Consequences of post-weaning social isolation on anxiety behavior and related neural circuits in rodents

Lukkes, Jodi L.

doi:10.3389/neuro.08.018.2009

Cited by 235Stress Responses and CortisolNeuroendocrine regulation and behaviorNeurotransmitter Receptor Influence on Behavior

Consequences of post-weaning social isolation on anxiety behavior and related neural circuits in rodents

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Lukkes, Jodi L.·2009·Frontiers in Behavioral Neuroscience

DOI 10.3389/neuro.08.018.2009PMC PMC2737489

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Abstract

Exposure to adverse experiences in early-life is implicated in the later vulnerability to development of psychiatric disorders, including anxiety and affective disorders in humans. Adverse early-life experiences likely impart their long-term consequences on mental health by disrupting the normal development of neural systems involved in stress responses, emotional behavior and emotional states. Neural systems utilizing the neurotransmitters serotonin, dopamine and the neuropeptide corticotropin-releasing factor (CRF) are implicated in mediating emotive behaviors, and dysfunction of these neurochemical systems is associated with mood/anxiety disorders. These neural systems continue maturing until early or mid-adolescence in humans, thus alterations to their development are likely to contribute to the long-term consequences of adverse early-life experiences. A large body of literature suggests that post-weaning isolation rearing of rodents models the behavioral consequences of adverse early-life experiences in humans. Overall, the majority findings suggest that post-weaning social isolation that encompasses pre-adolescence produces long-lasting alterations to anxiety behavior, while measures of monoaminergic activity in various limbic regions during social isolation suggest alterations to dopamine and serotonin systems. The goal of this review is to evaluate and integrate findings from post-weaning social isolation studies specifically related to altered fear and anxiety behaviors and associated changes in neuroendocrine function and the activity of monoaminergic systems.

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Complete social isolation in adolescent rodents evokes widespread structural and functional brain changes, most prominently in dopamine and serotonin systems and cortical/striatal targets.
“Complete social isolation in adolescent rodents evokes widespread structural and functional changes in the brain, most prominently in neuromodulatory dopamine and serotonin systems and particularly within cortical and striatal targets.33, 36, 37”
From The effects of social deprivation on adolescent development and mental health (2020) · cites this paper as [37]
The sections on dopaminergic function report isolation-associated changes in dopamine innervation and activity in the medial prefrontal cortex and nucleus accumbens, alongside changes in serotonin activity. But the review focuses on particular anxiety-related circuits; it does not establish that structural and functional changes are widespread across the brain or that cortical and striatal targets are the most affected. Page numbers are unavailable in our copy. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Rodent development progresses through similar stages as human development.
“An advantage of rodent animal models such as mice and rats is that their development progresses through similar stages as human development.37”
From The effects of social deprivation on adolescent development and mental health (2020) · cites this paper as [37]
Most consistent findings report increased dopamine release in reward regions such as nucleus accumbens and decreased dopamine activity in prefrontal cortex following adolescent isolation.
“More specifically, although some divergent effects have been observed, the most consistent findings report that dopamine release in reward regions such as the nucleus accumbens increases following adolescent isolation, but dopamine activity in the prefrontal cortex decreases.33, 36, 37”
From The effects of social deprivation on adolescent development and mental health (2020) · cites this paper as [37]
By depriving animals of play experiences that normally guide cortical development, post-weaning social isolation is conceptualized as a rodent model of adolescent adversity with long-lasting effects on neurobiology and behavior.
“By depriving animals of the play experiences that normally guide cortical development, post-weaning social isolation is conceptualized as a rodent model of adolescent adversity with long-lasting effects on neurobiology and behavior (Fone and Porkess, 2008; Lukkes et al., 2009; Robbins, 2016).”
From The effects of early life stress on reward processing (2018) · cites this paper as Lukkes et al., 2009
Post-weaning social isolation during the juvenile and adolescent period produces sensory processing deficits and increases in fear and anxiety-like behavior.
“While pre-weaning maternal separation is often conceptualized as early life neglect and results in a depressive-like phenotype (Pryce et al., 2005), post-weaning social isolation during the juvenile and adolescent period produces sensory processing deficits and increases in fear and anxiety-like behavior (Fone and Porkess, 2008; Lukkes et al., 2009).”
From The effects of early life stress on reward processing (2018) · cites this paper as Lukkes et al., 2009

