Sex, stress and steroids

Sze, Ying; Brunton, Paula J.

doi:10.1111/ejn.14615

Cited by 85Stress Responses and CortisolAdrenal Hormones and DisordersNeuroendocrine regulation and behavior

Sex, stress and steroids

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Sze, Ying, Brunton, Paula J.·2020·European Journal of Neuroscience

DOI 10.1111/ejn.14615

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Abstract

The hypothalamo–pituitary–adrenal (HPA) axis plays a key role in the neuroendocrine response to stress and in maintaining physiological homoeostasis. However, stress that is chronic in nature can lead to HPA axis dysfunction and increase the risk for developing affective disorders, particularly if the stress is experienced during vulnerable periods in life. Sex differences in how the HPA axis responds to stress are well established, with females typically displaying heightened responses. The underlying cause of these sex differences is important to understand, as many neuropsychiatric disorders disproportionately affect females. Much research has provided evidence for gonadal sex steroids in underpinning sex differences in HPA axis responsivity; however, we suggest that neuroactive metabolites of these steroids also play a key role in the brain in mediating sex differences in HPA axis responses to stress. The relationship between neuroactive steroids and stress is complex. Acute stress rapidly increases neuroactive steroid production, which can in turn modulate activity of the HPA axis. However, under chronic stress conditions, stress can impact the brain's capacity to generate steroids, and this in turn has corollary effects on HPA axis function that may increase the propensity for psychopathology, given both HPA axis dysfunction and deficits in neuroactive steroids are implicated in affective disorders. Hence, here we review the evidence from animal and human studies for sex differences in the interactions between neuroactive steroids and the stress axis at various stages of life, under physiological and pathophysiological stress conditions and consider the implications for health and disease.

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Paternal Transmission of Stress-Induced Pathologies
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“Notably, neuroactive steroids such as the progesterone metabolite, allopregnanolone and the corticosterone metabolite, tetrahydrodeoxycorticosterone (THDOC), concentrations of which both increase considerably following acute stress, positively modulate GABAA receptors via an allosteric binding site to potentiate inhib…”
Background
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Steroid hormone metabolites potentiate GABA receptor-mediated chloride ion flux with nanomolar potency
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“The mechanisms involved are not clear, but GABAA receptors are likely targets for allopregnanolone and THDOC actions, given their affinity for these receptors and their potent stress-suppressing and anxiolytic actions through potentiating GABA signalling (Patchev et al., 1996, 1994).”
Background
Effects of housing on male and female rats: Crowding stresses males but calms females
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“Puberty is accompanied by dynamic changes in circulating adrenal and gonadal steroids in males and females, which contribute to the organisation and maturation of the HPA axis (Viau et al., 2005).”
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Brain 5α-dihydroprogesterone and allopregnanolone synthesis in a mouse model of protracted social isolation
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Region-specific reduction in stress-induced c- fos mRNA expression during pregnancy and lactation
Costa, A. P. C., Wood, S. A., Ingram, C. D., & Lightman, S. L. (1996) · Brain Research · doi:10.1016/s0006-8993(96)00962-6 · Cited by 135 · see citing works
Sex differences in activated corticotropin-releasing factor neurons within stress-related neurocircuitry and hypothalamic–pituitary–adrenocortical axis hormones following restraint in rats
Babb, J. A., Masini, C. V., Day, H. E. W., & Campeau, S. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.12.051 · Cited by 134 · see citing works
Dysregulated Hypothalamic–Pituitary–Adrenal Axis Function Contributes to Altered Endocrine and Neurobehavioral Responses to Acute Stress
Kinlein, S. A., Wilson, C. D., & Karatsoreos, I. N. (2015) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2015.00031 · Cited by 134 · see citing works
Neuroendocrine Responses to Stress in Mice: Hyporesponsiveness in Pregnancy and Parturition
Douglas, A. J., Brunton, P. J., Bosch, O. J., Russell, J. A., & Neumann, I. D. (2003) · Endocrinology · doi:10.1210/en.2003-0461 · Cited by 134 · see citing works
Self-citation
Endocrine induced changes in brain function during pregnancy
Brunton, P. J., & Russell, J. A. (2010) · Brain Research · doi:10.1016/j.brainres.2010.09.062 · Cited by 134 · see citing works
Self-citation
Chapter 18 Lactogenic hormone regulation of maternal behavior
Mann, P. E., & Bridges, R. S. (2001) · Progress in Brain Research · doi:10.1016/s0079-6123(01)33019-4 · Cited by 133 · see citing works
Comparison of plasma and cerebrospinal fluid levels of neuroactive steroids with their brain, spinal cord and peripheral nerve levels in male and female rats
Caruso, D., Pesaresi, M., Abbiati, F., Calabrese, D., Giatti, S., García‐Segura, L. M., & Melcangi, R. C. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.04.016 · Cited by 133 · see citing works
