Time-Dependent Changes in Rat Brain Neuroactive Steroid Concentrations and GABA A Receptor Function after Acute Stress
Abstract
The time courses of changes in rat brain neuroactive steroid concentrations and gamma-aminobutyric acid type A (GABAA) receptor function elicited by acute stress were investigated in animals exposed to CO2 for 1 min, a treatment known to induce stress in rats and panic attacks in humans. Inhalation of CO2 induced increases in cerebral cortical steroid concentrations, the time dependence of which varied with the steroid examined. Thus, progesterone and deoxycorticosterone showed maximal increases (10- and 4-fold, respectively) 10 min after CO2 inhalation and had returned to basal values by 30 and 60 min, respectively. In contrast, pregnenolone and 3alpha-hydroxy-5alpha-pregnan-20-one (allopregnanolone) concentrations showed maximal increases (+174 and + 200%, respectively) at 30 min, were still higher than control at 60 min and returned to control values 120 min after stress. Inhalation of CO2 also resulted in increases in plasma steroid concentrations, most of which peaked at 30 min and had returned to control values by 60 min. A parallel analysis of the stress-induced changes in GABAA receptor function, assessed either biochemically by t-[35S]butylbicyclophosphorothionate ([35S]TBPS) binding to cerebral cortical membranes or behaviorally by the punished responding score in Vogel's test, showed that the effects of CO2 inhalation on both parameters were maximal (+51 and -40%, respectively) after 10 min; the behavioral reaction returned to normal after 60 min, whereas [35S]TBPS binding had returned to control values 120 min after stress. The results show that: (a) the maximal increase in the brain concentrations of allopregnanolone, a potent and efficacious positive modulator of GABAA receptors, occurred at a time (30 min) when both conflict behavior and [35S]TBPS binding begun to decrease, and (b) both allopregnanolone concentrations and [35S]TBPS binding had returned to control values 120 min after CO2 inhalation. The data are thus consistent with a physiological role of neuroactive steroids in restoring GABAergic tone after stress.
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The first global effect of acute stress is a rapid decrease of GABAergic transmission together with an increase of glutamate transmission in brain areas involved in cognitive functions, such as prefrontal cortex and hippocampus.
“Accordingly, the first global effect of acute stress is a rapid decrease of GABAergic transmission together with an increase of glutamate transmission in brain areas involved in cognitive functions, such as prefrontal cortex and hippocampus [66,67].”
From Fibromyalgia pathogenesis explained by a neuroendocrine multistable model (2024) · cites this paper as [66]
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Neurosteroids in the context of stress: implications for depressive disorders
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InfluentialSelf-citationStress-induced increase in brain neuroactive steroids: Antagonism by abecarnil
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BackgroundInfluentialMeasurement of Steroid Concentrations in Brain Tissue: Methodological Considerations
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“Focused microwave irradiation is thus potentially useful for preventing continued steroid metabolism and has been used in a few studies of brain steroid levels (e.g., Korneyev et al., 1993a,b; Barbaccia et al., 1996; Concas et al., 2000).”
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“Progesterone was administered rather than 3α-5α-THP because it is known that elevated circulating levels of P, such as found during the estrous (or menstrual) cycle or after stress, (Barbaccia et al., 1996; Kellogg and Frye, 1999; Purdy et al., 1991; Steimer et al., 1997; Vallee et al., 2000; Wilson and Biscardi, 1997…”
BackgroundInfluentialRole of hormones and neurosteroids in epileptogenesis
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Stress-induced plasticity of GABAergic inhibition
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“THDOC is produced in response to acute stress, increasing to physiologically-relevant levels which can act on GABAARs (Purdy et al., 1991; Barbaccia et al., 1996a).”
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“…allopregnanolone have been associated with stress, pregnancy, the menstrual cycle, menopause, regulation of neuronal excitability, and a variety of neurological or psychiatric disorders (Barbaccia et al. 1996; Bicikova et al. 1998; Biggio and Purdy 2001; Concas et al. 1998; Genazzani et al. 1998).”
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“These conditions increase endogenous 3α, 5α-THP levels that are found to be pharmacologically relevant and modify the functioning of central GABAA receptors in vivo (Hiemke et al. 1991; Paul and Purdy 1992; Barbaccia et al. 1996; Morrow et al. 1995; Concas et al. 1998).”
