Increased Basolateral Amygdala Pyramidal Cell Excitability May Contribute to the Anxiogenic Phenotype Induced by Chronic Early-Life Stress
Open accessAbstract
Adolescence represents a particularly vulnerable period during which exposure to stressors can precipitate the onset of psychiatric disorders and addiction. The basolateral amygdala (BLA) plays an integral role in the pathophysiology of anxiety and addiction. Acute and chronic stress promote increases in BLA pyramidal cell firing, and decreasing BLA excitability alleviates anxiety measures in humans and rodents. Notably, the impact of early-life stress on the mechanisms that govern BLA excitability is unknown. To address this gap in our knowledge, we used a rodent model of chronic early-life stress that engenders robust and enduring increases in anxiety-like behaviors and ethanol intake and examined the impact of this model on the intrinsic excitability of BLA pyramidal cells. Adolescent social isolation was associated with a significant increase in the intrinsic excitability of BLA pyramidal cells and a blunting of the medium component of the afterhyperpolarization potential, a voltage signature of calcium-activated potassium (Kca) channel activity. Western blot analysis revealed reduced expression of small-conductance Kca (SK) channel protein in the BLA of socially isolated (SI) rats. Bath application of a positive SK channel modulator (1-EBIO) normalized firing in ex vivo recordings from SI rats, and in vivo intra-BLA 1-EBIO infusion reduced anxiety-like behaviors. These findings reveal that chronic adolescent stress impairs SK channel function, which contributes to an increase in BLA pyramidal cell excitability and highlights BLA SK channels as promising targets for the treatment of anxiety disorders and comorbid addiction. SIGNIFICANCE STATEMENT: Although anxiety disorders and alcohol addiction frequently co-occur, the mechanisms that contribute to this comorbidity are poorly understood. Here, we used a rodent early-life stress model that leads to robust and longlasting increases in behaviors associated with elevated risk of anxiety disorders and addiction to identify novel neurobiological substrates that may underlie these behaviors. Our studies focused on the primary output neurons of the basolateral amygdala, a brain region that plays a key role in anxiety and addiction. We discovered that early-life stress decreases the activity of a specific class of potassium channels and increases the intrinsic excitability of BLA neurons and present evidence that enhancing the function of these channels normalizes BLA excitability and attenuates anxiety-like behaviors.
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The BLA is generally hyperactive following chronic stress.
“The stress-induced attenuation of BLA→DMS activity was surprising because the BLA is, generally, hyperactive following chronic stress54–61 (c.f.62).”
From A dual-pathway architecture for stress to disrupt agency and promote habit (2025) · cites this paper as [58]
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- Authors
- Rau, A. R., Chappell, A. M., Butler, T. R., Ariwodola, O. J., & Weiner, J. L.
- Affiliations
- Wake Forest University (US)
- University of Dayton (US)
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2015-07-01
- Volume
- 35
- Issue
- 26
- Pages
- 9730-9740
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC4571506
- OpenAlex
- W1903965668
- Cited by
- 136
- References
- 77
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 14 · 2023: 17 · 2022: 12 · 2021: 14 · 2020: 13 · 2019: 12 · 2018: 12 · 2017: 11 · 2016: 15
- FWCI
- 5.91
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute on Alcohol Abuse and Alcoholism (R01AA017531, P01AA021099, F31AA022046, R37AA010422, R01AA010422, R37AA017531)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- basolateral amygdala, adolescent social isolation, anxiety-like behavior, small conductance calcium-activated potassium channels, 1-EBIO, afterhyperpolarization, ethanol consumption, intrinsic excitability
- MeSH terms
- Germinal Center Kinases, Action Potentials, Age Factors, Analysis of Variance, Animals, Animals, Newborn, Benzimidazoles, Calcium Channel Agonists, Disease Models, Animal, Male, Microinjections, Social Isolation, Stress, Psychological, Protein Serine-Threonine Kinases, Pyramidal Cells, Patch-Clamp Techniques, Rats, Long-Evans, Rats, Small-Conductance Calcium-Activated Potassium Channels, Basolateral Nuclear Complex, In Vitro Techniques
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