Skip to main content

Neural organization of the defensive behavior system responsible for fear

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.

References

  • Ayres, J. J. B., Axelrod, H., Mercker, E., Muchnik, F., &Vigorito, M. (1985). Concurrent observations of barpress suppression and freezing: Effects of CS modality and on-line vs. off-line training.Animal Learning & Behavior,13, 44–50.

    Google Scholar 

  • Bandler, R., Carrive, P., &Zhang, S. P. (1991). Integration of somatic and autonomic reactions within the midbrain periaqueductal grey: Viscerotopic, somatotopic and functional organization. In G. Holstege (Ed.),Progress in brain research: Vol. 87. Role of the forebrain in sensation and behavior (pp. 269–305). Amsterdam: Elsevier.

    Chapter  Google Scholar 

  • Bandler, R., &Depaulis, A. (1988). Elicitation of intraspecific defence reactions in the rat from midbrain periaqueductal grey by microinjection of kainic acid without neurotoxic effects.Neuroscience Letters,88, 291–296.

    Article  PubMed  Google Scholar 

  • Bandler, R., &Depaulis, A. (1991). Midbrain periaqueductal gray control of defensive behavior in the cat and the rat. In A. Depaulis & R. Bandler (Eds.),The midbrain periaqueductal grey matter: Functional, anatomical and immunohistochemical organization (NATO ASI Series A: Vol. 213, pp. 175–198). New York: Plenum.

    Google Scholar 

  • Blanchard, D. C., &Blanchard, R. J. (1969). Crouching as an index of fear.Journal of Comparative & Physiological Psychology,67, 370–375.

    Article  Google Scholar 

  • Blanchard, D. C., &Blanchard, R. J. (1972). Innate and conditioned reactions to threat in rats with amygdaloid lesions.Journal of Comparative & Physiological Psychology,81, 281–290.

    Article  Google Scholar 

  • Blanchard, R. J., Blanchard, D. C., Agullana, R., &Weis, S. M. (1991). Twenty-two kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems.Physiology & Behavior,50, 967–972.

    Article  Google Scholar 

  • Blanchard, R. J., Blanchard, D. C., &Hori, K. (1989). An ethoexperimental approach to the study of defense. In R. J. Blanchard, P. F. Brain, D. C. Blanchard, & S. Parmigiani (Eds.),Ethoexperimental approaches to the study of behavior (NATO ASI Series D: Vol. 48, pp. 114–136). Boston: Kluver Academic Publishers.

    Google Scholar 

  • Blanchard, R. J., Fukunaga, K. K., &Blanchard, D. C. (1976). Environmental control of defensive reactions to footshock.Bulletin of the Psychonomic Society,8, 129–130.

    Google Scholar 

  • Blomqvist, A., &Craig, A. D. (1991). Organization of spinal and trigeminal input to the PAG. In A. Depaulis & R. Bandler (Eds.),The midbrain periaqueductal grey matter: Functional, anatomical and immunohistochemical organization (NATO ASI Series A: Vol. 213, pp. 345–363). New York: Plenum.

    Google Scholar 

  • Bolles, R. C. (1970). Species-specific defense reactions and avoidance learning.Psychological Review,77, 32–48.

    Article  Google Scholar 

  • Bolles, R. C. (1975).Theory of motivation (2nd ed). New York: Harper & Row.

    Google Scholar 

  • Bolles, R. C., &Collier, A. C. (1976). Effect of predictive cues on freezing in rats.Animal Learning & Behavior,4, 6–8.

    Google Scholar 

  • Bolles, R. C., &Fanselow, M. S. (1980). A perceptual-defensiverecuperative model of fear and pain.Behavioral & Brain Sciences,3, 291–301.

    Article  Google Scholar 

  • Bolles, R. C., &Riley, A. L. (1973). Freezing as an avoidance response: Another look at the operant-respondent distinction.Learning & Motivation,4, 268–275.

    Article  Google Scholar 

  • Cannon, J. T., Prieto, G. J., Lee, A., &Liebeskind, J. C. (1982). Evidence for opioid and non-opioid forms of stimulation-produced analgesia in the rat.Brain Research,243, 315–321.