Neurosteroids, neuroactive steroids, and symptoms of affective disorders
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“Acute stress both in humans or experimental animals increases thebrainandplasma levelsof Allo (Bali and Jaggi 2013; Barbaccia et al. 1996; Purdy et al. 1991; Vallée et al. 2000); on the other hand, environmental stress for prolonged periods of time is associated with a decline of neurosteroid biosynthesis and involves…”
Neurosteroids’ effects and mechanisms for social, cognitive, emotional, and physical functions
Frye, C. A. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.07.005 · Cited by 88 · see citing works
“We now know that hormone levels can change in response to extreme environmental and/or behavioral situations and, thereby, influence the likelihood of subsequent hormone-mediated processes (Barbaccia et al., 1996; Drugan et al., 1995; Patchev et al., 1994, 1996).”
BackgroundRelationship between salivary cortisol and progesterone levels in humans
Wirth, M. M., Meier, E. A., Fredrickson, B. L., & Schultheiss, O. C. (2006) · Biological Psychology · doi:10.1016/j.biopsycho.2006.06.007 · Cited by 86 · see citing works
“All rights reserved. doi:10.1016/j.biopsycho.2006.06.007 metabolite, allopregnanolone, in response to stress (Barbaccia et al., 1996; Genazzani et al., 1998; Girdler et al., 2001; Klatzkin et al., 2006; Purdy et al., 1991) and other motivation/emotionarousing stimuli (Schultheiss et al., 2004).”
InfluentialRegion‐ and Sex‐Specific Modulation of Anxiety Behaviours in the Rat
Toufexis, D. (2007) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2007.01552.x · Cited by 87 · see citing works
Toufexis, D. J., Davis, C., Hammond, A., & Davis, M. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1386-04.2004 · Cited by 86 · see citing works
“…male rats are increased 4- to 20-fold over baseline values (Purdy et al., 1991), and serum THP is increased after injection of CRF and adrenocorticotropin hormone (Torres et al., 2001) after CO2 exposure (Barbaccia et al., 1996) and after footshock (Barbaccia et al., 1997) in male rats.”
Background(EFSA), E. F. S. A. (2005) · EFSA Journal · doi:10.2903/j.efsa.2005.292 · Cited by 86 · see citing works
Sze, Y., & Brunton, P. J. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14615 · Cited by 85 · see citing works
“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…”
BackgroundSkilbeck, K. J., Johnston, G. A. R., & Hinton, T. (2009) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2009.06539.x · Cited by 85 · see citing works
The role of pregnane neurosteroids in ethanol withdrawal: behavioral genetic approaches
Finn, D. A., Ford, M. M., Wiren, K. M., Roselli, C. E., & Crabbe, J. C. (2004) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2003.10.006 · Cited by 83 · see citing works
Follesa, P., Concas, A., Porcu, P., Sanna, E., Serra, M., Mostallino, M. C., Purdy, R. H., & Biggio, G. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00125-4 · Cited by 83 · see citing works
Self-citationSocial isolation stress and neuroactive steroids
Serra, M., Sanna, E., Mostallino, M. C., & Biggio, G. (2006) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2006.03.004 · Cited by 83 · see citing works
Self-citationStress, ethanol, and neuroactive steroids
Biggio, G., Concas, A., Follesa, P., Sanna, E., & Serra, M. (2007) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2007.04.005 · Cited by 82 · see citing works
“…1979) that induces a transient reduction in GABA-mediated inhibitory neurotransmission and increases the brain and plasma concentrations of steroids (Barbaccia et al., 1996c; Barbaccia et al., 1997)—also increased the abundance of progesterone, 3α,5α-THP, and 3α,5α-THDOC in the cerebral cortex and…”
BackgroundResultInfluentialSelf-citationKim, Y., Zhang, H., & Kim, H. (2000) · Analytical Biochemistry · doi:10.1006/abio.1999.4384 · Cited by 82 · see citing works
Brunelli, S. A., & Hofer, M. A. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.04.014 · Cited by 80 · see citing works
Altered expression of δGABAA receptors in health and disease
Whissell, P. D., Lecker, I., Wang, D.-S., Yu, J., & Orser, B. A. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.08.003 · Cited by 81 · see citing works
Hardoy, M. C., Serra, M., Carta, M. G., Contu, P., Pisu, M. G., & Biggio, G. (2006) · Journal of Clinical Psychopharmacology · doi:10.1097/01.jcp.0000229483.52955.ec · Cited by 80 · see citing works
“Quantitative analysis of steroids was performed by radioimmunoassay with specific antibodies and respective tritiated standards as described previously.(38,39) Antibodies to 3a,5a-THPROG and 3a,5aTHDOC were characterized previously,(38) and those to progesterone and to cortisol were from ICN (Costa Mesa, CA).”
