Cited by 512Stress Responses and CortisolNeuroendocrine regulation and behaviorMemory and Neural Mechanisms

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Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat

Weiss, Isabelle C, Pryce, Christopher R, Jongen-Rêlo, Ana L, Nanz-Bahr, Nina I, Feldon, Joram·2004·Behavioural Brain Research

DOI 10.1016/j.bbr.2003.10.015

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Abstract

The present study investigated the effects of post-weaning social isolation (SI) on behavioural and neuroendocrine reactivity to stress of male and female rats. Innate aspects of fear and anxiety were assessed in the open field and elevated plus maze tests. Spontaneous startle reflex and conditioned fear response were further investigated. The neuroendocrine response of isolates was examined by measuring basal and stress release of ACTH and corticosterone and by evaluating the mRNA expression of mineralocorticoid (MR) and glucocorticoid (GR) receptors using in situ hybridization. Locomotor activity in the open field was not modified by chronic SI. In males, but not females, SI produced an anxiogenic profile in the elevated plus maze. Male isolates showed a trend towards increased startle reflex amplitude relative to socially-reared controls. Moreover, SI in males produced alterations of the HPA axis functioning as reflected by higher basal levels of ACTH, and enhanced release of ACTH and corticosterone following stress. In contrast, startle response or HPA axis functioning were not altered in female isolates. Social isolates from both genders showed reduced contextual fear-conditioning. Finally, the mRNA expression of MR and GR was not modified by SI. The results of the present study suggest that chronic SI increases emotional reactivity to stress and produces a hyperfunction of the HPA axis in adult rats, particularly in males.

