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Cited by 86Neuroendocrine regulation and behaviorStress Responses and CortisolMemory and Neural Mechanisms

Long-lasting consequences of neonatal maternal separation on social behaviors in ovariectomized female mice.

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Tsuda, Mumeko C., Ogawa, Sonoko·2012·PLoS ONE
DOI 10.1371/journal.pone.0033028PMC PMC3296763
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Abstract

Maternal separation (MS) stress is known to induce long-lasting alterations in emotional and anxiety-related behaviors, but effects on social behaviors are not well defined. The present study examined MS effects on female social behaviors in the social investigation (SIT) and social preference (SPT) tests, in addition to non-social behaviors in the open-field (OFT) and light-dark transition (LDT) tests in C57BL/6J mice. All females were tested as ovariectomized to eliminate confounding effects of endogenous estrogen during behavioral testing. Daily MS (3 hr) from postnatal day 1 to 14 did not affect anxiety levels in LDT, but were elevated in OFT with modified behavioral responses to the novel environment. Furthermore, MS altered social investigative behaviors and preference patterns toward unfamiliar stimulus mice in SIT and short- and long-term SPT paradigms. In SIT, MS reduced social investigation duration and increased number of stretched approaches towards both female and male unfamiliar stimulus mice, suggesting increased social anxiety levels in MS females. Similarly, MS heightened levels of social anxiety during short-term SPT but no MS effect on social preference was found. On the other hand, MS females displayed a distinctive preference for female stimuli, unlike control females, when tested for long-term SPT over a prolonged period of 5 days. Evaluation of FosB expression in the paraventricular nucleus, medial and central amygdala following stimulus exposure demonstrated greater number of FosB immunopositive cells in all three brain regions in MS females compared to control females. These results suggest that MS females might differ in neuroendocrine responses toward unfamiliar female and male opponents, which may be associated with modifications in social behaviors found in the present study. Taken together, this study provides new evidence that early life stress modifies female social behaviors by highlighting alterations in behavioral responses to situations involving social as well as non-social novelty.

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  • 3 h of daily maternal separation reduced social interest in both adult male and female mandarin voles and mice.

    “It was observed that 3 h of daily maternal separation reduced social interest (i.e., time spent exploring a conspecific) in both adult male and female mandarin voles (Wei et al., 2013; Yu et al., 2013) and mice (Tsuda and Ogawa, 2012; Zoicas and Neumann, 2016).”

    From Effects of Maternal Deprivation and Complex Housing on Rat Social Behavior in Adolescence and Adulthood (2018) · cites this paper as Tsuda and Ogawa, 2012

    The Methods (Maternal Separation Procedure) report daily 3-hour separation and specify that only female offspring mice were studied. The Results (MS Effects on Social Preference Patterns) report less social investigation by separated adult females. This source does not establish the claim for adult male mice; the vole findings are attributed to other citations in the sentence. (LLM, conf=0.88)

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Authors
Tsuda, M. C., & Ogawa, S.
Affiliations
University of Tsukuba (JP)
Corresponding author
Ogawa, Sonoko
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2012-03-07
Volume
7
Issue
3
Pages
e33028
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0033028
PMC
PMC3296763
OpenAlex
W2135828915
Cited by
86
References
9
Citations by year
2026: 1 · 2025: 2 · 2024: 5 · 2023: 10 · 2022: 8 · 2021: 12 · 2020: 2 · 2019: 7 · 2018: 8 · 2017: 8 · 2016: 4 · 2015: 5 · 2014: 6 · 2013: 4 · 2012: 4
FWCI
9.17
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • University of Tsukuba
  • Japan Society for the Promotion of Science (23653219, 23240057, 17330151, 17052001)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
maternal separation, early life stress, female social behavior, social anxiety, social investigation, social preferences, ovariectomy, FosB, paraventricular nucleus, amygdala, sex differences, C57BL/6J mice
MeSH terms
Animals, Anxiety, Behavior, Animal, Emotions, Female, Male, Maternal Deprivation, Mice, Inbred C57BL, Ovariectomy, Pregnancy, Social Behavior, Proto-Oncogene Proteins c-fos, Mice

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