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Brain corticotropin-releasing hormone (CRH) circuits in the developing rat: Effect of maternal deprivation
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The effects of social deprivation on adolescent development and mental health
Orben, A., Tomova, L., & Blakemore, S.-J. (2020) · The Lancet Child & Adolescent Health · doi:10.1016/s2352-4642(20)30186-3 · Cited by 1,229 · see citing works
Adolescent alcohol exposure: Are there separable vulnerable periods within adolescence?
SPEAR, L. P. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.01.027 · Cited by 364 · see citing works
Neurobiology and consequences of social isolation stress in animal model—A comprehensive review
Mumtaz, F., Khan, M. I., Zubair, M., & Dehpour, A. R. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.05.086 · Cited by 369 · see citing works
Impact of adolescent social experiences on behavior and neural circuits implicated in mental illnesses
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Stress in adolescence and drugs of abuse in rodent models: role of dopamine, CRF, and HPA axis
Burke, A. R., & Miczek, K. A. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3369-1 · Cited by 207 · see citing works
Social influences on neurobiology and behavior: Epigenetic effects during development
Curley, J. P., Jensen, C. L., Rahia Mashoodh, A., & Champagne, F. A. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.06.005 · Cited by 195 · see citing works
The effects of early life stress on reward processing
Novick, A. M., Levandowski, M. L., Laumann, L. E., Philip, N. S., Price, L. H., & Tyrka, A. R. (2018) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2018.02.002 · Cited by 192 · see citing works
“By depriving animals of the play experiences that normally guide cortical development, post-weaning social isolation is conceptualized as a rodent model of adolescent adversity with long-lasting effects on neurobiology and behavior (Fone and Porkess, 2008; Lukkes et al., 2009; Robbins, 2016).”
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Understanding stress: Insights from rodent models
Atrooz, F., Alkadhi, K. A., & Salim, S. (2021) · Current Research in Neurobiology · doi:10.1016/j.crneur.2021.100013 · Cited by 201 · see citing works
Adolescence and Reward: Making Sense of Neural and Behavioral Changes Amid the Chaos
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Animal Models of Depression: What Can They Teach Us about the Human Disease?
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Social deprivation enhances VTA synaptic plasticity and drug-induced contextual learning
Whitaker, L. R., Degoulet, M., & Morikawa, H. (2013) · Neuron · doi:10.1016/j.neuron.2012.11.022 · Cited by 177 · see citing works
Rodent Models of Depression: Neurotrophic and Neuroinflammatory Biomarkers
Stepanichev, M. Y., Дыгало, Н. Н., Grigoryan, G. A., Shishkina, G. T., & Gulyaeva, N. V. (2014) · BioMed Research International · doi:10.1155/2014/932757 · Cited by 172 · see citing works
Ethological approach to social isolation effects in behavioral studies of laboratory rodents
Arakawa, H. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.12.022 · Cited by 144 · see citing works
Long-Term Behavioral Effects of Post-weaning Social Isolation in Males and Females
Walker, D. M., Cunningham, A. M., Gregory, J. K., & Nestler, E. J. (2019) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2019.00066 · Cited by 139 · see citing works
Enduring increases in anxiety‐like behavior and rapid nucleus accumbens dopamine signaling in socially isolated rats
Yorgason, J. T., España, R. A., Konstantopoulos, J. K., Weiner, J. L., & Jones, S. R. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12113 · Cited by 132 · see citing works
The effects of allostatic load on neural systems subserving motivation, mood regulation, and social affiliation
Beauchaine, T. P., Neuhaus, E., Zalewski, M., Crowell, S. E., & Potapova, N. V. (2011) · Development and Psychopathology · doi:10.1017/s0954579411000459 · Cited by 129 · see citing works
Neuroplastic Correlates in the mPFC Underlying the Impairment of Stress-Coping Ability and Cognitive Flexibility in Adult Rats Exposed to Chronic Mild Stress during Adolescence
Zhang, Y., Shao, F., Wang, Q., Xie, X., & Wang, W. (2017) · Neural Plasticity · doi:10.1155/2017/9382797 · Cited by 125 · see citing works