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“Socially deprived mice exhibit changes in immune-endocrine responses displaying a hyper-reactivity to novel situations [37] or stressful stimuli [38].”
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Girella, A., Bartolomeo, M. D., Dainese, E., Buzzelli, V., Trezza, V., & D’Addario, C. (2024) · Neurochemical Research · doi:10.1007/s11064-024-04117-9 · Cited by 6
“How these changes in gene expression might be affected by life stressors, such as SI, is today poorly understood [13, 20, 21].”
From market baskets to mole rats
McCloskey, D. P., Kress, M., Imberman, S. P., Кушнір, І. М., & Briffa-Mirabella, S. (2011) · ACM SIGKDD Conference on Knowledge Discovery and Data Mining (KDD) · doi:10.1145/2020408.2020459 · Cited by 7
“However these behavior detection systems have the limitation that animals are housed individually, which can be stressful for most rodents [26].”
Background
Sex differences and the role of acute stress in the open-field tower maze
Lipatova, O., Campolattaro, M. M., Dixon, D. C., & Durak, A. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.02.046 · Cited by 7
Sumatriptan attenuates fear-learning despair induced by social isolation stress in mice: Mediating role of hypothalamic-pituitary-adrenal axis
Moradi, K., Badripour, A., Moradi, A., Bagheri, S., Soltani, Z. E., Moassefi, M., Faghani, S., & Dehpour, A. R. (2024) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2024.107006 · Cited by 6
Postpartum repeated separation from pups affects the behavior and neuroendocrine parameters of mandarin vole fathers
Kong, L., Wu, R., Wang, L., Feng, W., Cao, Y., & Tai, F. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.11.017 · Cited by 6
“Additionally, isolationreared rats showed dysregulation of the HPA axis activation responding to stress and exhibited anxiety-like behaviors [67], and increased serum cortisol levels are implicated in anxiety and depression [68].”
Background
Social isolation as a laboratory model of depression
Ünal, G. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-824289-6.00005-2 · Cited by 6
Sleep-Wake Rhythm and Oscillatory Pattern Analysis in a Multiple Hit Schizophrenia Rat Model (Wisket)
Adlan, L. G., Csordás-Nagy, M., Bodosi, B., Kalmár, G., Nyúl, L. G., Nagy, A., Kékesi, G., Büki, A., & Horváth, G. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.799271 · Cited by 7
Impact of tobacco smoke constituents on nicotine-seeking behavior in adolescent and adult male rats
Gellner, C. A., Carreño, D., Belluzzi, J. D., & Leslie, F. M. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1096213 · Cited by 6
“Studies have shown individually housed rats display an anxiogenic phenotype (42, 43) and show increased sensitivity to reward-related cues (41, 44).”
Background
Investigating the Robustness of a Rodent “Double Hit” (Post-Weaning Social Isolation and NMDA Receptor Antagonist) Model as an Animal Model for Schizophrenia: A Systematic Review
Shangase, K. B., Luvuno, M., & Mabandla, M. V. (2023) · Brain Sciences · doi:10.3390/brainsci13060848 · Cited by 6
Adversity in early adolescence promotes an enduring anxious phenotype and increases serotonergic innervation of the infralimbic medial prefrontal cortex
Tao, C. S., Dhamija, P., Booij, L., & Menard, J. L. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.09.004 · Cited by 7
For neuroscience, social history matters
George, A., Padilla-Coreano, N., & Opendak, M. M. (2023) · Neuropsychopharmacology · doi:10.1038/s41386-023-01566-8 · Cited by 5
Wheel access has opposing effects on stress physiology depending on social environment in female prairie voles (Microtus ochrogaster)
Jarcho, M. R., McNeal, N., Colburn, W., Normann, M. C., Watanasriyakul, W. T., & Grippo, A. J. (2019) · Stress · doi:10.1080/10253890.2018.1553948 · Cited by 6
Epigenética, Cuidados Maternais e Vulnerabilidade ao Estresse: Conceitos Básicos e Aplicabilidade
Noro, G., & Gon, M. C. C. (2015) · Psicologia Reflexão e Crítica · doi:10.1590/1678-7153.201528422 · Cited by 5
Chronic early-life social isolation enhances spatial memory in male and female rats
Davari, S., D’Costa, N., Ramezan, R., & Mielke, J. G. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114433 · Cited by 5
Shifts in naturalistic behaviors induced by early social isolation stress are associated with adult binge-like eating in female rats
Simon, T. B., Sierra, J., Williams, A., Wright, G., Rhee, A., Horn, J., Lou, J., Sharafeddin, F., Ontiveros‐Ángel, P., & Figueroa, J. D. (2024) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2024.1519558 · Cited by 4
Pubertal stress decreases sexual motivation and supresses the relation between cerebral theta rhythms and testosterone levels in adult male rats
Hernández‐Arteaga, E., González, M. H., Bonilla‐Jaime, H., Guevara, M. Á., & Ågmo, A. (2020) · Brain Research · doi:10.1016/j.brainres.2020.146937 · Cited by 6
Group management of young dairy cattle in relation to animal behaviour and welfare
Raussi, S. (2005) · Organic Eprints (International Centre for Research in Organic Food Systems, and Research Institute of Organic Agriculture) · Cited by 5
Establishment of an Animal Model of Depression: The Serotonin Transporter Knockout Rat
Kidwell, M. (2019) · doi:10.26686/wgtn.17135999.v1 · Cited by 5
The Influence of Social Isolation and Enriched Environment on Fear Conditioning in Rats after Early Proinflammatory Stress
Pavlova, I. V., & Broshevitskaya, N. D. (2021) · Journal of Evolutionary Biochemistry and Physiology · doi:10.1134/s0022093021040062 · Cited by 4
The interaction between Environmental Enrichment and fluoxetine in inhibiting sucrose-seeking renewal in mice depend on social living condition
