Cited by 225Stress Responses and CortisolNeurotransmitter Receptor Influence on BehaviorNeuroendocrine regulation and behavior

Impact of adolescent social experiences on behavior and neural circuits implicated in mental illnesses

Burke, Andrew R., McCormick, Cheryl M., Pellis, Sergio M., Lukkes, Jodi L.·2017·Neuroscience & Biobehavioral Reviews

Abstract

Negative social experiences during adolescence are central features for several stress-related mental illnesses. Social play fighting behavior in rats peaks during early adolescence and is essential for the final maturation of brain and behavior. Manipulation of the rat adolescent social experience alters many neurobehavioral measurements implicated in anxiety, depression, and substance abuse. In this review, we will highlight the importance of social play and the use of three separate social stress models (isolation-rearing, social defeat, and social instability stress) to disrupt the acquisition of this adaptive behavior. Social stress during adolescence leads to the development of anxiety and depressive behavior as well as escalated drug use in adulthood. Furthermore, sex- and age-dependent effects on the hormonal stress response following adolescent social stress are also observed. Finally, manipulation of the social experience during adolescence alters stress-related neural circuits and monoaminergic systems. Overall, positive social experiences among age-matched conspecifics during rat adolescence are critical for healthy neurobehavioral maturation.

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Crossref · 10.1016/j.neubiorev.2017.01.018

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  • Studies depriving rodents of peer contact during peak social play periods (postnatal days 21-43, roughly early to mid adolescence in humans) show increased anxiety-like and depression-like behaviours, reward seeking, impaired reward learning, and impaired habituation to novel stimuli.

    “In most of these studies, animals were isolated from peers from around postnatal days 21 to 43, corresponding roughly to early adolescence (aged 10–13 years) and mid adolescence (aged 14–16 years) in humans.34 Such studies show similar effects to those investigating isolation throughout the whole adolescent period, including increased anxiety-like behaviours, depression-like behaviours, and reward”
  • Rodent research shows social isolation causes substantial changes in brain and behaviour, especially if isolation occurs during development.

    “This rodent research has shown that social isolation causes substantial changes in brain and behaviour,31 especially if isolation occurs during development.33, 34”
  • After weaning, rodents show a strong orientation towards peers, actively seek peer interaction, and these interactions are important for healthy development and social learning.

    “Similar to adolescent humans, after weaning, rodents show a strong orientation towards their peers.38 These animals actively seek out peer interaction and these interactions are considered to be important social input for healthy development39 and specifically for social learning.34”
  • Adolescent isolation alters serotonin levels, with increased serotonergic activity in prefrontal cortex and decreased activity in hippocampus.

    “Additional neurochemical changes include alterations to serotonin levels, with the direction of the effects differing between brain regions. For example, the prefrontal cortex shows increased serotonergic activity, whereas other brain areas, such as the hippocampus, show decreased activity. These alterations have been proposed to underlie observed behavioural changes such as increased anxiety and”
  • Studying rough-and-tumble play can be a valuable tool both for basic research on communication and other processes involved in regulating social behavior and for translational research on neurodevelopmental disorders.

    “Studying RTP can be a valuable tool both for basic research on communication and other processes that are involved in regulating social behavior (Palagi et al., 2016b), and for translational research on neurodevelopmental disorders (Burke et al., 2017).”

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References 321 · Cited by 225

Authors
Burke, A. R., McCormick, C. M., Pellis, S. M., & Lukkes, J. L.
Affiliations
  • Indiana University School of Medicine (US)
  • Brock University (CA)
  • University of Lethbridge (CA)
Corresponding author
Burke, Andrew R.
Venue
Neuroscience & Biobehavioral Reviews
Publisher
Elsevier BV
Published
2017-05
Volume
76
Issue
Pt B
Pages
280-300
ISSN
0149-7634 (ISSN-L)
OpenAlex
W2578057592
Cited by
225
References
321
Citations by year
2026: 19 · 2025: 19 · 2024: 18 · 2023: 24 · 2022: 34 · 2021: 38 · 2020: 26 · 2019: 17 · 2018: 20 · 2017: 9
FWCI
1.74
Type
journal article
Language
en
Open access
closed
Locations
  • Neuroscience & Biobehavioral Reviews (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • Brain and Behavior Research Foundation
  • Natural Sciences and Engineering Research Council Discovery
Topics
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Keywords
social stress, isolation rearing, social defeat, anxiety, depression, substance abuse, stress response, sex differences, age-dependent effects, monoaminergic systems, neural circuits, rats
MeSH terms
Adaptation, Psychological, Adolescent, Animals, Anxiety, Brain, Depression, Humans, Social Behavior, Stress, Psychological

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