CRH receptor antagonism reverses the effect of social subordination upon central GABAA receptor binding in estradiol-treated ovariectomized female rhesus monkeys
•Social subordination alters GABAARs binding in estradiol-treated female monkeys.•Status effect on GABAAR is site specific, only seen in the prefrontal cortex.•CRH receptor antagonism reverses status differences in GABAAR binding.•Implicates the stress axis in the dysregulation of GABAAR in subordin...
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| Published in | Neuroscience Vol. 250; pp. 300 - 308 |
|---|---|
| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Amsterdam
Elsevier Ltd
10.10.2013
Elsevier |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0306-4522 1873-7544 1873-7544 |
| DOI | 10.1016/j.neuroscience.2013.07.002 |
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| Abstract | •Social subordination alters GABAARs binding in estradiol-treated female monkeys.•Status effect on GABAAR is site specific, only seen in the prefrontal cortex.•CRH receptor antagonism reverses status differences in GABAAR binding.•Implicates the stress axis in the dysregulation of GABAAR in subordinate females.•Provides mechanism by which subordination alters the actions of estradiol.
Persistent exposure to environmental stressors causes dysregulation of the limbic–hypothalamic–pituitary–adrenal (LHPA) axis and alters GABAA receptor (GABAAR) levels throughout the brain. Social subordination in socially housed female rhesus results in distinctive stress-related physiological and behavioral phenotypes that are dependent on the ovarian hormone estradiol (E2). In the present study, we utilized ovariectomized adult female rhesus monkeys undergoing hormone replacement with E2 to test the hypothesis that the chronic psychosocial stress of subordination alters GABAAR binding potential (GABAAR BPND) in limbic regions implicated in emotional processing including the prefrontal cortex, temporal lobe (amygdala and hippocampus), and hypothalamus. Furthermore, we tested the hypothesis that peripheral administration of a corticotropin-releasing hormone (CRH) receptor antagonist (astressin B) would reverse the alterations in GABAAR binding within these regions in subordinate females. After subjects received astressin B or saline for three consecutive days, GABAAR BPND was determined by positron emission tomography (PET) using 18F-flumazenil as a radioligand. T1-weighted structural magnetic resonance imaging scans were also acquired for PET scan co-registration, in order to perform a region of interest analysis using the pons as a reference region. Compared to socially dominant females, subordinate females exhibited increased GABAAR BPND in the prefrontal cortex but not in the temporal lobe or the hypothalamus. Administration of astressin B eliminated the status difference in GABAAR BPND in the prefrontal cortex, suggesting that the chronic stressor of social subordination modulates GABAergic tone via effects on CRH and the LHPA axis, at least in prefrontal regions. |
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| AbstractList | •Social subordination alters GABAARs binding in estradiol-treated female monkeys.•Status effect on GABAAR is site specific, only seen in the prefrontal cortex.•CRH receptor antagonism reverses status differences in GABAAR binding.•Implicates the stress axis in the dysregulation of GABAAR in subordinate females.•Provides mechanism by which subordination alters the actions of estradiol.
Persistent exposure to environmental stressors causes dysregulation of the limbic–hypothalamic–pituitary–adrenal (LHPA) axis and alters GABAA receptor (GABAAR) levels throughout the brain. Social subordination in socially housed female rhesus results in distinctive stress-related physiological and behavioral phenotypes that are dependent on the ovarian hormone estradiol (E2). In the present study, we utilized ovariectomized adult female rhesus monkeys undergoing hormone replacement with E2 to test the hypothesis that the chronic psychosocial stress of subordination alters GABAAR binding potential (GABAAR BPND) in limbic regions implicated in emotional processing including the prefrontal cortex, temporal lobe (amygdala and hippocampus), and hypothalamus. Furthermore, we tested the hypothesis that peripheral administration of a corticotropin-releasing hormone (CRH) receptor antagonist (astressin B) would reverse the alterations in GABAAR binding within these regions in subordinate females. After subjects received astressin B or saline for three consecutive days, GABAAR BPND was determined by positron emission tomography (PET) using 18F-flumazenil as a radioligand. T1-weighted structural magnetic resonance imaging scans were also acquired for PET scan co-registration, in order to perform a region of interest analysis using the pons as a reference region. Compared to socially dominant females, subordinate females exhibited increased GABAAR BPND in the prefrontal cortex but not in the temporal lobe or the hypothalamus. Administration of astressin B eliminated the status difference in GABAAR BPND in the prefrontal cortex, suggesting that the chronic stressor of social subordination modulates GABAergic