Isolation rearing attenuates social interaction-induced expression of immediate early gene protein products in the medial prefrontal cortex of male and female rats
Wall, V. L., Fischer, E. K., & Bland, S. T. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.09.002 · Cited by 123 · see citing works
The impact of loneliness and social isolation on the development of cognitive decline and Alzheimer’s Disease
Ren, Y. L., Savadlou, A., Park, S., Siska, P., Epp, J. R., & Sargin, D. (2023) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2023.101061 · Cited by 130 · see citing works
Effects of Degree and Timing of Social Housing on Reversal Learning and Response to Novel Objects in Dairy Calves
Meagher, R. K., Daros, R. R., Costa, J. H. C., von Keyserlingk, M. A. G., Hötzel, M. J., & Weary, D. M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132828 · Cited by 121 · see citing works
Exposure to early adversity: points of cross-species translation that can lead to improved understanding of depression
Andersen, S. L. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000103 · Cited by 116 · see citing works
Adolescent Social Isolation as a Model of Heightened Vulnerability to Comorbid Alcoholism and Anxiety Disorders
Butler, T. R., Karkhanis, A. N., Jones, S. R., & Weiner, J. L. (2016) · Alcoholism Clinical and Experimental Research · doi:10.1111/acer.13075 · Cited by 105 · see citing works
Differential neuronal changes in medial prefrontal cortex, basolateral amygdala and nucleus accumbens after postweaning social isolation
Wang, Y., Ho, U., Ko, M., Liao, C., & Lee, L. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0355-4 · Cited by 102 · see citing works
Cortisol levels in relation to maternal interaction and child internalizing behavior in preterm and full‐term children at 18 months corrected age
Brummelte, S., GRUNAU, R. E., Zaidman‐Zait, A., Weinberg, J., Nordstokke, D., & Cepeda, I. L. (2010) · Developmental Psychobiology · doi:10.1002/dev.20511 · Cited by 92 · see citing works
Brief social isolation in early adolescence affects reversal learning and forebrain BDNF expression in adult rats
Xiao, H., Wang, W., Xue, X., Shao, F., & Li, N. (2011) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2011.07.008 · Cited by 84 · see citing works
Chronic social isolation reduces 5-HT neuronal activity via upregulated SK3 calcium-activated potassium channels
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Social isolation in rats: effects on animal welfare and molecular markers for neuroplasticity
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Social Isolation Induces Rac1-Dependent Forgetting of Social Memory
Liu, Y., Lv, L., Wang, L., & Zhong, Y. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.09.033 · Cited by 75 · see citing works
Social isolation stress in adolescence, but not adulthood, produces hypersocial behavior in adult male and female C57BL/6J mice
Rivera-Irizarry, J. K., Skelly, M. J., & Pleil, K. E. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.00129 · Cited by 72 · see citing works
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Authors: Lukkes, J. L.
Affiliations: University of Colorado Boulder (US)
Corresponding author: Lukkes, Jodi L.
ORCID: Lukkes, Jodi L.
Venue: Frontiers in Behavioral Neuroscience
Publisher: Frontiers Media SA
Published: 2009
Volume: 3
Pages: 18-18
ISSN: 1662-5153 (ISSN-L)
DOI: 10.3389/neuro.08.018.2009
PMC: PMC2737489
OpenAlex: W2074801302
Cited by: 235
References: 138
Citations by year: 2026: 11 · 2025: 20 · 2024: 23 · 2023: 16 · 2022: 13 · 2021: 20 · 2020: 19 · 2019: 10 · 2018: 15 · 2017: 13 · 2016: 8 · 2015: 10 · 2014: 12 · 2013: 13 · 2012: 9
FWCI: 4.09
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders: National Science Foundation (CAREER)
National Alliance for Research on Schizophrenia and Depression
National Institutes of Health
National Institute on Drug Abuse (R01DA019921)
National Center for Research Resources (P20RR015567)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: post-weaning social isolation, childhood adversity, anxiety-like behavior, fear behavior, monoaminergic systems, serotonin, dopamine, corticotropin-releasing factor, neuroendocrine function, limbic system, late childhood, psychiatric vulnerability, rodent models

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Consequences of post-weaning social isolation on anxiety behavior and related neural circuits in rodents

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