Pintori, N., Piva, A., Guardiani, V., Marzo, C., Decimo, I., & Chiamulera, C. (2022) · Psychopharmacology · doi:10.1007/s00213-022-06124-6 · Cited by 4
Neural Basis of Anhedonia Associated with Stress-Induced Eating Disorders
Jahng, J. W. (2014) · Springer eBooks · doi:10.1007/978-94-017-8591-4_13 · Cited by 4
Developmental Programming via Activation of the Hypothalamic–Pituitary–Adrenal Axis: A New Role for Acoustic Stimuli in Shaping Behavior?
Spencer, K. A., & Minderman, J. (2018) · Advances in the study of behavior · doi:10.1016/bs.asb.2017.11.003 · Cited by 4
Early unhealthy eating habits underlie morpho-functional changes in the liver and adipose tissue in male rats
Nogueira, S., Garcez, F., Sá, S., Moutinho, L. C., Cardoso, A., Soares, R. A., Fonseca, B. M., & Leal, S. M. (2022) · Histochemistry and Cell Biology · doi:10.1007/s00418-022-02092-2 · Cited by 4
Type 1 Corticotropin-Releasing Factor Receptor Differentially Modulates Neurotransmitter Levels in the Nucleus Accumbens of Juvenile versus Adult Rats
Zegers-Delgado, J., Aguilera-Soza, A., Calderon, F., Davidson, H., Verbel‐Vergara, D., Yarur, H. E., Novoa, J., Blanlot, C., Bastias, C. P., Andrés, M. E., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231810800 · Cited by 3
An evaluation of the rat intestinal monoamine biogeography days following exposure to acute stress
Bauer, E. E., Reed, C. H., Lyte, M., & Clark, P. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.1021985 · Cited by 3
“Rats were group housed to minimize the possible influence of chronic social isolation stress (Weiss et al., 2004) that could interact with the single episode of acute stress (described below), employed in this study, to confound the dependent measures.”
Method
Mate Discrimination Using Chemical Cues by Male Guppies
Saoshiro, S., & Karino, K. (2023) · ZOOLOGICAL SCIENCE · doi:10.2108/zs220103 · Cited by 3
“It is known that among some animals, social isolation can serve as a stressor that may adversely affect the physiological systems and behavior of individuals (Alexander et al., 1988; Weiss et al., 2004; Grippo et al., 2007).”
Background
Transcriptomic analysis of rat prefrontal cortex following chronic stress induced by social isolation – Relevance to psychiatric and neurodevelopmental illness, and implications for treatment
Goh, J.-Y., Rueda, P., Taylor, J., Rathbone, A., Scott, D., LANGMEAD, C. J., Fone, K. C. F., Stewart, G. D., & King, M. V. (2024) · Neurobiology of Stress · doi:10.1016/j.ynstr.2024.100679 · Cited by 4
“Cognitive deficits in isolated rats encompass fear conditioning (e.g. Weiss et al., 2004; Mora-Gallegos and Fornaguera, 2019), reversal learning (e.g. Jones et al., 1991; Schrijver et al., 2004; Powell et al., 2015) and attentional set shifting (Schrijver and Würbel, 2001; McLean et al., 2010),…”
Effects of Early Stress Exposure on Anxiety-like Behavior and MORC1 Expression in Rats
Mundorf, A., & Freund, N. (2024) · Biomolecules · doi:10.3390/biom14121587 · Cited by 3
The effect of voluntary wheel running on the antioxidant status is dependent on sociability conditions
Cunha, M. P., Machado, D. G., Mancini, G., Glaser, V., Martins, R. D. P., Bem, A. F. D., Latini, A., Dafré, A. L., & Rodrigues, A. L. S. (2020) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2020.173018 · Cited by 3
“In line with this, studies indicate that SIS in rodents is a stressful paradigm, since it produces a negative impact on behavior and endocrine responses, such as increased corticosterone, adrenocorticotropic hormone (ACTH), and catecholamine serum levels (Grippo et al., 2007a, 2007b, 2007c; Weiss et al., 2004).”
Periadolescent Social Isolation Effects on Extinction of Conditioned Fear
Drummond, K. D., & Kim, J. H. (2023) · Neuromethods · doi:10.1007/978-1-0716-3218-5_2 · Cited by 3
Varied impacts of social relationships on neuroendocrine state
Prior, N. H., Haakenson, C. M., Clough, S., Ball, G. F., & Sandkam, B. A. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105403 · Cited by 3
Effects of short-term isolation on social behaviors in prairie voles
Madrid, J. E., Pranic, N. M., Chu, S., Bergstrom, J. J. D., Singh, R., Rabinovich, J., Lopez, K. A., Ophir, A. G., & Tschida, K. (2024) · PLoS ONE · doi:10.1371/journal.pone.0313172 · Cited by 4
Assessment of impulsivity using an automated, self-adjusting delay discounting procedure
Carr, M. R., van Mourik, Y., Gómez-Sotres, P., Solinas, M., Vries, T. J. D., & Pattij, T. (2024) · Behavioural Brain Research · doi:10.1016/j.bbr.2024.115405 · Cited by 3
Toward a diagnostic framework for the equine depressive phenotype: A narrative review
Brien, C. O., Parker, M. O., & McBride, S. D. (2025) · Journal of Veterinary Behavior · doi:10.1016/j.jveb.2025.04.004 · Cited by 3
A laboratory exercise for a college-level, introductory neuroscience course demonstrating effects of housing environment on anxiety and psychostimulant sensitivity.
Pritchard, L. M., Kempen, T. A. V., Williams, H., & Zimmerberg, B. (2008) · Europe PMC (PubMed Central) · Cited by 3
The impact of social isolation on rat behaviour
Porkess, V. (2008) · Nottingham ePrints (University of Nottingham) · Cited by 3
Sex differences in chronic social stress models in micePreprint
Furman, O., Tsoory, M., & Chen, A. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/605527 · Cited by 3
“…using a highly familiar same-sex partner throughout the experiment, as previous research has shown that social isolation is a potent stressor (Weiss et al. 2004; Hatch et al. 1963), group housing increases trait variability (Prendergast, Onishi, and Zucker 2014), and social instability is a…”
Method
Effects of Social Isolation Throughout the Lifespan on Behaviors and Related Neuroendocrine Functions in Rodents
Kin, K., Gaini, R., & Niwa, M. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-819641-0.00090-6 · Cited by 3