Steroid withdrawal in the mouse results in anxiogenic effects of 3α,5β-THP: a possible model of premenstrual dysphoric disorder
Smith, S. S., Ruderman, Y., Frye, C. A., Homanics, G. E., & Yuan, M. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0168-3 · Cited by 130 · see citing works
The Effects of Estrogen and Progesterone on Corticotropin-Releasing Hormone and Arginine Vasopressin Messenger Ribonucleic Acid Levels in the Paraventricular Nucleus and Supraoptic Nucleus of the Rhesus Monkey
Roy, B. N., Reid, R. L., & Vugt, D. A. V. (1999) · Endocrinology · doi:10.1210/endo.140.5.6684 · Cited by 128 · see citing works
Anxiety and increased 5-HT1A receptor response in NCAM null mutant mice
Stork, O., Welzl, H., Wotjak, C. T., Hoyer, D., Delling, M., Cremer, H., & Schachner, M. (1999) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(19990905)40:3 · Cited by 127 · see citing works
Steroid Profiling in Brain and Plasma of Male and Pseudopregnant Female Rats after Traumatic Brain Injury: Analysis by Gas Chromatography/Mass Spectrometry
Meffre, D., Pianos, A., Lière, P., Eychenne, B., Cambourg, A., Schumacher, M., Stein, D. G., & Guennoun, R. (2007) · Endocrinology · doi:10.1210/en.2006-1678 · Cited by 126 · see citing works
Central opioid inhibition of neuroendocrine stress responses in pregnancy in the rat is induced by the neurosteroid allopregnanolone
Brunton, P. J., McKay, A. J., Ochędalski, T., Piastowska, A., Rębas, E., Lachowicz, A., & Russell, J. A. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0708-09.2009 · Cited by 126 · see citing works
Self-citation
Estrogen Receptor-β Agonist Diarylpropionitrile: Biological Activities of R- and S-Enantiomers on Behavior and Hormonal Response to Stress
Weiser, M. J., Wu, T. J., & Handa, R. J. (2009) · Endocrinology · doi:10.1210/en.2008-1355 · Cited by 124 · see citing works
Stress-induced sensitization: the hypothalamic–pituitary–adrenal axis and beyond
Belda, X., Fuentes, S., Daviu, N., Nadal, R., & Armario, A. (2015) · Stress · doi:10.3109/10253890.2015.1067678 · Cited by 123 · see citing works
Allopregnanolone in the brain: Protecting pregnancy and birth outcomes
Brunton, P. J., Russell, J. A., & Hirst, J. J. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2013.08.005 · Cited by 122 · see citing works
Self-citation
Beyond the HPA Axis: Progesterone-Derived Neuroactive Steroids in Human Stress and Emotion
Wirth, M. M. (2011) · Frontiers in Endocrinology · doi:10.3389/fendo.2011.00019 · Cited by 121 · see citing works
Endogenous Opioids and Attenuated Hypothalamic-Pituitary-Adrenal Axis Responses to Immune Challenge in Pregnant Rats
Brunton, P. J., Meddle, S., Ma, S., Ochędalski, T., Douglas, A. J., & Russell, J. A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0866-05.2005 · Cited by 120 · see citing works
Self-citation
Neonatal treatment of rats with the neuroactive steroid tetrahydrodeoxycorticosterone (THDOC) abolishes the behavioral and neuroendocrine consequences of adverse early life events.
Patchev, V., Montkowski, A., Rouskova, D., Korányi, L., Holsboer, F., & Almeida, O. F. X. (1997) · Journal of Clinical Investigation · doi:10.1172/jci119261 · Cited by 120 · see citing works
Top‐down and bottom‐up control of stress‐coping
de Kloet, E. R., de Kloet, S. F., de Kloet, C. S., & de Kloet, A. D. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12675 · Cited by 120 · see citing works
Estradiol or diarylpropionitrile decrease anxiety-like behavior of wildtype, but not estrogen receptor beta knockout, mice
Walf, A., Koonce, C. J., & Frye, C. (2008) · Behavioral Neuroscience · doi:10.1037/a0012749 · Cited by 118 · see citing works
Anxiety-like behaviour and associated neurochemical and endocrinological alterations in male pups exposed to prenatal stress
Laloux, C., Mairesse, J., Camp, G. V., Giovine, A., Branchi, I., Bouret, S. G., Morley‐Fletcher, S., Bergonzelli, G. E., Malagodi, M., Gradini, R., et al. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.02.010 · Cited by 117 · see citing works
Rapid Induction of Corticotropin-Releasing Hormone Gene Transcription in the Paraventricular Nucleus of the Developing Rat1
Dent, G. W., Smith, M. A., & Levine, S. D. (2000) · Endocrinology · doi:10.1210/endo.141.5.7455 · Cited by 117 · see citing works
Sex differences in neuroactive steroid levels in the nervous system of diabetic and non-diabetic rats
Pesaresi, M., Maschi, O., Giatti, S., García‐Segura, L. M., Caruso, D., & Melcangi, R. C. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.04.008 · Cited by 114 · see citing works
Neuroactive Steroids and GABAergic Involvement in the Neuroendocrine Dysfunction Associated With Major Depressive Disorder and Postpartum Depression
Maguire, J. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00083 · Cited by 113 · see citing works
Sex-dependent changes in anxiety, memory, and monoamines following one week of stress
Bowman, R. E., Micik, R., Gautreaux, C., Fernandez, L., & Luine, V. N. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.01.012 · Cited by 111 · see citing works
Neurosteroid, GABAergic and hypothalamic pituitary adrenal (HPA) axis regulation: what is the current state of knowledge in humans?
Crowley, S. K., & Girdler, S. S. (2014) · Psychopharmacology · doi:10.1007/s00213-014-3572-8 · Cited by 111 · see citing works

Flagged first, then by citations

13 of the 332 references couldn’t be matched to a known paper.

