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Neural organization of the defensive behavior system responsible for fear

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Fanselow, Michael S.·1994·Psychonomic Bulletin & Review
DOI 10.3758/bf03210947
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Abstract

This paper applies the behavior systems approach to fear and defensive behavior, examining the neural circuitry controlling fear and defensive behavior from this vantage point. The defensive behavior system is viewed as having three modes that are activated by different levels of fear. Low levels of fear promote pre-encounter defenses, such as meal-pattern reorganization. Moderate levels of fear activate post-encounter defenses. For the rat, freezing is the dominant post-encounter defensive response. Since this mode of defense is activated by learned fear, forebrain structures such as the amygdala play a critical role in its organization. Projections from the amygdala to the ventral periaqueductal gray activate freezing. Extremely high levels of fear, such as those provoked by physical contact, elicit the vigorous active defenses that compose the circa-strike mode. Midbrain structures such as the dorsolateral periaqueductal gray and the superior colliculus play a crucial role in organizing this mode of defense. Inhibitory interactions between the structures mediating circa-strike and post-encounter defense allow for the rapid switching between defensive modes as the threatening situation varies.

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Crossref · 10.3758/bf03210947

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  • Fight-or-flight reactions are associated with sympathetically driven heart rate acceleration.

    “Whereas freezing is a form of behavioural inhibition accompanied by parasympathetically dominated heart rate deceleration, fight-or-flight reactions are associated with sympathetically driven heart rate acceleration.”

    From Freeze for action: neurobiological mechanisms in animal and human freezing (2017) · cites this paper as [8]

    In CIRCA-STRIKE DEFENSE (page unavailable), the paper links active defense to autonomic changes, including a shift of blood flow toward skeletal muscle. It mentions tachycardia in the same section, but as part of post-encounter defense, which includes freezing; it does not specify sympathetically driven heart-rate acceleration during fight-or-flight reactions. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • Attentive immobility enables the animal to continue scanning the environment and readies the animal for an active response such as flight or fight.

    “Attentive immobility enables the animal to continue scanning the environment and readies the animal for an active response such as flight or fight.16,45,61”

    From Fear and the Defense Cascade (2015) · cites this paper as [45]

    The paper describes freezing as a rat’s post-encounter defense and, in “Interactions Between the Post-Encounter and Circa-Strike Modes” (page unavailable), says it can transition immediately to active defense. It does not say that immobility enables the animal to keep scanning its environment or specifically readies it for flight or fight. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • The function of tonic immobility is to deactivate the predator's killing reflex or to discourage consumption, as many predators are reluctant to eat dead meat.

    “Its function is to deactivate the predator’s killing reflex or to discourage consumption, as many predators are reluctant to eat dead meat (see Figure 4).16,45,52,85”

    From Fear and the Defense Cascade (2015) · cites this paper as [45]

    In the passage labeled Abstract (page not provided), Fanselow says that freezing in rats probably removes signals that trigger a predator’s attack. That partly supports the proposed attack-prevention function, but the paper does not identify this response as tonic immobility or say that predators avoid eating dead meat. (LLM, conf=0.78)

    Experimental — accuracy not yet measured

  • Freezing is activated at intermediate levels of predator threat.

    “Freezing is activated at intermediate levels of predator threat.”

    From Freeze for action: neurobiological mechanisms in animal and human freezing (2017) · cites this paper as [8]

  • Upon increasing levels of threat, animals activate qualitatively different defensive modes, including freezing and active fight-or-flight reactions.

    “Upon increasing levels of threat, animals activate qualitatively different defensive modes, including freezing and active fight-or-flight reactions.”

    From Freeze for action: neurobiological mechanisms in animal and human freezing (2017) · cites this paper as [8]

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Cites

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Research works printed but not linked: 7

  1. AYRES, J. J. B., AXELROD, H., MERCKER, E., MUCHNIK, F., & VIG- ORITO, M. (1985). Concurrent observations of bar press suppression and freezing: Effects of CS modality and on-line vs. off-line train- ing. Animal Learning & Behavior, 13, 44-50.
  2. DE OcA, 8., DECOLA, J, P" LIEBESKIND, J, c., & FANSELOW, M, S, (in press), Differential effects of ventral and dorsal periaqueductal a closed economy. Journal ofthe Experimental Analysis of Behav- ior, 50, 361-374.
  3. FANSELOW, M. S., & TIGHE,T. J. (1988). Contextual conditioning with massed versus distributed unconditional stimuli. Journal ofExper- imental Psychology: Animal Behavior Processes, 14,187-199.
  4. JURGENS, U. (1991). Neurochemical study ofPAG control of vocal be- havior. In A. Depaulis & R. Bandler (Eds.), The midbrain periaque- ductal grey matter: Functional, anatomical and immunohistochemi- cal organization (NATO ASI Series A: Vol. 213, pp. 11-21). New York: Plenum.
  5. LARSON, C. R. (199 I). Activity ofPAG neurons during conditioned vo- calization in the macaque monkey. In A. Depaulis & R. Bandler (Eds.), The midbrain periaqueductal grey matter: Functional, anatomical and immunohistochemical organization (NATO ASI Se- ries A: Vol. 213, pp. 23-40). New York: Plenum.
  6. LEDoux, J. E. (1992). Emotion and the amygdala. In 1. P. Aggleton (Ed.), The amygdala: Neurobiological aspects ofemotion, memory, and mental dysfunction (pp. 339-351). New York: Wiley-Liss.
  7. YOUNG, S. L., & FANSELOW, M. S. (1992). Associative regulation of Pavlovian fear conditioning: US intensity, incentive shifts & latent inhibition. Journal of Experimental Psychology: Animal Behavior Processes, 18, 400-4 I3. (Manuscript received November 19, 1993; revision accepted for publication June 13, 1994.)

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Authors
Fanselow, M. S.
Affiliations
University of California, Los Angeles (US)
Corresponding author
Fanselow, Michael S.
ORCID
Fanselow, Michael S.
Venue
Psychonomic Bulletin & Review
Publisher
Springer Science and Business Media LLC
Published
1994-12
Volume
1
Issue
4
Pages
429-438
ISSN
  • 1069-9384 (ISSN-L)
  • 1531-5320
DOI
10.3758/bf03210947
OpenAlex
W2047541308
Cited by
1,000
References
86
Citations by year
2026: 31 · 2025: 38 · 2024: 42 · 2023: 46 · 2022: 45 · 2021: 38 · 2020: 34 · 2019: 68 · 2018: 47 · 2017: 54 · 2016: 39 · 2015: 48 · 2014: 41 · 2013: 32 · 2012: 24
FWCI
8.15
Type
journal article
Language
en
Open access
Licence
www.springer.com/tdm (tdm)
Locations
  • Psychonomic Bulletin & Review (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • John D. and Catherine T. MacArthur Foundation
  • Center for Advanced Study in the Behavioral Sciences, Stanford University
  • National Institute of Mental Health (MH39786)
  • Center for Advanced Study, University of Illinois at Urbana-Champaign
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 › Neural and Behavioral Psychology Studies
Keywords
fear, defensive behavior, behavior systems, neural circuits, amygdala, ventral periaqueductal gray, dorsolateral periaqueductal gray, superior colliculus, freezing, active defense, inhibitory interactions

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