Active Avoidance Requires a Serial Basal Amygdala to Nucleus Accumbens Shell Circuit
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Freezing is a species-typical defensive reaction to conditioned threats. While the neural circuitry of aversive Pavlovian behavior has been extensively studied, less is known about the circuitry underlying more active responses to danger. Here we show that the flow of information between the basal amygdala (BA) and the nucleus accumbens (NAcc) is necessary for signaled active avoidance behavior. Rats trained to avoid shock by shuttling during an auditory conditioned stimulus showed increased expression of the activity-dependent protein c-Fos in the NAcc, specifically the shell subregion (NAccSh). Silencing neural activity in the NAccSh, but not in the adjacent NAcc core, disrupted avoidance behavior. Disconnection of the BA and the NAccSh was just as effective at disrupting avoidance behavior as bilateral NAccSh inactivations, suggesting learned avoidance behavior requires an intact BA-NAccSh circuit. Together, these data highlight an essential role for the amygdalar projection to the ventral striatum in aversively motivated actions.
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The vmPFC toggles between amygdala output paths, shifting information flow to promote aversively motivated action instead of Pavlovian freezing responses.
“The vmPFC is proposed to toggle between these different output paths of the amygdala, shifting the flow of information to promote aversively motivated action instead of Pavlovian freezing responses (Moscarello and LeDoux, 2013; Ramirez et al., 2015).”
From Active avoidance: Neural mechanisms and attenuation of pavlovian conditioned responding (2017) · cites this paper as Ramirez et al., 2015
The Discussion (page not provided) describes separate amygdala outputs for freezing and avoidance and suggests a mechanism that toggles between these behaviors. It also proposes that infralimbic prefrontal cortex could suppress freezing, but does not specifically say that it toggles information flow between the two amygdala output paths. (LLM, conf=0.83)
Experimental — accuracy not yet measuredThe lateral nucleus projects to the basal nucleus of the amygdala, which projects to the striatum, and these connections are essential for avoidance learning.
“The lateral nucleus also projects to the basal nucleus of the amygdala, which projects to the striatum. These connections are essential for avoidance learning (Amorapanth et al., 2000; Ramirez et al., 2015).”
From Active avoidance: Neural mechanisms and attenuation of pavlovian conditioned responding (2017) · cites this paper as Ramirez et al., 2015
The Introduction describes information passing from the lateral to the basal amygdala and identifies a basal-amygdala projection to the nucleus accumbens, a region of the ventral striatum. The Results section, “Disconnection of NAccSh and BA during SigAA impairs avoidance responding,” finds that the basal-amygdala–accumbens-shell circuit is required for the expression of learned avoidance behavior in rats. It does not establish that both connections are essential for avoidance learning itself. (LLM, conf=0.86)
Experimental — accuracy not yet measuredInstrumental control over threat involves the amygdala, striatum, and ventromedial prefrontal cortex in rodents.
“Instrumental control over threat has been shown to involve the amygdala, striatum, and ventromedial prefrontal cortex (vmPFC) in rodents.”
From Active avoidance: Neural mechanisms and attenuation of pavlovian conditioned responding (2017) · cites this paper as Ramirez et al., 2015
The basal nucleus of the amygdala is engaged during avoidance learning and may transfer information about CS-US association to the striatum.
“However, the basal nucleus of the amygdala is engaged during avoidance learning and may transfer information about CS-US association to the striatum (Amorapanth et al., 2000; Ramirez et al., 2015).”
From Active avoidance: Neural mechanisms and attenuation of pavlovian conditioned responding (2017) · cites this paper as Ramirez et al., 2015
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- Authors
- Ramirez, F., Moscarello, J. M., LeDoux, J. E., & Sears, R. M.
- Affiliations
- New York University (US)
- Nathan Kline Institute for Psychiatric Research (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2015-02-25
- Volume
- 35
- Issue
- 8
- Pages
- 3470-3477
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC4339356
- OpenAlex
- W2091209465
- Cited by
- 198
- References
- 58
- Citations by year
- 2026: 14 · 2025: 14 · 2024: 16 · 2023: 18 · 2022: 15 · 2021: 25 · 2020: 21 · 2019: 25 · 2018: 17 · 2017: 14 · 2016: 11 · 2015: 8
- FWCI
- 10.02
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- Funders
- National Science Foundation (0920153)
- National Institute of Mental Health (R01 MH38774, R01MH038774, MH38774)
- National Institute on Drug Abuse (R01DA029053, R56DA029053)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- active avoidance, basal amygdala, nucleus accumbens shell, freezing behavior, auditory conditioned stimulus, shock avoidance, neural circuits, Fos expression, ventral striatum, neural silencing, circuit disconnection
- MeSH terms
- Amygdala, Animals, Avoidance Learning, Conditioning, Classical, Fear, Male, Neural Pathways, Nucleus Accumbens, Proto-Oncogene Proteins c-fos, Rats, Sprague-Dawley, Rats
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