tone via effects on CRH and the LHPA axis, at least in prefrontal regions. Persistent exposure to environmental stressors causes dysregulation of the limbic-hypothalamic-pituitary-adrenal (LHPA) axis and alters GABAA receptor (GABAAR) levels throughout the brain. Social subordination in socially housed female rhesus results in distinctive stress-related physiological and behavioral phenotypes that are dependent on the ovarian hormone estradiol (E2). In the present study, we utilized ovariectomized adult female rhesus monkeys undergoing hormone replacement with E2 to test the hypothesis that the chronic psychosocial stress of subordination alters GABAAR binding potential (GABAAR BPND) in limbic regions implicated in emotional processing including the prefrontal cortex, temporal lobe (amygdala and hippocampus), and hypothalamus. Furthermore, we tested the hypothesis that peripheral administration of a corticotropin-releasing hormone (CRH) receptor antagonist (astressin B) would reverse the alterations in GABAAR binding within these regions in subordinate females. After subjects received astressin B or saline for three consecutive days, GABAAR BPND was determined by positron emission tomography (PET) using (18)F-flumazenil as a radioligand. T1-weighted structural magnetic resonance imaging scans were also acquired for PET scan co-registration, in order to perform a region of interest analysis using the pons as a reference region. Compared to socially dominant females, subordinate females exhibited increased GABAAR BPND in the prefrontal cortex but not in the temporal lobe or the hypothalamus. Administration of astressin B eliminated the status difference in GABAAR BPND in the prefrontal cortex, suggesting that the chronic stressor of social subordination modulates GABAergic tone via effects on CRH and the LHPA axis, at least in prefrontal regions.Persistent exposure to environmental stressors causes dysregulation of the limbic-hypothalamic-pituitary-adrenal (LHPA) axis and alters GABAA receptor (GABAAR) levels throughout the brain. Social subordination in socially housed female rhesus results in distinctive stress-related physiological and behavioral phenotypes that are dependent on the ovarian hormone estradiol (E2). In the present study, we utilized ovariectomized adult female rhesus monkeys undergoing hormone replacement with E2 to test the hypothesis that the chronic psychosocial stress of subordination alters GABAAR binding potential (GABAAR BPND) in limbic regions implicated in emotional processing including the prefrontal cortex, temporal lobe (amygdala and hippocampus), and hypothalamus. Furthermore, we tested the hypothesis that peripheral administration of a corticotropin-releasing hormone (CRH) receptor antagonist (astressin B) would reverse the alterations in GABAAR binding within these regions in subordinate females. After subjects received astressin B or saline for three consecutive days, GABAAR BPND was determined by positron emission tomography (PET) using (18)F-flumazenil as a radioligand. T1-weighted structural magnetic resonance imaging scans were also acquired for PET scan co-registration, in order to perform a region of interest analysis using the pons as a reference region. Compared to socially dominant females, subordinate females exhibited increased GABAAR BPND in the prefrontal cortex but not in the temporal lobe or the hypothalamus. Administration of astressin B eliminated the status difference in GABAAR BPND in the prefrontal cortex, suggesting that the chronic stressor of social subordination modulates GABAergic tone via effects on CRH and the LHPA axis, at least in prefrontal regions. Persistent exposure to environmental stressors causes dysregulation of the limbic-hypothalamic-pituitary-adrenal (LHPA) axis and alters GABAA receptor (GABAAR) levels throughout the brain. Social subordination in socially housed female rhesus results in distinctive stress-related physiological and behavioral phenotypes that are dependent on the ovarian hormone estradiol (E2). In the present study, we utilized ovariectomized adult female rhesus monkeys undergoing hormone replacement with E2 to test the hypothesis that the chronic psychosocial stress of subordination alters GABAAR binding potential (GABAAR BPND) in limbic regions implicated in emotional processing including the prefrontal cortex, temporal lobe (amygdala and hippocampus), and hypothalamus. Furthermore, we tested the hypothesis that peripheral administration of a corticotropin-releasing hormone (CRH) receptor antagonist (astressin B) would reverse the alterations in GABAAR binding within these regions in subordinate females. After subjects received astressin B or saline for three consecutive days, GABAAR BPND was determined by positron emission tomography (PET) using 18F-flumazenil as a radioligand. T1-weighted structural magnetic resonance imaging scans were also acquired for PET scan co-registration, in order to perform a region of interest analysis using the pons as a reference region. Compared to socially dominant females, subordinate females exhibited increased GABAAR BPND in the prefrontal cortex but not in the temporal lobe or the hypothalamus. Administration of astressin B