Forced Abstinence from Volitional Ethanol Intake Drives a Vulnerable Period of Hyperexcitability in BNST-Projecting Insular Cortex Neurons

The insular cortex (IC) integrates sensory and interoceptive cues to inform downstream circuitry executing adaptive behavioral responses. The IC communicates with areas involved canonically in stress and motivation. IC projections govern stress and ethanol recruitment of bed nucleus of the stria ter...

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Published inThe Journal of neuroscience Vol. 44; no. 4; p. e1121232023
Main Authors Taylor, Anne, Adank, Danielle N., Young, Phoebe A., Quan, Yizhen, Nabit, Brett P., Winder, Danny G.
Format Journal Article
LanguageEnglish
Published United States Society for Neuroscience 24.01.2024
Subjects
Abstinence
Animals
Cortex (insular)
Cortex (somatosensory)
Drinking
Drinking behavior
Electrophysiology
Emotional behavior
Ethanol
Ethanol - pharmacology
Excitability
Female
Gene expression
Homeostatic plasticity
Humans
Hybridization
Insular Cortex
Integrated circuits
Large-Conductance Calcium-Activated Potassium Channels - metabolism
Mice
Neurons
Neurons - physiology
Phenotypes
Potassium channels (calcium-gated)
Septal Nuclei - physiology
Stria terminalis
Sucrose
BNST
chronic ethanol
BK channels
insular cortex
Online AccessGet full text
ISSN0270-6474
1529-2401
1529-2401
DOI10.1523/JNEUROSCI.1121-23.2023

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Abstract The insular cortex (IC) integrates sensory and interoceptive cues to inform downstream circuitry executing adaptive behavioral responses. The IC communicates with areas involved canonically in stress and motivation. IC projections govern stress and ethanol recruitment of bed nucleus of the stria terminalis (BNST) activity necessary for the emergence of negative affective behaviors during alcohol abstinence. Here, we assess the impact of the chronic drinking forced abstinence (CDFA) volitional home cage ethanol intake paradigm on synaptic and excitable properties of IC neurons that project to the BNST (IC →BNST ). Using whole-cell patch-clamp electrophysiology, we investigated IC →BNST circuitry 24 h or 2 weeks following forced abstinence (FA) in female C57BL6/J mice. We find that IC →BNST cells are transiently more excitable following acute ethanol withdrawal. In contrast, in vivo ethanol exposure via intraperitoneal injection, ex vivo via ethanol wash, and acute FA from a natural reward (sucrose) all failed to alter excitability. In situ hybridization studies revealed that at 24 h post FA BK channel mRNA expression is reduced in IC. Further, pharmacological inhibition of BK channels mimicked the 24 h FA phenotype, while BK activation was able to decrease AP firing in control and 24 h FA subjects. All together these data suggest a novel mechanism of homeostatic plasticity that occurs in the IC →BNST circuitry following chronic drinking.
