Cited by 570Neuroendocrine regulation and behaviorHuman-Animal Interaction StudiesAttachment and Relationship Dynamics

Early experience in humans is associated with changes in neuropeptides critical for regulating social behavior

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Fries, Alison B. Wismer, Ziegler, Toni E., Kurian, Joseph R., Jacoris, Steve, Pollak, Seth D.·2005·Proceedings of the National Academy of Sciences

Abstract

The formation of social attachments is a critical component of human relationships. Infants begin to bond to their caregivers from the moment of birth, and these social bonds continue to provide regulatory emotional functions throughout adulthood. It is difficult to examine the interactions between social experience and the biological origins of these complex behaviors because children undergo both brain development and accumulate social experience at the same time. We had a rare opportunity to examine children who were reared in extremely aberrant social environments where they were deprived of the kind of care-giving typical for our species. The present experiment in nature provides insight into the role of early experience on the brain systems underlying the development of emotional behavior. These data indicate that the vasopressin and oxytocin neuropeptide systems, which are critical in the establishment of social bonds and the regulation of emotional behaviors, are affected by early social experience. The results of this experiment suggest a potential mechanism whose atypical function may explain the pervasive social and emotional difficulties observed in many children who have experienced aberrant care-giving. The present findings are consistent with the view that there is a critical role for early experience in the development of the brain systems underlying basic aspects of human social behavior.

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Crossref · 10.1073/pnas.0504767102

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  • Wismer Fries et al. reported that urinary oxytocin and vasopressin in orphans were affected by early neglect, but their reported levels were nearly a million-fold too high for both peptides, using a method neither sensitive nor selective enough to measure either peptide in urine; the report drew criticism, and the authors later improved their methodology.

    “The discrepancy between measurements in unextracted and extracted plasma is two orders of magnitude, but when Wismer Fries et al. reported that urinary excretion of oxytocin and vasopressin in orphans was affected by early neglect, they reported levels that were, for both peptides, nearly a million fold too high, after applying a method that was neither sensitive enough or selective enough to”

    From Intranasal Oxytocin: Myths and Delusions (2016) · cites this paper as [72]

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  • Adopted children do not show an increase in oxytocin levels after playing a physical contact game with their mothers, unlike birth children.

    “Unlike birth children, adopted children do not show an increase in oxytocin levels after playing a physical contact game with their mothers (Wismer Fries et al., 2005).”

    From The evolved nest, oxytocin functioning, and prosocial development (2023) · cites this paper as Wismer Fries et al., 2005

    The Results report that oxytocin increased after physical contact with mothers in family-reared children but not in children who had experienced early neglect. The Method identifies the latter group as children adopted after living in orphanages. The claim omits that restriction and therefore generalizes the finding to adopted children as a whole. (LLM, conf=0.88)

    Experimental — accuracy not yet measured
  • The buffering effect of oxytocin and social support is dependent upon early experience.

    “Studies comparing children from orphanages to children under typical conditions demonstrate that the buffering effect of oxytocin and social support are dependent upon early experience.”

    From The evolved nest, oxytocin functioning, and prosocial development (2023) · cites this paper as Wismer Fries et al., 2005

    The Results report that physical contact with mothers increased oxytocin levels in family-reared children but not in previously institutionalized children. They suggest that disruption of this system may interfere with the calming and comforting effects of caregiving. The study did not directly test a buffering effect of oxytocin and social support, so saying it demonstrates that effect overstates the finding. (LLM, conf=0.85)

    Experimental — accuracy not yet measured
  • The oxytocin system of children who have suffered severe neglect appeared less responsive to contact with bond partners.

    “The oxytocin system of children who have suffered severe neglect appeared less responsive to contact with bond partners (Fries et al., 2005).”
  • Children who played with their principle carer rather than with strangers showed higher urinary oxytocin levels, whereas orphans who had suffered severe neglect showed no change in urinary oxytocin levels across conditions.

    “In other human studies, Fries et al. (2005) showed that children who played with their principle carer rather than with strangers showed higher urinary oxytocin levels whereas orphans who had suffered severe neglect showed no change in urinary oxytocin levels across conditions.”

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Cited by

Sorted by citations

Authors
Fries, A. B. W., Ziegler, T. E., Kurian, J. R., Jacoris, S., & Pollak, S. D.
Affiliations
University of Wisconsin–Madison (US)
Corresponding author
Pollak, Seth D.
Venue
Proceedings of the National Academy of Sciences
Published
2005-11-22
Volume
102
Issue
47
Pages
17237-17240
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
OpenAlex
W1635412086
Cited by
570
References
50
Citations by year
2026: 5 · 2025: 10 · 2024: 16 · 2023: 11 · 2022: 16 · 2021: 20 · 2020: 21 · 2019: 35 · 2018: 26 · 2017: 28 · 2016: 44 · 2015: 32 · 2014: 36 · 2013: 33 · 2012: 38
FWCI
35.24
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Waisman Center (P30 HD03352, HD03352)
  • National Institutes of Health (HD033.52)
  • U.S. Public Health Service (R01 035215)
  • National Institute of Mental Health (T32MH18931, R01MH068858, T32MH018931, R01MH061285)
  • National Center for Research Resources (P51RR000167)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD03352., P30HD003352)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Human-Animal Interaction Studies
  • Social Sciences › Psychology › Social Psychology › Attachment and Relationship Dynamics
Keywords
early social experience, social deprivation, vasopressin, oxytocin, neuropeptides, social attachment, emotional behavior, brain development, children, social bonding, emotional problems
MeSH terms
Child Abuse, Child, Preschool, Female, Humans, Life Change Events, Male, Neuropeptides, Neurophysins, Oxytocin, Protein Precursors, Social Behavior, Socialization, Vasopressins

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