    Article  PubMed  Google Scholar 

  • Carrive, P., Bandler, R., &Dampney, R. A. L. (1989). Somatic and autonomic integration in the midbrain of the unanesthetized decerebrate cat: A distinctive pattern evoked by excitation of neurones in the subtentorial portion of the midbrain periaqueductal grey.Brain Research,483, 251–258.

    Article  PubMed  Google Scholar 

  • Chandler, S. C., Liu, H., Murphy, A. Z., Shipley, M. T., &Behbehani, M. M. (1993). Columnar organization in PAG: Physiological evidence for intercolumnar interactions.Society for Neuroscience Abstracts,19, 1408.

    Google Scholar 

  • Clugnet, M.-C., &LeDoux, J. E. (1990). Synaptic plasticity in fear conditioning circuits: Induction of LTP in the lateral nucleus of the amygdala by stimulation of the medial geniculate body.Journal of Neuroscience,10, 2818–2824.

    PubMed  Google Scholar 

  • Davis, M. (1992). The role of the amygdala in conditioned fear. In J. P. Aggleton (Ed.),The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction (pp. 255–305). New York: Wiley-Liss.

    Google Scholar 

  • Dean, P., Redgrave, P., &Westby, G. W. M. (1989). Event or emergency? Two response systems in the mammalian superior colliculus.Trends in Neuroscience,12, 137–147.

    Article  Google Scholar 

  • De Oca, B.,DeCola, J. P.,Liebeskind, J. C., &Fanselow, M. S. (in press). Differential effects of ventral and dorsal periaqueductal gray (PAG) lesions on defensive responses of rats to cats, shock and taste aversion.Society for Neuroscience Abstracts.

  • Depaulis, A., Bandler, R., &Vergnes, M. (1989). Characterization of pretentorial periaqueductal gray neurons mediating intraspecific defensive behaviors in the rat by microinjections of kainic acid.Brain Research,486, 121–132.

    Article  PubMed  Google Scholar 

  • Depaulis, A., Keay, K. A., &Bandler, R. (1992). Longitudinal neuronal organization of defensive reactions in the midbrain periaqueductal gray region of the rat.Experimental Brain Research,90, 307–318.

    Article  Google Scholar 

  • Estes, W. K., &Skinner, B. F. (1941). Some quantitative properties of anxiety.Journal of Experimental Psychology,29, 390–400.

    Article  Google Scholar 

  • Fanselow, M. S. (1980). Conditional and unconditional components of post-shock freezing.Pavlovian Journal of Biological Sciences,15, 177–182.

    Google Scholar 

  • Fanselow, M. S. (1982). The post-shock activity burst.Animal Learning & Behavior,10, 448–454.

    Google Scholar 

  • Fanselow, M. S. (1984). Opiate modulation of both the active and inactive components of the postshock reaction: Parallels between naloxone pretreatment and shock intensity.Behavioral Neuroscience,98, 269–277.

    Article  PubMed  Google Scholar 

  • Fanselow, M. S. (1986). Associative vs. topographical accounts of the immediate shock freezing deficit in rats: Implications for the response selection rules governing species specific defensive reactions.Learning & Motivation,17, 16–39.

    Article  Google Scholar 

  • Fanselow, M. S. (1989). The adaptive function of conditioned defensive behavior: An ecological approach to Pavlovian stimulus substitution theory. In R. J. Blanchard, P. F. Brain, D. C. Blanchard, & S. Parmigiani (Eds.),Ethoexperimental approaches to the study of behavior (NATO ASI Series D: Vol. 48, pp. 151–166). Boston: Kluver Academic Publishers.

    Google Scholar 

  • Fanselow, M. S. (1990). Factors governing one trial contextual conditioning.Animal Learning & Behavior,18, 264–270.

    Google Scholar 

  • Fanselow, M. S. (1991). The midbrain periaqueductal gray as a coordinator of action in response to fear and anxiety. In A. Depaulis & R. Bandler (Eds.),The midbrain periaqueductal grey matter: Functional, anatomical and immunohistochemical organization (NATO ASI Series A: Vol. 213, pp. 151–173). New York: Plenum.

    Google Scholar 

  • Fanselow, M. S., &Baackes, M. P. (1982). Conditioned fear-induced opiate analgesia on the formalin test: Evidence for two aversive motivational systems.Learning & Motivation,13, 220–221.