AbstractList The insular cortex (IC) integrates sensory and interoceptive cues to inform downstream circuitry executing adaptive behavioral responses. The IC communicates with areas involved canonically in stress and motivation. IC projections govern stress and ethanol recruitment of bed nucleus of the stria terminalis (BNST) activity necessary for the emergence of negative affective behaviors during alcohol abstinence. Here, we assess the impact of the chronic drinking forced abstinence (CDFA) volitional home cage ethanol intake paradigm on synaptic and excitable properties of IC neurons that project to the BNST (IC→BNST). Using whole-cell patch-clamp electrophysiology, we investigated IC→BNST circuitry 24 h or 2 weeks following forced abstinence (FA) in female C57BL6/J mice. We find that IC→BNST cells are transiently more excitable following acute ethanol withdrawal. In contrast, in vivo ethanol exposure via intraperitoneal injection, ex vivo via ethanol wash, and acute FA from a natural reward (sucrose) all failed to alter excitability. In situ hybridization studies revealed that at 24 h post FA BK channel mRNA expression is reduced in IC. Further, pharmacological inhibition of BK channels mimicked the 24 h FA phenotype, while BK activation was able to decrease AP firing in control and 24 h FA subjects. All together these data suggest a novel mechanism of homeostatic plasticity that occurs in the IC→BNST circuitry following chronic drinking.The insular cortex (IC) integrates sensory and interoceptive cues to inform downstream circuitry executing adaptive behavioral responses. The IC communicates with areas involved canonically in stress and motivation. IC projections govern stress and ethanol recruitment of bed nucleus of the stria terminalis (BNST) activity necessary for the emergence of negative affective behaviors during alcohol abstinence. Here, we assess the impact of the chronic drinking forced abstinence (CDFA) volitional home cage ethanol intake paradigm on synaptic and excitable properties of IC neurons that project to the BNST (IC→BNST). Using whole-cell patch-clamp electrophysiology, we investigated IC→BNST circuitry 24 h or 2 weeks following forced abstinence (FA) in female C57BL6/J mice. We find that IC→BNST cells are transiently more excitable following acute ethanol withdrawal. In contrast, in vivo ethanol exposure via intraperitoneal injection, ex vivo via ethanol wash, and acute FA from a natural reward (sucrose) all failed to alter excitability. In situ hybridization studies revealed that at 24 h post FA BK channel mRNA expression is reduced in IC. Further, pharmacological inhibition of BK channels mimicked the 24 h FA phenotype, while BK activation was able to decrease AP firing in control and 24 h FA subjects. All together these data suggest a novel mechanism of homeostatic plasticity that occurs in the IC→BNST circuitry following chronic drinking.
The insular cortex (IC) integrates sensory and interoceptive cues to inform downstream circuitry executing adaptive behavioral responses. The IC communicates with areas involved canonically in stress and motivation. IC projections govern stress and ethanol recruitment of bed nucleus of the stria terminalis (BNST) activity necessary for the emergence of negative affective behaviors during alcohol abstinence. Here, we assess the impact of the chronic drinking forced abstinence (CDFA) volitional home cage ethanol intake paradigm on synaptic and excitable properties of IC neurons that project to the BNST (IC→BNST). Using whole-cell patch-clamp electrophysiology, we investigated IC→BNST circuitry 24 h or 2 weeks following forced abstinence (FA) in female C57BL6/J mice. We find that IC→BNST cells are transiently more excitable following acute ethanol withdrawal. In contrast, in vivo ethanol exposure via intraperitoneal injection, ex vivo via ethanol wash, and acute FA from a natural reward (sucrose) all failed to alter excitability. In situ hybridization studies revealed that at 24 h post FA BK channel mRNA expression is reduced in IC. Further, pharmacological inhibition of BK channels mimicked the 24 h FA phenotype, while BK activation was able to decrease AP firing in control and 24 h FA subjects. All together these data suggest a novel mechanism of homeostatic plasticity that occurs in the IC→BNST circuitry following chronic drinking.
The insular cortex (IC) integrates sensory and interoceptive cues to inform downstream circuitry executing adaptive behavioral responses. The IC communicates with areas involved canonically in stress and motivation. IC projections govern stress and ethanol recruitment of bed nucleus of the stria terminalis (BNST) activity necessary for the emergence of negative affective behaviors during alcohol abstinence. Here, we assess the impact of the chronic drinking forced abstinence (CDFA) volitional home cage ethanol intake paradigm on synaptic and excitable properties of IC neurons that project to the BNST (IC →BNST ). Using whole-cell patch-clamp electrophysiology, we investigated IC →BNST circuitry 24 h or 2 weeks following forced abstinence (FA) in female C57BL6/J mice. We find that IC →BNST cells are transiently more excitable following acute ethanol withdrawal. In contrast, in vivo ethanol exposure via intraperitoneal injection, ex vivo via ethanol wash, and acute FA from a natural reward (sucrose) all failed to alter excitability. In situ hybridization studies revealed that at 24 h post FA BK channel mRNA expression is reduced in IC. Further, pharmacological inhibition of BK channels mimicked the 24 h FA phenotype, while BK activation was able to decrease AP firing in control and 24 h FA subjects. All together these data suggest a novel mechanism of homeostatic plasticity that occurs in the IC →BNST circuitry following chronic drinking.
