Cited by 131Neuroendocrine regulation and behaviorHuman-Animal Interaction StudiesStress Responses and Cortisol

Early interactions with mother and peers independently build adult social skills and shape BDNF and oxytocin receptor brain levels

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Branchi, Igor, Curley, James P., D’Andrea, Ivana, Cirulli, Francesca, Champagne, Frances A., Alleva, Enrico·2013·Psychoneuroendocrinology

Abstract

The early social environment has a profound impact on developmental trajectories. Although an impoverished early environment can undermine the acquisition of appropriate social skills, the specific role played by the different components of an individual's early environment in building social competencies has not been fully elucidated. Here we setup an asynchronous communal nesting paradigm in mice to disentangle the influence of maternal care and early peer interactions on adult social behavior and neural systems reportedly involved in the regulation of social interactions. The asynchronous communal nesting consists of three mothers giving birth three days apart, generating three groups of pups - the Old, the Middle and the Young - all raised in a single nest from birth to weaning. We scored the amount of maternal and peer interactions received by these mice and by a fourth group reared under standard conditions. At adulthood, the four experimental groups have been investigated for social behavior in a social interaction test, i.e. facing an unfamiliar conspecific during five 20-min daily encounters, and for oxytocin receptor and brain derived neurotrophic factor (BDNF) levels. Results show that only individuals exposed to high levels of both maternal and peer interactions demonstrated elaborate adult agonistic competencies, i.e. the ability to promptly display a social status, and high BDNF levels in the hippocampus, frontal cortex and hypothalamus. By contrast, only individuals exposed to high levels of peer interactions showed enhanced adult affiliative behavior and enhanced oxytocin receptor levels in selected nuclei of the amygdala. Overall these findings indicate that early interactions with mother and peers independently shape specific facets of adult social behavior and neural systems involved in social interaction.

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Crossref · 10.1016/j.psyneuen.2012.07.010

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  • For social mammals, communal rearing facilitates an increased ability to engage and interact appropriately with differing environments and contexts.

    “This suggests that for social mammals communal rearing facilitates an increased ability to engage and interact appropriately with differing environments and contexts (Branchi et al., 2013).”

    From The evolved nest, oxytocin functioning, and prosocial development (2023) · cites this paper as Branchi et al., 2013

    The Discussion (page unavailable) reports that communally reared mice receiving high levels of both maternal care and peer interaction developed greater adult social competence, adapting their behavior to an unfamiliar mouse and the social context. The study does not establish this for social mammals generally or for differing environments beyond social interactions. (LLM, conf=0.85)

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Authors
Branchi, I., Curley, J. P., D’Andrea, I., Cirulli, F., Champagne, F. A., & Alleva, E.
Affiliations
  • Istituto Superiore di Sanità (IT)
  • Columbia University (US)
  • Istituto Neurologico Mediterraneo (IT)
Corresponding author
Branchi, Igor
Venue
Psychoneuroendocrinology
Publisher
Elsevier BV
Published
2013-04
Volume
38
Issue
4
Pages
522-532
ISSN
0306-4530 (ISSN-L)
OpenAlex
W2126415643
Cited by
131
References
16
Citations by year
2026: 10 · 2025: 7 · 2024: 11 · 2023: 3 · 2022: 9 · 2021: 4 · 2020: 10 · 2019: 13 · 2018: 7 · 2017: 7 · 2016: 13 · 2015: 15 · 2014: 15 · 2013: 7
FWCI
17.85
Type
journal article
Language
en
Open access
Locations
  • Psychoneuroendocrinology (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institutes of Health (DP2OD001675, 1dp2od001674-01)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Human-Animal Interaction Studies
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords
early social environment, maternal care, peer interaction, social skills, brain-derived neurotrophic factor, oxytocin receptor, agonistic behavior, affiliative behavior, hippocampus, amygdala, hypothalamus, frontal cortex, mice
MeSH terms
Age Factors, Animals, Behavior, Animal, Brain, Female, Male, Maternal Behavior, Nesting Behavior, Peer Group, Social Behavior, Receptors, Oxytocin, Brain-Derived Neurotrophic Factor, Mice

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