Cited by 399Neuroendocrine regulation and behaviorAttachment and Relationship DynamicsInfant Health and Development

Specifying the Neurobiological Basis of Human Attachment: Brain, Hormones, and Behavior in Synchronous and Intrusive Mothers

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Atzil, Shir, Hendler, Talma, Feldman, Ruth·2011·Neuropsychopharmacology

Abstract

The mother-infant bond provides the foundation for the infant's future mental health and adaptation and depends on the provision of species-typical maternal behaviors that are supported by neuroendocrine and motivation-affective neural systems. Animal research has demonstrated that natural variations in patterns of maternal care chart discrete profiles of maternal brain-behavior relationships that uniquely shape the infant's lifetime capacities for stress regulation and social affiliation. Such patterns of maternal care are mediated by the neuropeptide Oxytocin and by stress- and reward-related neural systems. Human studies have similarly shown that maternal synchrony--the coordination of maternal behavior with infant signals--and intrusiveness--the excessive expression of maternal behavior--describe distinct and stable maternal styles that bear long-term consequences for infant well-being. To integrate brain, hormones, and behavior in the study of maternal-infant bonding, we examined the fMRI responses of synchronous vs intrusive mothers to dynamic, ecologically valid infant videos and their correlations with plasma Oxytocin. In all, 23 mothers were videotaped at home interacting with their infants and plasma OT assayed. Sessions were micro-coded for synchrony and intrusiveness. Mothers were scanned while observing several own and standard infant-related vignettes. Synchronous mothers showed greater activations in the left nucleus accumbens (NAcc) and intrusive mothers exhibited higher activations in the right amygdala. Functional connectivity analysis revealed that among synchronous mothers, left NAcc and right amygdala were functionally correlated with emotion modulation, theory-of-mind, and empathy networks. Among intrusive mothers, left NAcc and right amygdala were functionally correlated with pro-action areas. Sorting points into neighborhood (SPIN) analysis demonstrated that in the synchronous group, left NAcc and right amygdala activations showed clearer organization across time, whereas among intrusive mothers, activations of these nuclei exhibited greater cross-time disorganization. Correlations between Oxytocin with left NAcc and right amygdala activations were found only in the synchronous group. Well-adapted parenting appears to be underlay by reward-related motivational mechanisms, temporal organization, and affiliation hormones, whereas anxious parenting is likely mediated by stress-related mechanisms and greater neural disorganization. Assessing the integration of motivation and social networks into unified neural activity that reflects variations in patterns of parental care may prove useful for the study of optimal vs high-risk parenting.

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Crossref · 10.1038/npp.2011.172

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  • Both the early stages of romantic love and early parental love are characterized by typical behaviors, mental states, and activations of specific brain structures.

    “Both the early stages of romantic love and early parental love are characterized by typical behaviors, mental states, and activations of specific brain structures (Atzil et al., 2011; Bartels and Zeki, 2004; Leckman et al., 1999; van Anders et al., 2011).”

    From Oxytocin during the initial stages of romantic attachment: Relations to couples’ interactive reciprocity (2012) · cites this paper as Atzil et al., 2011

    The Introduction describes characteristic maternal behaviors and brain regions involved in human parenting, while the Discussion links maternal behavior to mental processes and neural activation. This supports the early parental-love portion, but the paper does not discuss the behaviors, mental states, and brain activations of early romantic love; romantic love appears only in reference titles. (LLM, conf=0.86)

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  • Gaze and affect are the main non-verbal channels of social communication.

    “Gaze and affect, the main non-verbal channels of social communication, were coded using a set of mutually-exclusive codes consistent with our prior brain and behavioral research20,64.”
  • The microlevel second-by-second coding scheme used was previously validated in the authors' lab and consistent with prior research showing correlations between these micro-level behaviors and brain activations.

    “We used a microlevel second-by-second coding scheme previously validated in our lab and consistent with prior research that showed correlations between these micro-level behaviors and brain activations64.”
  • Plasma OT is associated with bonding-related cognitions and increased activations in motivational-limbic brain areas in response to infant stimuli.

    “plasma OT has been associated with bonding-related cognitions (11) and increased activations in motivational-limbic brain areas in response to infant stimuli (12).”
  • When intrusive and synchronous mothers were compared, intrusive mothers showed greater responses in the amygdala to their own babies, whereas synchronous mothers showed greater activation in the NAcc.

    “When intrusive and synchronous mothers were compared, intrusive mothers showed greater responses in the amygdala to their own babies, whereas synchronous mothers showed greater activation in the NAcc.”

    From The maternal brain and its plasticity in humans (2016) · cites this paper as Atzil et al., 2011

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Authors
Atzil, S., Hendler, T., & Feldman, R.
Affiliations
  • Bar-Ilan University (IL)
  • Tel Aviv University (IL)
Corresponding author
Feldman, Ruth
Venue
Neuropsychopharmacology
Published
2011-08-31
Volume
36
Issue
13
Pages
2603-2615
ISSN
  • 0893-133X (ISSN-L)
  • 1740-634X
OpenAlex
W2004120576
Cited by
399
References
90
Citations by year
2026: 10 · 2025: 22 · 2024: 27 · 2023: 34 · 2022: 27 · 2021: 36 · 2020: 38 · 2019: 24 · 2018: 21 · 2017: 29 · 2016: 33 · 2015: 32 · 2014: 27 · 2013: 18 · 2012: 18
FWCI
27.60
Type
journal article
Language
en
Open access
Locations
  • Neuropsychopharmacology (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Alliance for Research on Schizophrenia and Depression
  • Israel Science Foundation (#1318/08)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Social Sciences › Psychology › Social Psychology › Attachment and Relationship Dynamics
  • Health Sciences › Health Professions › Pharmacy › Infant Health and Development
Keywords
maternal-infant bonding, maternal intrusiveness, oxytocin, nucleus accumbens, amygdala, functional connectivity, emotion regulation, theory of mind, empathy, reward processing, stress regulation
MeSH terms
Adult, Brain, Female, Humans, Infant, Male, Maternal Behavior, Mother-Child Relations, Oxytocin, Stress, Psychological, Young Adult

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