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Trends of Reproductive Hormones in Male Rats During Psychosocial Stress: Role of Glucocorticoid Metabolism in Behavioral Dominance1
Abstract
Stress in socially subordinate male rats, associated with aggressive attacks by dominant males, was studied in a group-housing context called the visible burrow system (VBS). It has been established that subordinate males have reduced serum testosterone (T) and higher corticosterone (CORT) relative to dominant and singly housed control males. The relationship of the decreased circulating T levels in subordinate males to changes in serum LH concentrations has not been evaluated previously. Since decreases in LH during stress may cause reductions in Leydig cell steroidogenic activity, the present study defined the temporal profiles of serum LH, T, and CORT in dominant and subordinate males on Days 4, 7, and 14 of a 14-day housing period in the VBS. The same parameters were followed in serum samples from single-housed control males. Leydig cells express glucocorticoid receptors and may also be targeted for direct inhibition of steroidogenesis by glucocorticoid. We hypothesize that Leydig cells are protected from inhibition by CORT at basal concentrations through oxidative inactivation of glucocorticoid by 11beta-hydroxysteroid dehydrogenase (11betaHSD). However, Leydig cell steroidogenesis is inhibited when 11betaHSD metabolizing capacity is exceeded. Therefore, 11betaHSD enzyme activity levels were measured in Leydig cells of VBS-housed males at the same time points. Significant increases in LH and T relative to control were observed in the dominant animals on Day 4, which were associated with the overt establishment of behavioral dominance as evidenced by victorious agonistic encounters. Serum LH and T were lower in subordinate males on Day 7, but T alone was lower on Day 14, suggesting that lowered LH secretion in subordinates may gradually be reversed by declines in androgen-negative feedback. Serum CORT levels were higher in subordinate males compared to control at all three time points. In contrast, oxidative 11betaHSD activity in Leydig cells of dominant males was higher relative to control and unchanged in subordinates. These results suggest the following: 1) failure of Leydig cells of subordinate males to compensate for increased glucocorticoid action during stress, by increasing 11betaHSD oxidative activity, potentiates stress-mediated reductions in T secretion; and 2) an inhibition of the reproductive axis in subordinate males at the level of the pituitary.
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“When LE rats form a dominance hierarchy within a laboratory enclosure, it has been shown that subordinate rats have elevated levels of CORT compared to dominants and can be prone to illness and weight loss due to chronic stress (Blanchard et al., 1995, Hardy et al., 2002).”
From Early life adversity during the infant sensitive period for attachment: Programming of behavioral neurobiology of threat processing and social behavior (2017) · cites this paper as Hardy et al., 2002
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Metadata
- Authors
- Hardy, M. P., Sottas, C. M., Ge, R., McKittrick, C. R., Tamashiro, K. L., McEwen, B. S., Haider, S. G., Markham, C. M., Blanchard, R. J., Blanchard, D. C., & Sakai, R. R.
- Affiliations
- Population Council (US)
- Rockefeller University (US)
- University of Cincinnati (US)
- Heinrich Heine University Düsseldorf (DE)
- University of Hawaiʻi at Mānoa (US)
- Corresponding author
- Hardy, Matthew P.
- ORCID
- Venue
- Biology of Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2002-12-01
- Volume
- 67
- Issue
- 6
- Pages
- 1750-1755
- ISSN
- 0006-3363 (ISSN-L)
- 1529-7268
- OpenAlex
- W2156146487
- Cited by
- 122
- References
- 34
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 2 · 2023: 1 · 2022: 4 · 2021: 3 · 2020: 4 · 2019: 4 · 2018: 4 · 2017: 8 · 2016: 4 · 2015: 9 · 2014: 6 · 2013: 5 · 2012: 17
- FWCI
- 1.65
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biology of Reproduction (publishedVersion)
- PubMed (publishedVersion)
- BioOne Complete (BioOne) (submittedVersion)
- Funders
- National Science Foundation (9815480, 9815481, 9728543)
- Harry Frank Guggenheim Foundation
- John Simon Guggenheim Memorial Foundation
- National Alliance for Research on Schizophrenia and Depression
- National Institutes of Health
- U.S. Public Health Service (33000)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
- Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
- Keywords
- psychosocial stress, social dominance, testosterone, luteinizing hormone, corticosterone, Leydig cells, 11β-hydroxysteroid dehydrogenase, glucocorticoid metabolism, Leydig cell steroidogenesis, male rats, aggression, reproductive axis
- MeSH terms
- Animals, Behavior, Animal, Corticosterone, Glucocorticoids, Hydroxysteroid Dehydrogenases, Immunohistochemistry, Leydig Cells, Luteinizing Hormone, Male, Pituitary Gland, Reproduction, Social Dominance, Stress, Psychological, Testosterone, Rats, Long-Evans, 11-beta-Hydroxysteroid Dehydrogenases, Rats
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