Sex‐specific plasticity in CRF regulation of inhibitory control in central amygdala CRF1 neurons after chronic voluntary alcohol drinking

Agoglia, Abigail E.; Zhu, Manhua; Quadir, Sema G.; Bluitt, Maya N.; Douglass, Eliza; Hanback, T. D.; Tella, Jyoshitha; Ying, Rose; Hodge, Clyde W.; Herman, Melissa A.

doi:10.1111/adb.13067

Cited by 12 publications

(9 citation statements)

References 54 publications

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“…Furthermore, in a study using transgenic CRF 1 reporter mice, voluntary alcohol drinking increased the sensitivity of CRF 1 -positive neurons in the CeA to the effects of acute alcohol in males but not females. In contrast, alcohol drinking increased acute CRF sensitivity of these neurons in both males and females [ 37 ]. Tonic CRF activity was also found to be sexually dimorphic, as the CRF 1 antagonist R121919 decreased GABA release in water and alcohol-drinking females, but not in either male group [ 37 ].…”

Section: Discussionmentioning

confidence: 99%

“…In contrast, alcohol drinking increased acute CRF sensitivity of these neurons in both males and females [ 37 ]. Tonic CRF activity was also found to be sexually dimorphic, as the CRF 1 antagonist R121919 decreased GABA release in water and alcohol-drinking females, but not in either male group [ 37 ]. A study by Retson and colleagues also reported sex differences in the CRF system of the rat CeA, which found that alcohol drinking activated CeA CRF neurons and enhanced the response of these neurons to stress selectively in male but not female rats [ 38 ].…”

Section: Discussionmentioning

confidence: 99%

“…However, another important factor to consider is the composition of the cell population being studied, which can be associated with distinct responses. For instance, the Agoglia et al study specifically targeted CRF 1 + neurons in mice [ 37 ], while our electrophysiology data come from neurons of unknown CRF 1 expression in rats. As our in situ hybridization data show, naïve females have fewer GABAergic neurons expressing CRF 1 .…”

Section: Discussionmentioning

confidence: 99%

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Alcohol Dependence Induces CRF Sensitivity in Female Central Amygdala GABA Synapses

Rodriguez

Kirson

Wolfe

et al. 2022

IJMS

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Alcohol use disorder (AUD) is a chronically relapsing disease characterized by loss of control in seeking and consuming alcohol (ethanol) driven by the recruitment of brain stress systems. However, AUD differs among the sexes: men are more likely to develop AUD, but women progress from casual to binge drinking and heavy alcohol use more quickly. The central amygdala (CeA) is a hub of stress and anxiety, with corticotropin-releasing factor (CRF)-CRF1 receptor and Gamma-Aminobutyric Acid (GABA)-ergic signaling dysregulation occurring in alcohol-dependent male rodents. However, we recently showed that GABAergic synapses in female rats are less sensitive to the acute effects of ethanol. Here, we used patch-clamp electrophysiology to examine the effects of alcohol dependence on the CRF modulation of rat CeA GABAergic transmission of both sexes. We found that GABAergic synapses of naïve female rats were unresponsive to CRF application compared to males, although alcohol dependence induced a similar CRF responsivity in both sexes. In situ hybridization revealed that females had fewer CeA neurons containing mRNA for the CRF1 receptor (Crhr1) than males, but in dependence, the percentage of Crhr1-expressing neurons in females increased, unlike in males. Overall, our data provide evidence for sexually dimorphic CeA CRF system effects on GABAergic synapses in dependence.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Alcohol Dependence Induces CRF Sensitivity in Female Central Amygdala GABA Synapses

Rodriguez

Kirson

Wolfe

et al. 2022

IJMS

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“…The study did not find any statistically significant sex differences but suggested that acute alcohol reduces GABA release onto CRF1R+ neurons in males and not in females ( Agoglia et al, 2020 ). The same group followed up on these experiments and saw that voluntary alcohol drinking through the two-bottle choice paradigm led to an increase in presynaptic spontaneous GABAergic transmission in CRF1R+ neurons in the CeA in males only, with no changes in females and no sex differences in postsynaptic activity ( Agoglia et al, 2022 ). It is worth noting that there were no sex or treatment group (water or alcohol) differences in baseline GABA activity.…”

Section: Gabaergic Transmissionmentioning

confidence: 99%

Subregional Differences in Alcohol Modulation of Central Amygdala Neurocircuitry

Melkumyan

Silberman

2022

Front. Mol. Neurosci.