Sorted by citations

Higher Circulating Cortisol in the Follicular vs. Luteal Phase of the Menstrual Cycle: A Meta-Analysis
Hamidovic, A., Karapetyan, K., Serdarevic, F., Choi, S. H., Eisenlohr-Moul, T., & Pinna, G. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00311 · Cited by 99 · see citing works
Neurosteroid allopregnanolone (3α,5α-THP) inhibits inflammatory signals induced by activated MyD88-dependent toll-like receptors
Balan, I. S., Aurelian, L., Schleicher, R. L., Boero, G., O’Buckley, T. K., & Morrow, A. L. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01266-1 · Cited by 76 · see citing works
A Review of Psychological Stress among Students and Its Assessment Using Salivary Biomarkers
Špiljak, B., Vilibić, M., Glavina, A., Crnković, M., Šešerko, A., & Lugović‐Mihić, L. (2022) · Behavioral Sciences · doi:10.3390/bs12100400 · Cited by 68 · see citing works
Anxiety and Depression: What Do We Know of Neuropeptides?
Kupcová, I., Danišovič, Ľ., Grgac, I., & Harsányi, Š. (2022) · Behavioral Sciences · doi:10.3390/bs12080262 · Cited by 57 · see citing works
“This goes in line with observed HPA axis dysfunction in patients with major depression or schizophrenia, where the continuous effect of CRH on the HPA axis causes disbalance (increased cortisol, increased ACTH, reduced feedback) and results in a pathology [92,93].”
Background
The maternal-placental-fetal interface: Adaptations of the HPA axis and immune mediators following maternal stress and prenatal alcohol exposure
Ruffaner‐Hanson, C. D., Noor, S., Sun, M. S., Solomon, E. R., Marquez, L. E., Rodriguez, D. E., Allan, A. M., Caldwell, K. K., Bakhireva, L. N., & Milligan, E. D. (2022) · Experimental Neurology · doi:10.1016/j.expneurol.2022.114121 · Cited by 52 · see citing works
“There is some evidence from preclinical studies that this downregulation occurs much more readily when the sex of the fetus is female (Duthie and Reynolds, 2013; Stroud et al., 2016; Howland et al., 2017; Sze and Brunton, 2020).”
Background
A review on how stress modulates fear conditioning: Let's not forget the role of sex and sex hormones
Peyrot, C., Brouillard, A., Morand‐Beaulieu, S., & Marin, M. (2020) · Behaviour Research and Therapy · doi:10.1016/j.brat.2020.103615 · Cited by 38 · see citing works
Maternal antioxidant treatment prevents the adverse effects of prenatal stress on the offspring's brain and behavior
Scott, H., Phillips, T. J., Sze, Y., Alfieri, A., Rogers, M. F., Volpato, V., Case, C. P., & Brunton, P. J. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100281 · Cited by 41 · see citing works
“Differences in sex steroids may render certain brain regions more vulnerable to prenatal stress in males versus females (Sze and Brunton, 2019), however, differences in gene expression or epigenetic profiles are also likely to play a role (McCarthy et al.”
BackgroundSelf-citation
Inflammation-related microRNAs are involved in stressful life events exposure and in trauma-focused psychotherapy in treatment-resistant depressed patients
Maffioletti, E., Bocchio‐Chiavetto, L., Perusi, G., Silva, R. C., Sacco, C., Bazzanella, R., Zampieri, E., Bortolomasi, M., Gennarelli, M., & Minelli, A. (2021) · European Journal of Psychotraumatology · doi:10.1080/20008198.2021.1987655 · Cited by 37 · see citing works
Selenium in Bodily Homeostasis: Hypothalamus, Hormones, and Highways of Communication
Toh, P., Nicholson, J. L., Vetter, A. M., Berry, M. J., & Torres, D. J. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232315445 · Cited by 42 · see citing works
Do corticosterone levels predict female depressive‐like behavior in rodents?
Kokras, N., Krokida, S., Varoudaki, T. Z., & Dalla, C. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24686 · Cited by 37 · see citing works
Modelling female physiology from head to Toe: impact of sex hormones, menstrual cycle, and pregnancy
Abo, S., Smith, D., Stadt, M., & Layton, A. (2022) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2022.111074 · Cited by 35 · see citing works
Gonads under stress: A systematic review and meta-analysis on the effects of acute psychosocial stress on gonadal steroids secretion in humans
Domes, G., Linnig, K., & von Dawans, B. (2024) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2024.107004 · Cited by 40 · see citing works
“Published reviews in content-related areas have focused on the modulation of HPA axis activity by gonadal steroids (Heck and Handa, 2019; Klusmann et al., 2023; Sze and Brunton, 2020; Toufexis et al., 2014; Zuloaga et al., 2020).”
Background
Hypothalamus-pituitary-adrenal axis imbalance and inflammation contribute to sex differences in separation- and restraint-induced depression
Dong, Y., Wang, X., Zhou, Y., Zheng, Q., Chen, Z., Zhang, H., Sun, Z., Xu, G., & Hu, G. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104741 · Cited by 31 · see citing works
Nutrition, anxiety and hormones. Why sex differences matter in the link between obesity and behavior.
