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The role of amygdala nuclei in the expression of auditory signaled two-way active avoidance in rats.

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Choi, June-Seek, Cain, Christopher K., LeDoux, Joseph E.·2010·Learning & Memory
DOI 10.1101/lm.1676610PMC PMC2832923
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Abstract

Using a two-way signaled active avoidance (2-AA) learning procedure, where rats were trained in a shuttle box to avoid a footshock signaled by an auditory stimulus, we tested the contributions of the lateral (LA), basal (B), and central (CE) nuclei of the amygdala to the expression of instrumental active avoidance conditioned responses (CRs). Discrete or combined lesions of the LA and B, performed after the rats had reached an asymptotic level of avoidance performance, produced deficits in the CR, whereas CE lesions had minimal effect. Fiber-sparing excitotoxic lesions of the LA/B produced by infusions of N-methyl-d-aspartate (NMDA) also impaired avoidance performance, confirming that neurons in the LA/B are involved in mediating avoidance CRs. In a final series of experiments, bilateral electrolytic lesions of the CE were performed on a subgroup of animals that failed to acquire the avoidance CR after 3 d of training. CE lesions led to an immediate rescue of avoidance learning, suggesting that activity in CE was inhibiting the instrumental CR. Taken together, these results indicate that the LA and B are essential for the performance of a 2-AA response. The CE is not required, and may in fact constrain the instrumental avoidance response by mediating the generation of competing Pavlovian responses, such as freezing.

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Crossref · 10.1101/lm.1676610

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  • All defense responses in the animal model of the defense cascade-arousal, freezing, flight or fight, tonic immobility, collapsed immobility, and quiescent immobility-are responses to threat mediated by neural circuits involving the extended amygdala, hypothalamus, periaqueductal gray, ventral pontine tegmentum, ventral and dorsal medulla, and spinal cord.

    “All defense responses in the animal model of the defense cascade—arousal, freezing, flight or fight, tonic immobility, collapsed immobility, and quiescent immobility—are responses to threat mediated by neural circuits involving the extended amygdala, hypothalamus, periaqueductal gray (PAG), ventral pontine tegmentum, ventral and dorsal medulla, and spinal cord.22–25”

    From Fear and the Defense Cascade (2015) · cites this paper as [22]

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  • Depending on the degree of threat and the distance between predator and prey, distinct animal defense responses-freezing, flight or fight, tonic immobility, and quiescent immobility-proceed sequentially along a continuum termed the defense cascade.

    “Subsequent research with animals determined that, depending on the degree of threat and the distance between the predator and prey, distinct responses—freezing, flight or fight, tonic immobility, and quiescent immobility—proceed sequentially along a continuum, termed the defense cascade.”

    From Fear and the Defense Cascade (2015) · cites this paper as [9]

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  • The order of the human defense cascade differs from conceptualizations based on the distance of the predatory threat, in which freezing is discussed before flight or fight.

    “This order differs from conceptualizations based on the distance of the predatory threat—in which freezing is discussed before flight or fight.2,8,9,17”

    From Fear and the Defense Cascade (2015) · cites this paper as [9]

    The Discussion describes freezing as interfering with active avoidance in rats, but it does not describe a defense cascade ordered by distance from a predator. Searches for predatory-threat distance and freezing before flight or fight found no passage addressing that ordering; the cited claim cannot be verified from our copy. (LLM, conf=0.74)

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Research works printed but not linked: 7

  1. Cain CK, LeDoux JE. 2008b. Brain mechanisms of Pavlovian and instrumental aversive conditioning. In Handbook of anxiety and fear (ed. DJ Nutt et al.), pp. 103 -125. Elsevier Academic Press, Amsterdam, The Netherlands.
  2. Gray JA. 1975. Elements of a two-process theory of learning. Academic Press, New York.
  3. Kapp BS, Pascoe JP, Bixler MA. 1984. The amygdala a neuroanatomical systems approach to its contributions to aversive conditioning. In Neuropsychology of memory (ed. N Buttlers, LR Squire), pp. 473 -488.
  4. Levis DJ. 1989. The case for a return to a two-factor theory of avoidance: The failure of non-fear interpretations. In Contemporary learning theories: Pavlovian conditioning and the status of traditional learning theory (ed. SB Klein, RR Mowrer), pp. 227 -277.
  5. McAllister WR, McAllister DE. 1971. Behavioral measurement of conditioned fear. In Aversive conditioning and learning (ed. FR Brush), pp. 105 -179. Academic Press, New York.
  6. McAllister DE, McAllister WR. 1991. Fear theory and aversively motivated behavior: Some controversial issues. In Fear, avoidance, and phobias: A fundamental analysis (ed. MR Denny), pp. 135 -163. Erlbaum, Hillsdale, NJ.
  7. Paxinos G, Watson C. 1998. The rat brain. Academic Press, San Diego, CA.

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Authors
Choi, J.-S., Cain, C. K., & LeDoux, J. E.
Affiliations
  • New York University (US)
  • Nathan Kline Institute for Psychiatric Research (US)
ORCID
Venue
Learning & Memory
Publisher
Cold Spring Harbor Laboratory
Published
2010-02-26
Volume
17
Issue
3
Pages
139-147
ISSN
  • 1072-0502 (ISSN-L)
  • 1549-5485
DOI
10.1101/lm.1676610
PMC
PMC2832923
OpenAlex
W2169214568
Cited by
187
References
78
Citations by year
2026: 6 · 2025: 8 · 2024: 16 · 2023: 10 · 2022: 7 · 2021: 16 · 2020: 14 · 2019: 12 · 2018: 15 · 2017: 12 · 2016: 12 · 2015: 15 · 2014: 16 · 2013: 11 · 2012: 6
Type
posted content
Language
en
Open access
Locations
  • Learning & Memory (publishedVersion)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Science Foundation (0920153)
  • National Research Foundation
  • National Research Foundation of Korea
  • National Institutes of Health (1f32mh077458-01)
  • National Institute of Mental Health (R37MH038774, R01MH038774, R32 MH38774, MH38774, F32-MH077458)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Keywords
amygdala, lateral amygdala, basal amygdala, central amygdala, avoidance conditioning, rats
MeSH terms
Acoustic Stimulation, Amygdala, Analysis of Variance, Animals, Association Learning, Avoidance Learning, Behavior, Animal, Conditioning, Classical, Electrolysis, Vocalization, Animal, Rats, Sprague-Dawley, Rats

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