MethodSelf-citationReddy, D. S. (2011) · Frontiers in Endocrinology · doi:10.3389/fendo.2011.00038 · Cited by 80 · see citing works
Motzo, C., Porceddu, M. L., Maira, G., Flore, G., Concas, A., Dazzi, L., & Biggio, G. (1996) · Journal of Psychopharmacology · doi:10.1177/026988119601000402 · Cited by 78 · see citing works
Self-citationStress and neurosteroids in adult and aged rats
Barbaccia, M. L., Concas, A., Serra, M., & Biggio, G. (1998) · Experimental Gerontology · doi:10.1016/s0531-5565(98)00042-4 · Cited by 77 · see citing works
Self-citationO’Dell, L. E., Alomary, A. A., Vallée, M., Koob, G. F., Fitzgerald, R. L., & Purdy, R. H. (2003) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2003.11.031 · Cited by 78 · see citing works
“The present results using GC/MS are in agreement with the previous studies of Barbaccia et al. (1996, 2001) using RIA for neuroactive steroid measurement.”
Self-citationReddy, D. S. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.10.016 · Cited by 73 · see citing works
Trapani, G., Laquintana, V., Denora, N., et al. (2004) · Journal of Medicinal Chemistry · doi:10.1021/jm049610q · Cited by 71 · see citing works
Self-citationSinnott, R. S., Phillips, T. J., & Finn, D. A. (2002) · Psychopharmacology · doi:10.1007/s00213-002-1123-1 · Cited by 69 · see citing works
“Steroid levels can increase to pharmacologically relevant concentrations in response to stress, estrus cycle, and pregnancy (Paul and Purdy 1992; Barbaccia et al. 1996; Concas et al. 1998).”
BackgroundPorcu, P., Sogliano, C., Cinus, M., Purdy, R. H., Biggio, G., & Concas, A. (2003) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)01065-1 · Cited by 69 · see citing works
Self-citationReddy, D. S., & Rogawski, M. A. (2010) · Epilepsia · doi:10.1111/j.1528-1167.2010.02870.x · Cited by 66 · see citing works
Serra, M., Pisu, M. G., Muggironi, M., Parodo, V., Papi, G., Sari, R., Dazzi, L., Spiga, F., Purdy, R. H., & Biggio, G. (2001) · Psychopharmacology · doi:10.1007/s002130100853 · Cited by 67 · see citing works
Self-citationIncreased allopregnanolone levels in the fetal sheep brain following umbilical cord occlusion
Nguyen, P. N., Yan, E. B., Castillo-Meléndez, M., Walker, D. W., & Hirst, J. J. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.069336 · Cited by 67 · see citing works
“2002) and of others of responses to stress in adult animals (Barbaccia et al. 1996).”
BackgroundResultAllopregnanolone and pregnanolone are produced by the human corpus luteum
Ottander, U., Poromaa, I. S., Bjurulf, E., Skytt, Å., Bäckström, T. C., & Olofsson, J. I. (2005) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2005.04.007 · Cited by 66 · see citing works
Neurosteroids and neuroactive drugs in mental disorders
Pisu, M. G., & Serra, M. (2004) · Life Sciences · doi:10.1016/j.lfs.2003.12.002 · Cited by 66 · see citing works
- Authors
- Barbaccia, M. L., Roscetti, G., Trabucchi, M., Mostallino, M. C., Concas, A., Purdy, R. H., & Biggio, G.
- Affiliations
- University of Rome Tor Vergata (IT)
- University of Cagliari (IT)
- University of California San Diego (US)
- ORCID
- Venue
- Neuroendocrinology
- Publisher
- S. Karger AG
- Published
- 2008-04-09
- Volume
- 63
- Issue
- 2
- Pages
- 166-172
- ISSN
- 0028-3835 (ISSN-L)
- 1423-0194
- OpenAlex
- W2084243951
- Cited by
- 303
- References
- 0
- Citations by year
- 2025: 3 · 2024: 9 · 2023: 3 · 2022: 7 · 2021: 6 · 2020: 7 · 2019: 5 · 2018: 5 · 2017: 2 · 2016: 9 · 2015: 4 · 2014: 17 · 2013: 7 · 2012: 13
- FWCI
- 6.12
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Cineca Institutional Research Information System (Tor Vergata University) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- neurosteroids, GABAA receptor, acute stress, CO2 inhalation, allopregnanolone, progesterone, deoxycorticosterone, pregnenolone, cerebral cortex, GABAergic tone, panic attacks, [35S]TBPS binding
- MeSH terms
- Animals, Brain Chemistry, Carbon Dioxide, Cerebral Cortex, Conflict, Psychological, Male, Receptors, GABA-A, Steroids, Stress, Psychological, Time Factors, Rats, Sprague-Dawley, Bridged Bicyclo Compounds, Heterocyclic, Rats
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