Clark, T. D., Reichelt, A. C., Ghosh‐Swaby, O. R., Simpson, S. J., & Crean, A. J. (2022) · Physiology & Behavior · doi:10.1016/j.physbeh.2022.113713 · Cited by 27 · see citing works
Progesterone and Allopregnanolone Neuroprotective Effects in the Wobbler Mouse Model of Amyotrophic Lateral Sclerosis
Nicola, A. F. D., Meyer, M., Garay, L. I., Kruse, M. S., Schumacher, M., Guennoun, R., & Deniselle, M. C. G. (2021) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-021-01118-y · Cited by 25 · see citing works
The Role of the Stress Response in Metabolic Dysfunction-Associated Fatty Liver Disease: A Psychoneuroendocrineimmunology-Based Perspective
Demori, I., & Grasselli, E. (2023) · Nutrients · doi:10.3390/nu15030795 · Cited by 29 · see citing works
Impact of polyphenols on stress and anxiety: a systematic review of molecular mechanisms and clinical evidence
Meléndez, G. P. P., Valero-Jara, V., Acevedo-Hernández, P., & Thomas‐Valdés, S. (2022) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2022.2122925 · Cited by 25 · see citing works
“Sympathetic nervous system can modulate the stress response by synthesis of catecholamines, which can change physiological pathways and may regulate behavior (Sze and Brunton 2020).”
Background
Shared reproductive disruption, not neural crest or tameness, explains the domestication syndrome
Gleeson, B. T., & Wilson, L. A. B. (2023) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2022.2464 · Cited by 27 · see citing works
“Females typically experience more stress due to sex-hormone effects upon developing neuroendocrine systems [100,101] and maternal stress leads to poor reproductive outcomes, including: fewer offspring, lower birth weights, and poor health and survivorship of young [95–97].”
Background
Sex differences in CRF1, CRF, and CRFBP expression in C57BL/6J mouse brain across the lifespan and in response to acute stress
Locci, A., Yan, Y., Rodríguez, G., & Dong, H. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15157 · Cited by 21 · see citing works
“Our results added evidence supporting sex differences in stress sensitivity (Heck & Handa, 2019; Sze & Brunton, 2019).”
Result
Overexpression of angiotensin converting enzyme 2 reduces anxiety-like behavior in female mice.
de Kloet, A. D., Cahill, K. M., Scott, K. A., & Krause, E. G. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113002 · Cited by 20 · see citing works
“Relative to males, females exhibit a heightened HPA axis response to acute stressors (Sze and Brunton 2019).”
Background
Anxiolytic and antioxidant effects of Euterpe oleracea Mart. (açaí) seed extract in adult rat offspring submitted to periodic maternal separation
de Bem, G. F., Okinga, A., Ognibene, D. T., da Costa, C. A., Santos, I. B., Soares, R. D. A., Silva, D. L. B., da Rocha, A. P. M., Isnardo-Fernandes, J., Fraga, M. C., et al. (2020) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2020-0099 · Cited by 20 · see citing works
Neuroendocrine mechanisms in the links between early life stress, affect, and youth substance use: A conceptual model for the study of sex and gender differences
Donovan, A., Assari, S., Grella, C. E., Shaheen, M. A., Richter, L., & Friedman, T. C. (2024) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2024.101121 · Cited by 21 · see citing works
“The response is eventually terminated through a negative feedback mechanism dependent on GR and other receptors in the hypothalamus, hippocampus, and pituitary (Herman, 2022; Sze & Brunton, 2020).”
Background
Sex matters in neuroscience and neuropsychopharmacology
Pawluski, J. L., Kokras, N., Charlier, T. D., & Dalla, C. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14880 · Cited by 19 · see citing works
“Sex steroids such as neuroestrogens are not the only hormones to be produced centrally and the review of Sze and Brunton focuses on the role of neuroactive steroids in the stress response from early life, to puberty, and into adulthood (Sze & Brunton, 2019).”
Background
Effects of prenatal stress on neuroactive steroid responses to acute stress in adult male and female rats
Sze, Y., & Brunton, P. J. (2020) · Journal of Neuroendocrinology · doi:10.1111/jne.12916 · Cited by 18 · see citing works
Self-citation
Gender Differences in Perceived Stress and Its Relationship to Telomere Length in Costa Rican Adults
Méndez-Chacón, E. (2022) · Frontiers in Psychology · doi:10.3389/fpsyg.2022.712660 · Cited by 19 · see citing works
“Sexual differences in how the hypothalamic-pituitary-adrenal axis responds to stress are well established, and women tend to show more intense responses (Sze and Brunton, 2019).”
Background
The hypothalamic steroidogenic pathway mediates susceptibility to inflammation-evoked depression in female mice
Xu, F.-R., Wei, Z., Xu, X.-X., Zhang, X., Wei, C., Qi, X., Li, Y., Gao, X., & Wu, Y. H. (2023) · Journal of Neuroinflammation · doi:10.1186/s12974-023-02976-7 · Cited by 16 · see citing works
“Although evidence supporting the involvement of neu-rosteroids in rodent models of psychiatric disorders is compelling [45, 53, 54], the potential role of neuroactive steroids in mediating sex differences in vulnerability to depression, as well as variations in neurosteroidogenesis contributing to…”
BackgroundInfluential
(3α,5α)3-hydroxypregnan-20-one (3α,5α-THP) regulation of hypothalamic and extrahypothalamic corticotropin releasing factor (CRF): Sexual dimorphism and brain region specificity in Sprague Dawley rats
Boero, G., Tyler, R., Todd, C. A., O'Buckley, T., Balan, I., Besheer, J., & Morrow, A. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108463 · Cited by 15 · see citing works
“Moreover, oestrous cycle phase does not affect basal corticosterone concentrations or the corticosterone response to swim stress (Ogle and Kitay, 1977; Sze and Brunton, 2020).”