eliminated the status difference in GABAAR BPND in the prefrontal cortex, suggesting that the chronic stressor of social subordination modulates GABAergic tone via effects on CRH and the LHPA axis, at least in prefrontal regions. Persistent exposure to environmental stressors causes dysregulation of the limbic-hypothalamic-pituitary-adrenal (LHPA) axis and alters GABAA receptor (GABAAR) levels throughout the brain. Social subordination in socially housed female rhesus results in distinctive stress-related physiological and behavioral phenotypes that are dependent on the ovarian hormone estradiol (E2). In the present study, we utilized ovariectomized adult female rhesus monkeys undergoing hormone replacement with E2 to test the hypothesis that the chronic psychosocial stress of subordination alters GABAAR binding potential (GABAAR BPND) in limbic regions implicated in emotional processing including the prefrontal cortex, temporal lobe (amygdala and hippocampus), and hypothalamus. Furthermore, we tested the hypothesis that peripheral administration of a corticotropin-releasing hormone receptor (CRHR) antagonist (astressin B) would reverse the alterations in GABAAR binding within these regions in subordinate females. After subjects received astressin B or saline for three consecutive days, GABAAR BPND was determined by positron emission tomography (PET) using 18F-flumazenil as a radioligand. T1-weighted structural MRI scans were also acquired for PET scan co-registration, in order to perform a region of interest analysis using the pons as a reference region. Compared to socially dominant females, subordinate females exhibited increased GABAAR BPND in the prefrontal cortex but not in the temporal lobe or the hypothalamus. Administration of astressin B eliminated the status difference in GABAAR BPND in the prefrontal cortex, suggesting that the chronic stressor of social subordination modulates GABAergic tone via effects on CRH and the LHPA axis, at least in prefrontal regions. Highlights • Social subordination alters GABAA Rs binding in estradiol-treated female monkeys. • Status effect on GABAA R is site specific, only seen in the prefrontal cortex. • CRH receptor antagonism reverses status differences in GABAA R binding. • Implicates the stress axis in the dysregulation of GABAA R in subordinate females. • Provides mechanism by which subordination alters the actions of estradiol. Persistent exposure to environmental stressors causes dysregulation of the limbic-hypothalamic-pituitary-adrenal (LHPA) axis and alters GABAA receptor (GABAAR) levels throughout the brain. Social subordination in socially housed female rhesus results in distinctive stress-related physiological and behavioral phenotypes that are dependent on the ovarian hormone estradiol (E2). In the present study, we utilized ovariectomized adult female rhesus monkeys undergoing hormone replacement with E2 to test the hypothesis that the chronic psychosocial stress of subordination alters GABAAR binding potential (GABAAR BPND) in limbic regions implicated in emotional processing including the prefrontal cortex, temporal lobe (amygdala and hippocampus), and hypothalamus. Furthermore, we tested the hypothesis that peripheral administration of a corticotropin-releasing hormone (CRH) receptor antagonist (astressin B) would reverse the alterations in GABAAR binding within these regions in subordinate females. After subjects received astressin B or saline for three consecutive days, GABAAR BPND was determined by positron emission tomography (PET) using (18)F-flumazenil as a radioligand. T1-weighted structural magnetic resonance imaging scans were also acquired for PET scan co-registration, in order to perform a region of interest analysis using the pons as a reference region. Compared to socially dominant females, subordinate females exhibited increased GABAAR BPND in the prefrontal cortex but not in the temporal lobe or the hypothalamus. Administration of astressin B eliminated the status difference in GABAAR BPND in the prefrontal cortex, suggesting that the chronic stressor of social subordination modulates GABAergic tone via effects on CRH and the LHPA axis, at least in prefrontal regions. |
| Author | Michopoulos, V. Votaw, J.R. Reding, K. Toufexis, D. Goodman, M.M. Wilson, M.E. Berga, S.L. Embree, M. Rivier, J. Voll, R.J. Sanchez, M.M. |
| AuthorAffiliation | 2 Division of Developmental & Cognitive Neuroscience, Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA 5 Imaging Core, Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA 7 Department of Obstetrics &, Wake Forest University School of Medicine, Winston-Salem, NC, USA 6 The Clayton Foundation Laboratories for Peptide Biology, The Salk Institute, La Jolla, CA, USA 1 Department of Psychiatry & Behavioral Sciences, School of Medicine, Emory University, Atlanta, GA, United States 3 Department of Psychology, University of Vermont, Burlington VT, USA 4 Department of Radiology and Imaging Sciences, School of Medicine, Emory University, Atlanta, GA, USA |