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Alcohol use disorder is a highly significant medical condition characterized by an impaired ability to stop or control alcohol use, compulsive alcohol seeking behavior, and withdrawal symptoms in the absence of alcohol. Understanding how alcohol modulates neurocircuitry critical for long term and binge-like alcohol use, such as the central amygdala (CeA), may lead to the development of novel therapeutic strategies to treat alcohol use disorder. In clinical studies, reduction in the volume of the amygdala has been linked with susceptibility to relapse to alcohol use. Preclinical studies have shown the involvement of the CeA in the effects of alcohol use, with lesions of the amygdala showing a reduction in alcohol drinking, and manipulations of cells in the CeA altering alcohol drinking. A great deal of work has shown that acute alcohol, as well as chronic alcohol exposure via intake or dependence models, alters glutamatergic and GABAergic transmission in the CeA. The CeA, however, contains heterogeneous cell populations and distinct subregional differences in neurocircuit architecture which may influence the mechanism by which alcohol modulates CeA function overall. The current review aimed to parse out the differences in alcohol effects on the medial and lateral subregions of the CeA, and what role neuroinflammatory cells and markers, the endocannabinoid system, and the most commonly studied neuropeptide systems play in mediating these effects. A better understanding of alcohol effects on CeA subregional cell type and neurocircuit function may lead to development of more selective pharmacological interventions for alcohol use disorder.

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“…Human studies report that women are more likely to smoke to manage stress and experience anxiety more intensely during abstinence 16 . The corticotropin-releasing factor (CRF) system regulates stress responding and has been implicated in cocaine [17][18][19] , alcohol [20][21][22][23] , and nicotine addiction 24,25 . Nicotine activates the hypothalamic-pituitary-adrenal (HPA) axis to release CRF in the thalamus 26 .…”

Section: Introductionmentioning

confidence: 99%

Sex differences in the impact of electronic nicotine vapor on corticotropin-releasing factor receptor 1 neurons in the mouse ventral tegmental area

Zhu

Rogers

Jahad

et al. 2022

Preprint

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Nicotine engages dopamine neurons in the ventral tegmental area (VTA) to encode reward and drive the development of nicotine addiction, however how nicotine selectively alters other VTA populations remains to be determined. Here, we used male and female CRF1-GFP mice and nicotine vapor exposure to examine the effects of nicotine in VTA corticotropin-releasing factor receptor 1 (CRF1) neurons. We use immunohistochemistry and electrophysiology to examine neuronal activity, excitability, and inhibitory signaling. We found that VTA CRF1 neurons are mainly dopaminergic and project to the nucleus accumbens (VTA-NAcCRF1 neurons). VTA-NAcCRF1 neurons show greater phasic inhibition in naive females and greater focal nicotine-induced increases in firing in naive males. Following acute nicotine vapor exposure, phasic inhibition was not altered, but focal nicotine-induced tonic inhibition was enhanced in females and diminished in males. Acute nicotine vapor exposure did not affect firing in VTA-NAcCRF1 neurons, but females showed lower baseline firing and higher focal nicotine-induced firing. Activity (cFos) was increased in the CRF1 dopaminergic VTA population in both sexes, but with greater increases in females. Following chronic nicotine vapor exposure, both sexes displayed reduced basal phasic inhibition and the sex difference in tonic inhibition following acute vapor exposure was no longer observed. Additionally, activity of the CRF1 dopaminergic VTA population was no longer elevated in either sex. These findings reveal sex- and exposure-dependent changes in mesolimbic VTA-NAc CRF1 neuronal activity, inhibitory signaling, and nicotine sensitivity following nicotine vapor exposure. These changes potentially contribute to nicotine-dependent behaviors and the intersection between stress, anxiety, and addiction.

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Sex‐specific plasticity in CRF regulation of inhibitory control in central amygdala CRF1 neurons after chronic voluntary alcohol drinking

Cited by 12 publications

References 54 publications

Alcohol Dependence Induces CRF Sensitivity in Female Central Amygdala GABA Synapses

Alcohol Dependence Induces CRF Sensitivity in Female Central Amygdala GABA Synapses

Subregional Differences in Alcohol Modulation of Central Amygdala Neurocircuitry

Sex differences in the impact of electronic nicotine vapor on corticotropin-releasing factor receptor 1 neurons in the mouse ventral tegmental area

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