Background
Acute Cortisol Profile Associations With Cognitive Impairment After Severe Traumatic Brain Injury
Barton, D. J., Kumar, R. G., Schuster, A. A., Juengst, S. B., Oh, B., & Wagner, A. K. (2021) · Neurorehabilitation and neural repair · doi:10.1177/15459683211048771 · Cited by 16 · see citing works
Neurosteroid [3α,5α]-3-hydroxy-pregnan-20-one enhances IL-10 production via endosomal TRIF-dependent TLR4 signaling pathway
Balan, I. S., Grusca, A., O’Buckley, T. K., & Morrow, A. L. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1299420 · Cited by 14 · see citing works
The STRESS-EU database: A European resource of human acute stress studies for the worldwide research community
Sep, M. S. C., Veenman, K., Vinkers, C. H., Sep, M. S. C., Veenman, K., Habets, P. C., Bonapersona, V., Bakvis, P., Bentele, U. U., Binder, E. B., et al. (2024) · Neuroscience Applied · doi:10.1016/j.nsa.2024.104063 · Cited by 13 · see citing works
“…previous life experiences, etc.) and stressor (e.g. duration, intensity, controllability) related factors (Mcewen et al., 2020; Sanacora et al., 2022; Oyola et al., 2017; Juruena et al., 2020; Sze et al., 2020; Mikneviciute et al., 2023; Kuhn et al., 2021; Xin et al., 2020; Kühnel et al., 2020).”
Maternal Immune Activation with Toll-Like Receptor 7 Agonist During Mid-Gestation Alters Juvenile and Adult Developmental Milestones and Behavior
Sheng, J. A., & Tobet, S. (2024) · Journal of neuroendocrinology · doi:10.1111/jne.13417 · Cited by 11 · see citing works
“1,85,87,88 Improper development of these areas would increase risk for sex-biased disorders, including MDD and other comorbid diseases (e.g., cardiovascular disease, metabolic disorders, obesity, etc.).”
High-throughput rat immunoglobulin G N-glycosylation profiling revealed subclass-specific changes associated with chronic stress
Habazin, S., Mlinarević, D., Balog, M., Bardak, A., Gáspár, R., Szűcs, K. F., Vari, S. G., Vučković, F., Lauc, G., Novokmet, M., et al. (2021) · Journal of Proteomics · doi:10.1016/j.jprot.2021.104293 · Cited by 11 · see citing works
Neurosteroids and early-life programming: An updated perspective
Sze, Y., & Brunton, P. J. (2022) · Current Opinion in Endocrine and Metabolic Research · doi:10.1016/j.coemr.2022.100367 · Cited by 11 · see citing works
Self-citation
Non-Invasive Monitoring of Adrenocortical Activity in Three Sympatric Desert Gerbil Species
Navarro‐Castilla, Á., Garrido, M., Hawlena, H., & Barja, I. (2021) · Animals · doi:10.3390/ani11010075 · Cited by 11 · see citing works
White Matter Microstructure Is Associated with Serum Neuroactive Steroids and Psychological Functioning
Umminger, L. F., Rojczyk, P., Seitz‐Holland, J., Sollmann, N., Kaufmann, E., Kinzel, P., Zhang, F., Kochsiek, J., Langhein, M., Kim, C. L., et al. (2022) · Journal of Neurotrauma · doi:10.1089/neu.2022.0111 · Cited by 10 · see citing works
“148 The limited female sample size in our study, however, prevented from examining the sexes independently and should be targeted in future studies.”
Biomarkers of reproductive psychiatric disorders
Etyemez, S., Mehta, K., Iyer, S., Özdemir, İ., & Osborne, L. M. (2025) · The British Journal of Psychiatry · doi:10.1192/bjp.2025.134 · Cited by 8 · see citing works
Perceived Stress During the COVID-19-Related Confinement in Cyprus
Kyprianidou, M., Christophi, C. A., & Giannakou, K. (2021) · Frontiers in Public Health · doi:10.3389/fpubh.2021.673411 · Cited by 8 · see citing works
“with females typically presenting higher responses compared to males (24).”
Background
Acute Ozone-Induced Transcriptional Changes in Markers of Oxidative Stress and Glucocorticoid Signaling in the Rat Hippocampus and Hypothalamus Are Sex-Specific
Valdez, M. C., Freeborn, D. L., Vulimiri, P., Valdez, J. M., Kodavanti, U. P., & Kodavanti, P. R. S. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076404 · Cited by 9 · see citing works
“Alterations in glucocorticoid mechanisms and their levels are associated with chronic stress-related neurological disorders, known to affect males and females differently [54].”
Background
Reproductive status impact on tau phosphorylation induced by chronic stress
Muñoz-Mayorga, D., Rissman, R. A., & Morales, T. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100241 · Cited by 8 · see citing works
“Among them, a diminished response to diverse stressors has been reported during late pregnancy and lactation (Brunton and Russell, 2009; Sze and Brunton, 2019).”