| AuthorAffiliation_xml | – name: 2 Division of Developmental & Cognitive Neuroscience, Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA – name: 1 Department of Psychiatry & Behavioral Sciences, School of Medicine, Emory University, Atlanta, GA, United States – name: 6 The Clayton Foundation Laboratories for Peptide Biology, The Salk Institute, La Jolla, CA, USA – name: 3 Department of Psychology, University of Vermont, Burlington VT, USA – name: 4 Department of Radiology and Imaging Sciences, School of Medicine, Emory University, Atlanta, GA, USA – name: 5 Imaging Core, Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA – name: 7 Department of Obstetrics &, Wake Forest University School of Medicine, Winston-Salem, NC, USA |
| Author_xml | – sequence: 1 givenname: V. surname: Michopoulos fullname: Michopoulos, V. email: vmichop@emory.edu organization: Department of Psychiatry & Behavioral Sciences, School of Medicine, Emory University, Atlanta, GA, United States – sequence: 2 givenname: M. surname: Embree fullname: Embree, M. organization: Division of Developmental & Cognitive Neuroscience, Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA – sequence: 3 givenname: K. surname: Reding fullname: Reding, K. organization: Division of Developmental & Cognitive Neuroscience, Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA – sequence: 4 givenname: M.M. surname: Sanchez fullname: Sanchez, M.M. organization: Department of Psychiatry & Behavioral Sciences, School of Medicine, Emory University, Atlanta, GA, United States – sequence: 5 givenname: D. surname: Toufexis fullname: Toufexis, D. organization: Division of Developmental & Cognitive Neuroscience, Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA – sequence: 6 givenname: J.R. surname: Votaw fullname: Votaw, J.R. organization: Department of Radiology and Imaging Sciences, School of Medicine, Emory University, Atlanta, GA, USA – sequence: 7 givenname: R.J. surname: Voll fullname: Voll, R.J. organization: Department of Radiology and Imaging Sciences, School of Medicine, Emory University, Atlanta, GA, USA – sequence: 8 givenname: M.M. surname: Goodman fullname: Goodman, M.M. organization: Division of Developmental & Cognitive Neuroscience, Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA – sequence: 9 givenname: J. surname: Rivier fullname: Rivier, J. organization: The Clayton Foundation Laboratories for Peptide Biology, The Salk Institute, La Jolla, CA, USA – sequence: 10 givenname: M.E. surname: Wilson fullname: Wilson, M.E. organization: Division of Developmental & Cognitive Neuroscience, Yerkes National Primate Research Center, Emory University, Atlanta, GA, USA – sequence: 11 givenname: S.L. surname: Berga fullname: Berga, S.L. organization: Department of Obstetrics & Gynecology, Wake Forest University School of Medicine, Winston-Salem, NC, USA |
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| Keywords | ROIs stress MR MRI YNPRC PVN GAD GR FOV E2 LHPA CRHR1/2 GABAAR monkeys BNST social subordination CRH astressin B BPND LH flumazenil GABAA receptor PET magnetic resonance imaging GABA A receptor BP ND binding potential GABA AR estradiol Yerkes National Primate Research Center corticotropin-releasing hormone glucocorticoid regions of interest field of view luteinizing hormone limbic–hypothalamic–pituitary–adrenal mineralocorticoid glutamic acid decarboxylase bed nucleus of the stria terminalis CRH receptor type 1 and type 2 positron emission tomography paraventricular nucleus Ovariectomy Estrogen Monkey Estradiol Ovarian hormone Stress Vertebrata Flumazenil Mammalia CRF receptor Primates Female Sex steroid hormone Gabaergic receptor A BP(ND) GABA(A)R GABA(A) receptor |
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| Snippet | •Social subordination alters GABAARs binding in estradiol-treated female monkeys.•Status effect on GABAAR is site specific, only seen in the prefrontal... Highlights • Social subordination alters GABAA Rs binding in estradiol-treated female monkeys. • Status effect on GABAA R is site specific, only seen in the... Persistent exposure to environmental stressors causes dysregulation of the limbic-hypothalamic-pituitary-adrenal (LHPA) axis and alters GABAA receptor (GABAAR)... Persistent exposure to environmental stressors causes dysregulation of the limbic-hypothalamic-pituitary-adrenal (LHPA) axis and alters GABAA receptor (GABAAR)... |
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| SubjectTerms | Animals astressin B Biological and medical sciences Brain - diagnostic imaging Brain Mapping Corticotropin-Releasing Hormone - pharmacology Dominance-Subordination Estradiol - pharmacology Female flumazenil Flumazenil - analogs & derivatives Fundamental and applied biological sciences. Psychology GABAA receptor Image Processing, Computer-Assisted Macaca mulatta Magnetic Resonance Imaging monkeys Neurology Ovariectomy Peptide Fragments - pharmacology Positron-Emission Tomography Radiopharmaceuticals Receptors, Corticotropin-Releasing Hormone - antagonists & inhibitors Receptors, GABA-A - metabolism social subordination stress Vertebrates: nervous system and sense organs |
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| Title | CRH receptor antagonism reverses the effect of social subordination upon central GABAA receptor binding in estradiol-treated ovariectomized female rhesus monkeys |
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