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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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“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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Advances in neurosteroids: role in clinical practice
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Self-citationThe Allopregnanolone Response to Acute Stress in Females: Preclinical and Clinical Studies
Pisu, M. G., Concas, L., Siddi, C., Serra, M., & Porcu, P. (2022) · Biomolecules · doi:10.3390/biom12091262 · Cited by 20
Hypoxia Potentiates Endotoxin-Induced Allopregnanolone Concentrations in the Newborn Brain
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Progesterone, GABA and mood disorders in women
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“The major metabolites of progesterone; allopregnanolone and pregnanolone and the major metabolite of deoxycorticosterone (DOC), allotetrahydrocorticosterone (THDOC) have anxiolytic, antiaggressive and sedative effects in various animal models (Bitran et al., 1991; Purdy et al., 1991; Rodriguez-Sierra et al., 1984; Bar…”
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“Our findings also support the hypothesis that the upregulation of progesterone during acute external stress in animals (Barbaccia et al., 1996) and prolonged internal stress during cocaine withdrawal in humans (Fox et al.”
ResultSocial isolation increases the response of peripheral benzodiazepine receptors in the rat
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“Acute forced swim stress (FSS) increases circulating, cerebral cortical, and hypothalamic levels of 3α,5α-THP and 3α,5α-THDOC, as well as the precursor pregnenolone in various rat strains (Purdy et al., 1991; Barbaccia et al., 1996; Vallée et al., 2000).”
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“Accordingly, changes in its endogenous concentrations not only affect the behavioral aspects that are under GABAergic regulation, including expression of emotional reactivity (Barbaccia et al., 1996; Bitran et al., 2000; Serra et al., 2000; Zimmerberg et al, 2005), cognitive functions (Romeo et al.”
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Brain Allopregnanolone in the Fetal and Postnatal Rat in Response to Uteroplacental Insufficiency
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Demori, I., Losacco, S., Giordano, G., Mucci, V., Blanchini, F., & Burlando, B. (2024) · PLOS ONE · doi:10.1371/journal.pone.0303573 · Cited by 14
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Can animal models resemble a premenstrual dysphoric condition?
Estrada-Camarena, E. M., & López‐Rubalcava, C. (2022) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2022.101007 · Cited by 15
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“These effects are recapitulated in rat models, where acute forced swim stress (FSS) increases circulating, cerebral cortical, and hypothalamic levels of 3α,5αTHP and 3α,5α-THDOC, as well as the precursor pregnenolone (Barbaccia et al. 1996; Purdy et al. 1991; Vallee et al. 2000).”
Fleiss, B., Parkington, H. C., Coleman, H. A., Dickinson, H., Yawno, T., Castillo-Meléndez, M., Hirst, J. J., & Walker, D. W. (2011) · Brain Research · doi:10.1016/j.brainres.2011.11.035 · Cited by 14
“Reports that allopregnanolone levels increase in the brain in response to stress, including hypoxic-ischemia (HI; Barbaccia et al., 1996; Nguyen et al., 2004), suggest that allopregnanolone may function as an endogenous neuroprotectant.”
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Rahmani, B., Ghasemi, R., Dargahi, L., Ahmadiani, A., & Haeri, A. (2015) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2015.09.030 · Cited by 14
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“Several authors have reported a release of neuroactive steroids in plasma and in the brain after various acute stressors in rats (Purdy et al. 1991; Barbaccia et al. 1996 ) and in mice (Mele et al. 2004) consistent with the present results.”
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Heshmatian, B., Roshan-Milani, S., & Saboory, E. (2010) · DOAJ (DOAJ: Directory of Open Access Journals) · Cited by 14
Allopregnanolone alters follicular and luteal dynamics during the estrous cycle
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BackgroundIncrease in testosterone metabolism in the rat central nervous system by formalin-induced tonic pain
Amini, H., & Ahmadiani, A. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00986-3 · Cited by 11
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Prefrontal 5α-reductase 2 mediates male-specific acute stress response
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ResultDevelopmental and adult stress: effects of steroids and neurosteroids
Gore, I. R., & Gould, E. (2024) · Stress · doi:10.1080/10253890.2024.2317856 · Cited by 11
“Peak brain and plasma levels of allopregnanolone and tHDOc are noted in rats exposed to acute stressors such as cold swim stress, foot shock, or carbon dioxide exposure (Barbaccia et al., 1996, 1997).”
Effects of gestational allopregnanolone administration in rats bred for high affective behavior
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“The progesterone metabolite allopregnanolone (3α-hydroxy-5α-pregnan-20-one or 3α,5α-THP) is not only an ovarian steroid but an endogenous neurosteroid that is a potent positivemodulator of the GABA-A receptor, enhancing GABA-stimulated chloride uptake [1,2].”
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“…acting by intracellular membrane diffusion after being produced by these neurons (Wieland et al., 1991; Paul and Purdy, 1992; Patchev et al., 1994; Barbaccia et al., 1996; Brot et al., 1997; Beaulieu, 1998; Concas et al., 1998; Akwa et al., 1999; Rupprecht and Holsboer, 1999; Bitran et al., 2000;…”
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Neurosteroids and the Nervous System
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“Neurosteroids enhancing GABAA receptor function may minimize the reduction in GABAergic inhibitory transmission and restore HPA axis homeostatic control [69].”