Background
Corticotropin‐releasing factor signaling and its potential role in the prefrontal cortex‐dependent regulation of anxiety
Yang, X., & Geng, F. (2023) · Journal of Neuroscience Research · doi:10.1002/jnr.25238 · Cited by 9 · see citing works
Neurosteroid [3α,5α]-3-Hydroxy-pregnan-20-one Enhances the CX3CL1-CX3CR1 Pathway in the Brain of Alcohol-Preferring Rats with Sex-Specificity
Balan, I. S., Grusca, A., Chéry, S. L., Materia, B. R., O’Buckley, T. K., & Morrow, A. L. (2024) · Life · doi:10.3390/life14070860 · Cited by 6 · see citing works
“To mitigate potential circadian variations in neurosteroid levels, experiments were conducted in the morning [87,88].”
Method
Estrous cycle stage gates the effect of stress on reward learning
Johnston, M. P., Garcia-Castañeda, B. I., Cedillo, L. G., Patel, S. K., Vargas, V. S., & Wanat, M. J. (2025) · Neuropsychopharmacology · doi:10.1038/s41386-025-02170-8 · Cited by 6 · see citing works
“Across species, stress elicits greater activation of the hypothalamic-pituitary-adrenal (HPA) axis in females relative to males [1, 2].”
Premenstrual dysphoric disorder and sexual function: a narrative review
Susser, L., Parish, S. J., Dumas, E., & Nappi, R. E. (2023) · Sexual Medicine Reviews · doi:10.1093/sxmrev/qead007 · Cited by 6 · see citing works
In vitro binding analysis of legacy-linear and new generation-cyclic perfluoro-alkyl substances on sex hormone binding globulin and albumin, suggests low impact on serum hormone kinetics of testosterone
Pavan, A., Cendron, L., Nisio, A. D., Pedrucci, F., Šabović, I., Scarso, A., Ferlin, A., Angelini, A., Foresta, C., & Toni, L. D. (2023) · Toxicology · doi:10.1016/j.tox.2023.153664 · Cited by 6 · see citing works
Exploring metabolomic dynamics in acute stress disorder: amino acids, lipids, and carbohydrates
Gary, N. C., Misganaw, B., Hammamieh, R., & Gautam, A. (2024) · Frontiers in Genetics · doi:10.3389/fgene.2024.1394630 · Cited by 7 · see citing works
The Long-Term Effects of Chronic Unpredictable Mild Stress Experienced During Adolescence Could Vary Depending on Biological Sex
Shirokova, O. M., Kuzmina, D. M., Zaborskaya, O. G., Щелчкова, Н. А., Kozliaeva, E. V., Александровна, К. С., Pershin, V. I., Vasilchikov, P. I., & Mukhina, I. V. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26031251 · Cited by 6 · see citing works
The Effect of Allopregnanolone on Enzymatic Activity of the DNA Base Excision Repair Pathway in the Sheep Hippocampus and Amygdala under Natural and Stressful Conditions
Misztal, T., Kowalczyk, P., Młotkowska, P., & Marciniak, E. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21207762 · Cited by 5 · see citing works
“A protective action of AL against stress hormones, as well as its other beneficial effects on the CNS, have been widely documented in rodents and humans [64].”
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Applying the Research Domain Criteria to Rodent Studies of Sex Differences in Chronic Stress Susceptibility
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Ageing: Not only an age-related issue
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“…stress-related neuropsychiatric disease risk, in part resulting from dynamic hormonal reductions in women and other ageing-related cellular processes in limbic brain regions (Bale and Epperson, 2015; Bekhbat, and Neigh, 2018; Kelly et al., 2014; Navarro-Pardo et al., 2018; Sze, and Brunton, 2020).”
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Sex-dependent metabolic effects of pregestational exercise on prenatally stressed mice
Luft, C., Levices, I. P., Pedrazza, L., de Oliveira, J. R., & Donadio, M. V. F. (2020) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s2040174420000343 · Cited by 6 · see citing works
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Non-Targeted Metabolomics Investigation of a Sub-Chronic Variable Stress Model Unveils Sex-Dependent Metabolic Differences Induced by Stress
Kang, S., Kim, W., Nam, J., Li, K., Kang, Y., Bae, B., Chun, K., Chung, C., & Lee, J. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25042443 · Cited by 5 · see citing works
Assessment of preoperative health-related quality of life in patients undergoing thyroidectomy based on patient-reported outcomes
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“…(1) When faced with pressure, females are generally more likely to have stronger reactions and negative emotions such as anxiety or depression (Sze and Brunton, 2020); (2) The incision of open thyroidectomy is in a very prominent position, and females are more concerned about the neck scar…”
Background
Knockdown of cytochrome P450 1 A (cyp1a) gene suppresses growth and oxygen tolerance in zebrafish
Li, M., Wang, D., Huang, X., et al. (2025) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2025.111846 · Cited by 5 · see citing works
The Psychological Effects of Hormonal Treatment on Women Under IVF Treatment: A Comprehensive Review
Vasudevan, S. R., & Bhuvaneswari, M. (2024) · National Journal of Community Medicine · doi:10.55489/njcm.150620243829 · Cited by 5 · see citing works
“While there has been research examining the impact of sex steroids on the neurological process in both genders, regardless of their mental diseases, 8 there is a lack of comprehensive reviews that have specifically investigated the effects of hormonal therapies for infertility on mental health in…”
Background
The Influence of Factors such as Anxiety on the White Coat Effect during the Treatment of Patients with Hypertension
Xu, D., Qiu, H., Li, Z., Yan, P., He, X., Gu, Y., & Lin, H. (2022) · Reviews in Cardiovascular Medicine · doi:10.31083/j.rcm2311359 · Cited by 4 · see citing works
“However, this proposition has been disputable, and needs to be further studied [31].”