Authors: Weiss, I. C., Pryce, C. R., Jongen-Rêlo, A. L., Nanz-Bahr, N. I., & Feldon, J.
Affiliations: ETH Zurich (CH)
Corresponding author: Feldon, Joram
ORCID: Pryce, Christopher R
Venue: Behavioural Brain Research
Publisher: Elsevier BV
Published: 2004-07
Volume: 152
Issue: 2
Pages: 279-295
ISSN: 0166-4328 (ISSN-L)
DOI: 10.1016/j.bbr.2003.10.015
OpenAlex: W2076236287
Cited by: 512
References: 76
Citations by year: 2026: 7 · 2025: 20 · 2024: 26 · 2023: 18 · 2022: 29 · 2021: 33 · 2020: 46 · 2019: 25 · 2018: 19 · 2017: 30 · 2016: 22 · 2015: 25 · 2014: 25 · 2013: 24 · 2012: 26
FWCI: 3.26
Type: journal article
Language: en
Open access: closed
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Behavioural Brain Research (publishedVersion)
PubMed (publishedVersion)
Funders: Branco Weiss Fellowship – Society in Science
Eidgenössische Technische Hochschule Zürich
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: social isolation, post-weaning social isolation, stress reactivity, hypothalamic-pituitary-adrenal axis, ACTH, corticosterone, mineralocorticoid receptor, glucocorticoid receptor, anxiety, fear conditioning, startle response, sex differences, neuroendocrine response, rats
MeSH terms: Adrenocorticotropic Hormone, Analysis of Variance, Animals, Animals, Newborn, Behavior, Animal, Brain, Conditioning, Psychological, Corticosterone, Fear, Female, Glucocorticoids, Immunohistochemistry, Kidney, Male, Motor Activity, Neurosecretory Systems, Radioimmunoassay, Random Allocation, Reflex, Acoustic, Sex Factors, Social Isolation, Stress, Physiological, Weaning, Rats, Sprague-Dawley, In Situ Hybridization, Receptors, Mineralocorticoid, Maze Learning, Rats

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Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat

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