The insular cortex (IC) integrates sensory and interoceptive cues to inform downstream circuitry executing adaptive behavioral responses. The IC communicates with areas involved canonically in stress and motivation. IC projections govern stress and ethanol recruitment of bed nucleus of the stria terminalis (BNST) activity necessary for the emergence of negative affective behaviors during alcohol abstinence. Here, we assess the impact of the chronic drinking forced abstinence (CDFA) volitional home cage ethanol intake paradigm on synaptic and excitable properties of IC neurons that project to the BNST (IC ). Using whole-cell patch-clamp electrophysiology, we investigated IC circuitry 24 h or 2 weeks following forced abstinence (FA) in female C57BL6/J mice. We find that IC cells are transiently more excitable following acute ethanol withdrawal. In contrast, in vivo ethanol exposure via intraperitoneal injection, ex vivo via ethanol wash, and acute FA from a natural reward (sucrose) all failed to alter excitability. In situ hybridization studies revealed that at 24 h post FA BK channel mRNA expression is reduced in IC. Further, pharmacological inhibition of BK channels mimicked the 24 h FA phenotype, while BK activation was able to decrease AP firing in control and 24 h FA subjects. All together these data suggest a novel mechanism of homeostatic plasticity that occurs in the IC circuitry following chronic drinking.
Author Winder, Danny G.
Nabit, Brett P.
Taylor, Anne
Quan, Yizhen
Young, Phoebe A.
Adank, Danielle N.
AuthorAffiliation 2 Vanderbilt Center for Addiction Research, Vanderbilt University , Nashville, Tennessee 37235
3 Department of Molecular Physiology and Biophysics, Vanderbilt University , Nashville, Tennessee 37235
4 Department of Pharmacology, Vanderbilt University , Nashville, Tennessee 37235
1 Vanderbilt Brain Institute, Vanderbilt University , Nashville, Tennessee 37235
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Keywords BNST
chronic ethanol
BK channels
insular cortex
Language English
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Author contributions: A.T., D.N.A., and D.G.W. designed research; A.T., D.N.A., P.A.Y., Y.Q., B.P.N and D.G.W. performed research; A.T., D.N.A., P.A.Y., Y.Q., B.P.N and D.G.W. analyzed data; A.T., D.N.A., and D.G.W. wrote the first draft of the paper; A.T., D.N.A., P.A.Y., and D.G.W. edited the paper; A.T., D.N.A., and D.G.W. wrote the paper.
National Institute on Alcohol Abuse and Alcoholism (R37AA019455, F31AA030901).
The authors declare no competing financial interests.
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Snippet The insular cortex (IC) integrates sensory and interoceptive cues to inform downstream circuitry executing adaptive behavioral responses. The IC communicates...
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StartPage e1121232023
SubjectTerms Abstinence
Animals
Cortex (insular)
Cortex (somatosensory)
Drinking
Drinking behavior
Electrophysiology
Emotional behavior
Ethanol
Ethanol - pharmacology
Excitability
Female
Gene expression
Homeostatic plasticity
Humans
Hybridization
Insular Cortex
Integrated circuits
Large-Conductance Calcium-Activated Potassium Channels - metabolism
Mice
Neurons
Neurons - physiology
Phenotypes
Potassium channels (calcium-gated)
Septal Nuclei - physiology
Stria terminalis
Sucrose
Title Forced Abstinence from Volitional Ethanol Intake Drives a Vulnerable Period of Hyperexcitability in BNST-Projecting Insular Cortex Neurons
URI https://www.ncbi.nlm.nih.gov/pubmed/38050120
https://www.proquest.com/docview/2918625171
https://www.proquest.com/docview/2898313473
https://pubmed.ncbi.nlm.nih.gov/PMC10860622
https://www.ncbi.nlm.nih.gov/pmc/articles/10860622
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