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Role of Epigenetic Modification in the Intergeneration Transmission of War Trauma
Bolouki, A. (2024) · Indian Journal of Clinical Biochemistry · doi:10.1007/s12291-023-01136-1 · Cited by 5 · see citing works
“There are also many ambiguities regarding gender differences in HPA function following stress and the essential contribution of sex hormones and sex chromosomes [40].”
Sex-specific effects of neuromodulatory drugs on normal and stress-induced social dominance and aggression in rats
Ishaq, S., Zahid, S., & Ahmed, T. (2023) · Psychopharmacology · doi:10.1007/s00213-023-06503-7 · Cited by 4 · see citing works
“The future endocrine response is shaped by these hormones via the hypothalamus pituitary adrenal and hypothalamus pituitary gonadal (HPA & HPG) axes (Sze and Brunton 2020).”
Impact of Psychological Stress-Derived Hormones and Cytokines on Immune Cell Profiles in Vitiligo: Toward Improved Peripheral Blood Simulation in Animal Models
Tang, N., Zhang, Q., Xiong, X.-F., Liu, X.-W., Wang, G.-E., & Wu, Y. (2025) · Clinical Cosmetic and Investigational Dermatology · doi:10.2147/ccid.s555801 · Cited by 5 · see citing works
“16 Psychological stress induced deceases in the level of sex hormones such as estrogen and progesterone in rodents.”
Standardized Extract from the Gotu Kola Leaves Improves Suicidal Behavior in Stressed Rats Subjected to Social Isolation
Thakurdesai, P. A., Nimse, S. R., Kore, P. S., & Aswar, U. M. (2024) · Biomedical & Pharmacology Journal · doi:10.13005/bpj/2896 · Cited by 3 · see citing works
“HPA axis dysfunction is associated with stress-related mental health issues 75 Cortisol levels are considered a promising approach to predict suicidal behavior in animals after social stress 52 .”
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The psychological impact of COVID‐19 among newly diagnosed patients with breast cancer when cancer care was returning to normal
Li, J., Zhu, S., & Gao, W. (2022) · European Journal of Cancer Care · doi:10.1111/ecc.13762 · Cited by 3 · see citing works
The interaction effect of childhood emotional maltreatment and peer victimization on adolescents’ altruistic behaviors: Does gender matter?
Gao, H., Liu, Q., & Wang, Z. (2025) · Children and Youth Services Review · doi:10.1016/j.childyouth.2025.108360 · Cited by 2 · see citing works
Impact of Sex Steroids on the Stress Response and Welfare in Female Farm Ruminants
Freitas‐de‐Melo, A., & Ungerfeld, R. (2022) · Sustainable agriculture reviews · doi:10.1007/978-3-031-07496-7_1 · Cited by 3 · see citing works
The Role of Corticotropin-Releasing Factor Receptor 1 in the Stress-Induced Alteration of Visual Properties in Primary Visual Cortex: Insights from the Single Prolonged Stress Model
Xia, Q., Kuang, X., Meng, W., et al. (2024) · Neuroscience Bulletin · doi:10.1007/s12264-024-01204-3 · Cited by 2 · see citing works
“Since stress may have different impacts on the response in males and females [7], we conducted separate analyses of the data of male and female mice.”
Sex Differences in the Relationship Between Nucleus Accumbens Volume and Youth Tobacco or Marijuana Use Following Stressful Life Events
Assari, S., & Sheikhattari, P. (2024) · JOURNAL OF MENTAL HEALTH AND CLINICAL PSYCHOLOGY · doi:10.29245/2578-2959/2024/2.1305 · Cited by 3 · see citing works
Physiological Effects of Psychological Interventions Among Persons with Financial Stress: A Systematic Review, Meta-analysis, and Introduction to Psychophysiological Economics
Lehrer, P. M., Derby, L., Smith, J. E., Grable, J. E., & Hanlon, R. (2024) · Applied Psychophysiology and Biofeedback · doi:10.1007/s10484-024-09658-x · Cited by 2 · see citing works
“Sometimes cortisol output can be blocked in chronic stress, where homeostatic processes become dysregulated due to allostatic overload (Sze & Brunton, 2019).”
Perception of earthquake and analysis of its impact factors based on interpretable machine learning: data from the 6 august 2023 earthquake in Pingyuan County, China
Zhang, E., Ding, N., Yang, L., Wang, Y., Shi, J., & Xu, Y. (2025) · Natural Hazards · doi:10.1007/s11069-024-07073-3 · Cited by 2 · see citing works
“In a study by Sze and Brunton (2020) it was noted that the hypothalamic–pituitary–adrenal (HPA) axis plays a key role in the neuroendocrine response to stress and that females typically show a more intense response to stress.”
