Cited by 89Cannabis and Cannabinoid ResearchNeuroendocrine regulation and behaviorStress Responses and Cortisol

Adverse Social Experiences in Adolescent Rats Result in Enduring Effects on Social Competence, Pain Sensitivity and Endocannabinoid Signaling

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Schneider, Peggy, Bindila, Laura, Schmahl, Christian, Bohus, Martin, Meyer-Lindenberg, Andreas, Lutz, Beat, Spanagel, Rainer, Schneider, Miriam·2016·Frontiers in Behavioral Neuroscience

Abstract

Social affiliation is essential for many species and gains significant importance during adolescence. Disturbances in social affiliation, in particular social rejection experiences during adolescence, affect an individual’s well-being and are involved in the emergence of psychiatric disorders. The underlying mechanisms are still unknown, partly because of a lack of valid animal models. By using a novel animal model for social peer-rejection, which compromises adolescent rats in their ability to appropriately engage in playful activities, here we report on persistent impairments in social behavior and dysregulations in the endocannabinoid system. From postnatal day (pd) 21 to pd 50 adolescent female Wistar rats were either reared with same-strain partners (control) or within a group of Fischer 344 rats (inadequate social rearing, ISR), previously shown to serve as inadequate play partners for the Wistar strain. Adult ISR animals showed pronounced deficits in social interaction, social memory, processing of socially transmitted information, and decreased pain sensitivity. Molecular analysis revealed increased CB1 receptor protein levels and CP55,940 stimulated [35S]GTPγS binding activity specifically in the amygdala and thalamus in previously peer-rejected rats. Along with these changes, increased levels of the endocannabinoid anandamide and a corresponding decrease of its degrading enzyme fatty acid amide hydrolase were seen in the amygdala. Our data indicate lasting consequences in social behavior and pain sensitivity following peer-rejection in adolescent female rats. These behavioral impairments are accompanied by persistent alterations in CB1 receptor signaling. Finally, we provide a novel translational approach to characterize neurobiological processes underlying social peer-rejection in adolescence.

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Crossref · 10.3389/fnbeh.2016.00203

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  • The development of the medial prefrontal cortex and associated socio-cognitive skills is influenced by the experience of rough-and-tumble play with peers in the juvenile period (about 28-40 days post birth).

    “the development of the medial prefrontal cortex (mPFC) and associated socio-cognitive skills is influenced by the experience of RTP with peers in the juvenile period (about 28–40 days post birth; Bell et al., 2010; Baarendse et al., 2013; Schneider et al., 2016)”

    From The rough-and-tumble play of rats as a natural behavior suitable for studying the social brain (2022) · cites this paper as Schneider et al., 2016

    The Introduction says peer play is crucial for social competence and reports that play deprivation interferes with fronto-cortical development. The Methods examine play on postnatal days 30 and 35, but the copy does not establish the full 28–40-day window or report a medial prefrontal cortex finding from this study. (LLM, conf=0.82)

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  • The convergence of evidence from this study and others using different manipulations points to play experience being the critical driver of the impairments observed.

    “Nevertheless, the convergence of evidence from our study and others using different manipulations (e.g., reducing play by rearing juveniles with an adult or a peer from a less playful strain) points to play experience being the critical driver of the impairments observed (Schneider et al., 2016; Burleson et al., 2016; Pellis et al., 2017; Stark and Pellis, 2020, 2021).”

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Authors
Schneider, P., Bindila, L., Schmahl, C., Bohus, M., Meyer-Lindenberg, A., Lutz, B., Spanagel, R., & Schneider, M.
Affiliations
  • Heidelberg University (DE)
  • University of Antwerp (BE)
  • University Medical Center of the Johannes Gutenberg University Mainz (DE)
Corresponding author
Schneider, Miriam
Venue
Frontiers in Behavioral Neuroscience
Published
2016-10-20
Volume
10
Pages
203-203
ISSN
1662-5153 (ISSN-L)
OpenAlex
W2538922124
Cited by
89
References
80
Citations by year
2026: 4 · 2025: 7 · 2024: 11 · 2023: 14 · 2022: 15 · 2021: 8 · 2020: 8 · 2019: 8 · 2018: 6 · 2017: 7
FWCI
5.67
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Deutsche Forschungsgemeinschaft (KFO256 (SCHN958/5-1), FOR926 (SCHN958/4-1))
  • Bundesministerium für Bildung und Forschung (BMBF01EE1406C)
Topics
  • Health Sciences › Medicine › Pharmacology › Cannabis and Cannabinoid Research
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords
social rejection, peer rejection, adolescence, social affiliation, social competence, social memory, pain sensitivity, endocannabinoid system, CB1 receptor, anandamide, fatty acid amide hydrolase, amygdala, thalamus, female rats, animal models, mental illness

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