‘t Veer, A. E., Thijssen, S., Witteman, J., van IJzendoorn, M. H., & Bakermans-Kranenburg, M. J. (2019) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsz018 · Cited by 25 · see citing works
Alyousefi-van Dijk, K., van ‘t Veer, A. E., Meijer, W. M., Lotz, A. M., Rijlaarsdam, J., Witteman, J., & Bakermans-Kranenburg, M. J. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00105 · Cited by 22 · see citing works
- Authors
- Atzil, S., Hendler, T., Zagoory-Sharon, O., Winetraub, Y., & Feldman, R.
- Affiliations
- Bar-Ilan University (IL)
- Tel Aviv Sourasky Medical Center (IL)
- Corresponding author
- Feldman, Ruth
- Venue
- Journal of the American Academy of Child & Adolescent Psychiatry
- Publisher
- Elsevier BV
- Published
- 2012-08
- Volume
- 51
- Issue
- 8
- Pages
- 798-811
- ISSN
- 0890-8567 (ISSN-L)
- OpenAlex
- W2028971980
- Semantic Scholar
- 9ac1ffed9715db6694113cfd2c034a61a494945d
- Cited by
- 225
- References
- 37
- Citations by year
- 2026: 8 · 2025: 10 · 2024: 16 · 2023: 15 · 2022: 22 · 2021: 13 · 2020: 18 · 2019: 19 · 2018: 9 · 2017: 21 · 2016: 10 · 2015: 20 · 2014: 25 · 2013: 14 · 2012: 4
- FWCI
- 30.31
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of the American Academy of Child & Adolescent Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (DP5OD031858)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Social Sciences › Psychology › Social Psychology › Attachment and Relationship Dynamics
- Social Sciences › Psychology › Social Psychology › Action Observation and Synchronization
- Keywords
- oxytocin, vasopressin, social cognition, empathy, amygdala activation, infant cues, infant play, attachment, parental bonding
- MeSH terms
- Adult, Female, Humans, Infant, Limbic System, Magnetic Resonance Imaging, Male, Maternal Behavior, Neuropsychology, Object Attachment, Oxytocin, Parent-Child Relations, Parents, Paternal Behavior, Play and Playthings, Vasopressins, Videotape Recording, Parenting
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
