ACh signaling modulates activity of the GABAergic signaling network in the basolateral amygdala and behavior in stress-relevant paradigms
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Abstract
The balance between excitatory and inhibitory (E/I) signaling is important for maintaining homeostatic function in the brain. Indeed, dysregulation of inhibitory GABA interneurons in the amygdala has been implicated in human mood disorders. We hypothesized that acetylcholine (ACh) signaling in the basolateral amygdala (BLA) might alter E/I balance resulting in changes in stress-sensitive behaviors. We therefore measured ACh release as well as activity of calmodulin-dependent protein kinase II (CAMKII)-, parvalbumin (PV)-, somatostatin (SOM)- and vasoactive intestinal protein (VIP)-expressing neurons in the BLA of awake, behaving male mice. ACh levels and activity of both excitatory and inhibitory BLA neurons increased when animals were actively coping, and decreased during passive coping, in the light-dark box, tail suspension and social defeat. Changes in neuronal activity preceded behavioral state transitions, suggesting that BLA activity may drive the shift in coping strategy. In contrast to exposure to escapable stressors, prolonging ACh signaling with a cholinesterase antagonist changed the balance of activity among BLA cell types, significantly increasing activity of VIP neurons and decreasing activity of SOM cells, with little effect on CaMKII or PV neurons. Knockdown of α7 or β2-containing nAChR subtypes in PV and SOM, but not CaMKII or VIP, BLA neurons altered behavioral responses to stressors, suggesting that ACh signaling through nAChRs on GABA neuron subtypes contributes to stress-induced changes in behavior. These studies show that ACh modulates the GABAergic signaling network in the BLA, shifting the balance between SOM, PV, VIP and CaMKII neurons, which are normally activated coordinately during active coping in response to stress. Thus, prolonging ACh signaling, as occurs in response to chronic stress, may contribute to maladaptive behaviors by shifting the balance of inhibitory signaling in the BLA.
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VIP modulates numerous social behaviors including aggression and stress coping during social stressors like defeat stress.
“VIP modulates numerous social behaviors including aggression [74] as well as stress coping during social stressors like defeat stress [75].”
From Rapid changes in plasma corticosterone and medial amygdala transcriptome profiles during social status change reveal molecular pathways associated with a major life history transition in mouse dominance hierarchies (2025) · cites this paper as [75]
The Results (page not provided) report increased activity of VIP-expressing BLA neurons when mice approached an aggressor after social defeat, linking those neurons to a social stress paradigm. But increased activity does not establish that VIP modulates stress-coping behavior; the knockdown Results report no significant behavioral change from nAChR knockdown in VIP neurons. The aggression clause is attached to a different citation and is not assessed here. (LLM, conf=0.85)
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- Authors
- Mineur, Y. S., Mose, T. N., Maibom, K. L., Pittenger, S. T., Soares, A. R., Wu, H., Taylor, S. R., Huang, Y., & Picciotto, M. R.
- Affiliations
- Yale University (US)
- Vanderbilt University (US)
- Corresponding author
- Picciotto, Marina R.
- ORCID
- Venue
- Molecular Psychiatry
- Published
- 2022-09-01
- Volume
- 27
- Issue
- 12
- Pages
- 4918-4927
- ISSN
- 1359-4184 (ISSN-L)
- 1476-5578
- PMC
- PMC10718266
- OpenAlex
- W4294084859
- Cited by
- 36
- References
- 62
- Citations by year
- 2026: 7 · 2025: 12 · 2024: 11 · 2023: 5 · 2022: 1
- FWCI
- 3.21
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Licence
- Locations
- Molecular Psychiatry (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Department of Health & Human Services | NIH | National Institute of Mental Health (MH077681, MH105824)
- U.S. Department of Health & Human Services | NIH | National Institute on Drug Abuse (DA033945)
- U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (NS041228)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- acetylcholine signaling, basolateral amygdala, GABAergic interneurons, excitation-inhibition balance, stress coping, social defeat, tail suspension test, nicotinic acetylcholine receptors, parvalbumin interneurons, somatostatin interneurons, vasoactive intestinal peptide neurons, chronic stress, mood disorders, neuronal activity
- MeSH terms
- Acetylcholine, Amygdala, Animals, Interneurons, Male, Neurons, Stress, Psychological, Signal Transduction, Mice, Calcium-Calmodulin-Dependent Protein Kinase Type 2, GABAergic Neurons, Basolateral Nuclear Complex
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