Stress and the reproductive axis

Toufexis, D.; Rivarola, M. A.; Lara, H.; Viau, V.

doi:10.1111/jne.12179

Cited by 350Stress Responses and CortisolHypothalamic control of reproductive hormonesNeuroendocrine regulation and behavior

Stress and the reproductive axis

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Toufexis, D., Rivarola, M. A., Lara, H., Viau, V.·2014·Journal of Neuroendocrinology

DOI 10.1111/jne.12179PMC PMC4166402

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Abstract

There exists a reciprocal relationship between the hypothalamic-pituitary-adrenal (HPA) and the hypothalamic-pituitary-gonadal (HPG) axes, wherein the activation of one affects the function of the other and vice versa. For example, both testosterone and oestrogen modulate the response of the HPA axis, whereas activation of the stress axis, especially activation that is repeating or chronic, has an inhibitory effect upon oestrogen and testosterone secretion. Alterations in maternal care can produce significant effects on both HPG and HPA physiology, as well as behaviour in the offspring at adulthood. For example, changes in reproductive behaviour induced by altered maternal care may alter the expression of sex hormone receptors such as oestrogen receptor (ER)α that govern sexual behaviour, and may be particularly important in determining the sexual strategies utilised by females. Stress in adulthood continues to mediate HPG activity in females through activation of a sympathetic neural pathway originating in the hypothalamus and releasing norepinephrine into the ovary, which produces a noncyclic anovulatory ovary that develops cysts. In the opposite direction, sex differences and sex steroid hormones regulate the HPA axis. For example, although serotonin (5-HT) has a stimulatory effect on the HPA axis in humans and rodents that is mediated by the 5-HT1A receptor, only male rodents respond to 5-HT1A antagonism to show increased corticosterone responses to stress. Furthermore, oestrogen appears to decrease 5-HT1A receptor function at presynaptic sites, yet increases 5-HT1A receptor expression at postsynaptic sites. These mechanisms could explain the heightened stress HPA axis responses in females compared to males. Studies on female rhesus macaques show that chronic stress in socially subordinate female monkeys produces a distinct behavioural phenotype that is largely unaffected by oestrogen, a hyporesponsive HPA axis that is hypersensitive to the modulating effects of oestrogen, and changes in 5-HT1A receptor binding in the hippocampus and hypothalamus of social subordinate female monkeys that are restored or inverted by oestrogen replacement. This review summarises all of these studies, emphasising the profound effect that the interaction of the reproductive and stress axes may have on human reproductive health and emotional wellbeing.

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A relationship exists between the hypothalamic-pituitary-adrenal (HPA) and hypothalamic-pituitary-gonadal (HPG) axes, and both testosterone and oestrogen modulate the response of the HPA axis.
“As a relationship exists between the hypothala mic-pituitary-adrenal (HPA) and the hypothalamic-pituitary-go nadal (HPG) axes, and both testosterone and oestrogen modulate the response of the HPA axis (Toufexis et al., 2014)”
From Effect of weather conditions and presence of visitors on adrenocortical activity in captive African penguins (Spheniscus demersus) (2017) · cites this paper as Toufexis et al., 2014
Edges were verified independently using the authors' implementation of a Bayesian sentiment analysis classifier; disagreements between MedScan and this platform were reviewed and adjudicated by the authors.
“Edges were verified independently using our implementation of a Bayesian sentiment analysis classifier35. Disagreements between MedScan and this platform were reviewed and adjudicated by the authors.”
From Leveraging Prior Knowledge of Endocrine Immune Regulation in the Therapeutically-relevant Phenotyping of Women with Chronic Fatigue Syndrome (2019) · cites this paper as [35]
The provided sections on serotonin, stress, and reproductive physiology do not address a Bayesian sentiment-analysis classifier, MedScan, edge verification, or adjudication. Searches of our full-text copy for those methods likewise found no relevant passage. The source therefore does not verify the attributed methods claim. (LLM, conf=0.76)
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[121]Tung J Barreiro LB Johnson ZP Hansen KD Michopoulos V Toufexis D Michelini K Wilson ME Yoav G Social environment is associated with gene regulatory variation in rhesus macaque immune system Proceedings of the National Academy of Sciences 2012 in press PMC3340061 22493251
[145]Moore CJ Lowe J Michopoulos V Ulam P Toufexis D Wilson ME Johnson Z Small changes in meal patterns lead to significant changes in total caloric intake. Effects of diet and social status on food intake in female rhesus monkeys Appetite 2013 6260 6269 PMC4920003 23207191
[156]Michopoulos V Checchi M Sharpe D Wilson ME Estradiol effects on behavior and serum oxytocin are modified by social status and polymorphisms in the serotonin transporter gene in female rhesus monkeys Hormones and behavior 2011 59 4 528 535 21316367 PMC3081406
[171]Fiedler J Cold stress induces metabolic activation of thyrotrophin-releasing hormone-synthesising neurones in the magnocellular division of the hypothalamic paraventricular nucleus and concomitantly changes ovarian sympathetic activity parameters J Neuroendocrinol 2006 18 5 367 376 16629836

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Authors: Toufexis, D., Rivarola, M. A., Lara, H., & Viau, V.
Affiliations: University of Vermont (US)
Consejo Nacional de Investigaciones Científicas y Técnicas (AR)
University of Chile (CL)
University of British Columbia (CA)
Corresponding author: Toufexis, D.
ORCID: Toufexis, D.
Lara, H.
Viau, V.
Venue: Journal of Neuroendocrinology
Publisher: Wiley
Published: 2014-08-24
Volume: 26
Issue: 9
Pages: 573-586
ISSN: 0953-8194 (ISSN-L)
1365-2826
DOI: 10.1111/jne.12179
PMC: PMC4166402
OpenAlex: W2085026395
Cited by: 350
References: 168
Citations by year: 2026: 31 · 2025: 19 · 2024: 38 · 2023: 50 · 2022: 34 · 2021: 40 · 2020: 17 · 2019: 26 · 2018: 28 · 2017: 26 · 2016: 24 · 2015: 15 · 2014: 2
FWCI: 1.82
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Journal of Neuroendocrinology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Universidad de Chile (submittedVersion, cc-by-nc-nd)
Conicet (submittedVersion, cc-by-nc-sa)
Funders: Fondecyt (1130049)
CONICET
SECyT-UNC
NIH (HD 046501, MH081816, F31MH085445, RR00165)
Canadian Institutes of Health Research CIHR (MOP-42555)
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Keywords: stress, hypothalamic-pituitary-gonadal axis, hypothalamic-pituitary-adrenal axis, maternal care, estrogen receptor alpha, sexual behavior, anovulation, norepinephrine, 5-HT1A receptor, sex differences, estrogen, chronic stress, social dominance, rhesus monkeys, corticosterone, reproductive health, emotional well-being
MeSH terms: Animals, Brain, Humans, Hypothalamo-Hypophyseal System, Models, Biological, Pituitary-Adrenal System, Reproduction, Serotonin, Sex Characteristics, Social Dominance, Stress, Psychological, Sympathetic Nervous System

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