Comparative electrophysiological study of neuroactive steroid-induced hypnosis in mice: sex and drug-specific differences
Martin, A., Coulter, I. C., Cox, R., Covey, D. F., Todorovic, S. M., & Stamenić, T. T. (2025) · Experimental Biology and Medicine · doi:10.3389/ebm.2025.10550 · Cited by 2 · see citing works
Impact of maternal physical exercise on inflammatory and hypothalamic–pituitary–adrenal axis markers in the brain and lungs of prenatally stressed neonatal mice
da Costa, M. S., Luft, C., Sbruzzi, M., de Oliveira, J. R., & Donadio, M. V. F. (2022) · Developmental Psychobiology · doi:10.1002/dev.22330 · Cited by 1 · see citing works
The Effect of Various Types of Mother Stress on the Some Components of the Brain Redox System in Male and Female Rats on the 20th Day of the Embryonic Development Period
Vyushina, A. V., Притворова, А. В., Пивина, С. Г., Акулова, В. К., & Ordyan, N. E. (2024) · Neurochemical Journal · doi:10.1134/s181971242470034x · Cited by 1 · see citing works
Adolescent CB1 receptor expression at the BLA and CA1 and acute AM251 effects on sociability and emotional memory are sex-specific, and not modulated by heterotypic stress exposure
Person, E., & Plamondon, H. (2025) · Behavioural Brain Research · doi:10.1016/j.bbr.2025.115704 · Cited by 1 · see citing works
Changes in the Adrenal Cortex Induced by Liraglutide Treatment and Exercise in a Rat Model of Menopausal Transition
Gizdović, I., Šošić‐Jurjević, B., Vlahović, D., Ristić, N., Lavrnja, I. C., Filipović, B. R., Marina, L., & Trifunović, S. L. (2026) · Cells · doi:10.3390/cells15141258 · Cited by 1 · see citing works
“This difference correlates with a sex-specific ACTH response, suggesting that HPA axis sensitivity is modulated by biological sex [60] and hormonal phases [61].”
A study of the effect of some musical compositions on glucagon-like peptide 1, insulin, leptin, and body weight of crowded adult albino rats
Al-Etreby, M. Z., Khalil, A. A., & Abd-Elrhman, A. A.-E. (2023) · Al-Azhar Assiut Medical Journal · doi:10.4103/azmj.azmj_12_22 · Cited by 2 · see citing works
Perceived stress and delay discounting in schizophrenia, cannabis use disorder, and co-occurring disorders
Trask, C. L., Roth, R. M., Henricks, A. M., Hickey, S. M., & Brunette, M. F. (2024) · Psychiatry Research Communications · doi:10.1016/j.psycom.2024.100179 · Cited by 1 · see citing works
Sexually Dimorphic Effects of Neuromodulatory Drugs on Normal and Stress-Induced Social Interaction in Rats
Ishaq, S., & Ahmed, T. (2023) · Brain Sciences · doi:10.3390/brainsci13101378
“The differential effects of stress on different neuro-transmitter systems are controlled by sex-hormones and corticotrophin releasing hormone (CRH) via the hypothalamus-pituitary-adrenal (HPA) and hypothalamus-pituitary-gonadal (HPG) axes [32].”
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The Effect of Various Types of Mother Stress on the Some Components of the Brain Redox System in Male and Female Rats on the 20th Day of the Embryonic Development Period
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Wechselspiel zwischen Depression und Sexualität
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Sex steroid profiles align with phenotype in sex-reversed female lizards
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Steroid alterations in Cushing’s disease persist after remission: ACTH-driven steroid changes dissociate from mood-regulatory neurosteroids
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MicroRNAs expression changes associated with trauma-focused psychotherapy efficacy in treatment-resistant depression: An exploratory study
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Steroid 5α-reductases in the brain: From neurosteroidogenesis to therapeutic implications
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Authors: Sze, Y., & Brunton, P. J.
Affiliations: University of Edinburgh (GB)
Zhejiang University-University of Edinburgh Institute (CN)
Corresponding author: Brunton, Paula J.
ORCID: Sze, Ying
Brunton, Paula J.
Venue: European Journal of Neuroscience
Publisher: Wiley
Published: 2019-12-16
Volume: 52
Issue: 1
Pages: 2487-2515
ISSN: 0953-816X (ISSN-L)
1460-9568
DOI: 10.1111/ejn.14615
OpenAlex: W2986182493
Semantic Scholar: 159f8f5f1e1a321f860793073694d9286717da73
Cited by: 85
References: 332
Citations by year: 2026: 4 · 2025: 11 · 2024: 21 · 2023: 13 · 2022: 14 · 2021: 9 · 2020: 13
FWCI: 1.04
Type: journal article
Language: en
Open access: green
www.research.ed.ac.uk
Licence: other-oa
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: European Journal of Neuroscience (publishedVersion)
PubMed (publishedVersion)
Edinburgh Research Explorer (University of Edinburgh) (acceptedVersion, other-oa)
Funders: Biotechnology and Biological Sciences Research Council
University of Edinburgh
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Keywords: hypothalamic-pituitary-adrenal axis, sex differences, neurosteroids, chronic stress, acute stress, mood disorders, HPA axis dysregulation
MeSH terms: Animals, Female, Humans, Hypothalamo-Hypophyseal System, Male, Pituitary-Adrenal System, Sex Characteristics, Gonadal Steroid Hormones, Steroids, Stress, Physiological, Stress, Psychological

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