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Islas-Preciado, D., Estrada-Camarena, E. M., & Galea, L. A. M. (2024) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2024.101171 · Cited by 8
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“, 1998) while AlloP brain and plasma levels increase (Barbaccia et al., 1996; Purdy et al., 1991) in adult rats after acute stress, such as the exposure to CO2 or swimming.”
BackgroundEffect of Psychological Stress on [35S]TBPS Binding in Rat Brain
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Developmental Effects of Selective Breeding for an Infant Trait
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Allosteric Modulation of GABAA Receptor by Somatostatin Is Altered under Stress in Rat Brainstem
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Task‐ and Time‐Dependent Memory Enhancement byDehydroepiandosterone in Day‐Old Chicks
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“Rodent models of acute exposure to stress (e.g., swimming, foot shock or carbon dioxide exposure) show increased synthesis of neuroactive steroids and associated E/I balance disruption (Barbaccia et al., 1996, 1997; Reddy, 2010; Reddy et al., 2021).”
Thörnblom, E., Cunningham, J. L., Gingnell, M., Landén, M., Bergquist, J., & Bodén, R. (2024) · BMC Psychiatry · doi:10.1186/s12888-024-06167-3 · Cited by 2
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Self-citationPerimenopausia y trastornos afectivos: aspectos básicos y clínicos
Ramos, M. F., & Martı́nez-Mota, L. (2012) · Redalyc (Universidad Autónoma del Estado de México) · Cited by 2
Berretz, G., Packheiser, J., Wolf, O. T., & Ocklenburg, S. (2023) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2023.1054168 · Cited by 2
McFarland, M. H., Machado, M. M. F., Sansbury, G. M., Musselman, K. C., Boero, G., O’Buckley, T. K., Carr, C. C., Morrow, A. L., & Robinson, D. L. (2024) · Psychopharmacology · doi:10.1007/s00213-024-06534-8 · Cited by 2
“We showed in experi - ment 1 that acute cocaine increased pregnenolone levels in the serum of male and female rats, consistent with reports that acute and pharmacological stressors can increase lev - els of pregnenolone via HPA-axis activation (Barbaccia et al. 1996 ; Porcu et al. 2006).”
Neuroactive Steroids and the GABAA Receptor
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Floris, G., Asuni, G. P., Talani, G., Biggio, F., Pisu, M. G., Zanda, M. T., Contu, L., Maciocco, E., Serra, M., & Follesa, P. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.893835 · Cited by 2
“Neuroactive steroids from bilateral hippocampi were quantified by radioimmunoassay (RIA) as previously described (Barbaccia et al., 1996).”
MethodFollesa, P., Cagetti, E., Porta, S., Espositoto, G., & Biggio, G. (2000) · Molecular Brain Research · doi:10.1016/s0169-328x(00)00209-6 · Cited by 1
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Self-citationDubrovsky, B. O. (2008) · Springer eBooks · doi:10.1007/978-1-4020-6854-6_19
Neuroactive Steroids and the GABAA Receptor
Smith, S. S., & Shen, H. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00047-4
Neurosteroids in clinical practice: implications for women’s health
Genazzani, A. R., Bucci, F., Russo, N., Daino, D., Santoro, A. N., & Pluchino, N. (2011) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci.2011.120
TRACE ELEMENTS DISTRIBUTION IN THE BRAIN OF STRESSED RATS
kamal, K. (2012) · Neuroscience International · doi:10.3844/amjnsp.2012.79.86
BRIEF REPORT Stress induces a functional asymmetry in an emotional attention task
Nadolny, N., & Wolf, O. T. (2012)
Potential neurosteroid replacement therapy following premature birth and fetal growth restriction
Kelleher, M. A. (2012) · NOVA (University of Newcastle Australia)
Ethnicity and pain: psychosocial stress and stress Responses
Mechlin, B. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/rz2e-ja34
Bhogal, N., & Scrivens, M. (2008) · Alternatives to Laboratory Animals · doi:10.1177/026119290803600515
“The fact that CO2 has in the past been used as a pain stimulus and to induce acute stress in animals (22, 23), suggests that the suffering involved may be considerable.”
BackgroundBerretz, G., Packheiser, J., Höffken, O., et al. (2021) · Research Square · doi:10.21203/rs.3.rs-677791/v1
Mahmoud, U. T., El-Sayed, M. S. A., & Khalil, N. S. A. (2019) · Asian Journal of Animal Sciences · doi:10.3923/ajas.2020.25.32
Nenchovska, Z., Atanasova, M., Stoynova, T., Toteva, G., & Tchekalarova, J. (2024) · Physiology & Behavior · doi:10.1016/j.physbeh.2024.114712
“On the other hand, in rodent animal models, an increase in Pro levels is observed under stressors such as exposure to forced swimming [21,22], suggesting that this hormone has an adaptive stress-reducing effect in contrast to the CORT surge under stress conditions.”
Backgroundvan Vuuren, M. J. (2011) · SUNScholar (Stellenbosch University)
Metadata
- 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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