    Article  Google Scholar 

  • Fanselow, M. S.,DeCola, J. P.,De Oca, B., &Landeira-Fernandez, J. (in press). Ventral and dorsolateral regions of the midbrain periaqueductal gray control different stages of defensive behavior: Dorsolateral PAG lesions enhance the defensive freezing produced by massed and immediate shock.Aggressive Behavior.

  • Fanselow, M. S., DeCola, J. P., &Young, S. L. (1993). Mechanisms responsible for reduced contextual conditioning with massed unsignaled unconditional stimuli.Journal of Experimental Psychology: Animal Behavior Processes,19, 121–137.

    Article  PubMed  Google Scholar 

  • Fanselow, M. S., &Kim, J. J. (1992). The benzodiazepine inverse agonist DMCM as an unconditional stimulus for fear-induced analgesia: Implications for the role of GABAA receptors in fear related behavior.Behavioral Neuroscience,106, 336–344.

    Article  PubMed  Google Scholar 

  • Fanselow, M. S., &Kim, J. J. (1994). Acquisition of contextual Pavlovian fear conditioning is blocked by application of an NMDA receptor antagonist D,L-2-amino-5-phosphonovaleric acid to the basolateral amygdala.Behavioral Neuroscience,108, 210–212.

    Article  PubMed  Google Scholar 

  • Fanselow, M. S., Landeira-Fernandez, J., DeCola, J. P., &Kim, J. J. (1994). The immediate shock deficit and postshock analgesia: Implications for the relationship between the analgesic CR and UR.Animal Learning & Behavior,22, 72–76.

    Google Scholar 

  • Fanselow, M. S., &Lester, L. S. (1988). A functional behavioristic approach to aversively motivated behavior: Predatory imminence as a determinant of the topography of defensive behavior. In R. C. Bolles & M. D. Beecher (Eds.),Evolution and learning (pp. 185–211). Hillsdale, NJ: Erlbaum.

    Google Scholar 

  • Fanselow, M. S., Lester, L. S., &Helmstetter, F. J. (1988). Changes in feeding and foraging patterns as an antipredator defensive strategy: A laboratory simulation using aversive stimulation in a closed economy.Journal of the Experimental Analysis of Behavior,50, 361–374.

    Article  PubMed  Google Scholar 

  • Fanselow, M. S., Sigmundi, R. A., &Williams, J. (1987). Response selection and the hierarchical organization of species specific defense reactions: The relationship between freezing, flight and defensive burying.Psychological Record,37, 381–386.

    Google Scholar 

  • Fanselow, M. S., &Tighe, T. J. (1988). Contextual conditioning with massed versus distributed unconditional stimuli.Journal of Experimental Psychology: Animal Behavior Processes,14, 187–199.

    Article  PubMed  Google Scholar 

  • Grau, J. W. (1984). Influence of naloxone on shock-induced freezing and analgesia.Behavioral Neuroscience,98, 278–292.

    Article  PubMed  Google Scholar 

  • Helmstetter, F. J. (1992). The amygdala is essential for the expression of conditional hypoalgesia.Behavioral Neuroscience,106, 518–528.

    Article  PubMed  Google Scholar 

  • Helmstetter, F. J., &Fanselow, M. S. (1987). Effects of naltrexone on learning and performance of conditional fear-induced freezing and opioid analgesia.Physiology & Behavior,39, 501–505.

    Article  Google Scholar 

  • Helmstetter, F. J., &Fanselow, M. S. (1993). Aversively motivated changes in meal patterns of rats in a closed economy: The effects of shock density.Animal Learning & Behavior,21, 168–175.

    Google Scholar 

  • Helmstetter, F. J., &Landeira-Fernandez, J. (1991). Conditional hypoalgesia is attenuated by naltrexone applied to the periaqueductal gray.Brain Research,537, 88–92.

    Article  Google Scholar 

  • Hirsch, S. M., &Bolles, R. C. (1980). On the ability of prey to recognize predators.Zeitschrift für Tierpsychologie,54, 71–84.

    Google Scholar 

  • Hopkins, D. A., &Holstege, G. (1978). Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat.Experimental Brain Research,32, 529–547.

    Article  Google Scholar 

  • Jurgens, U. (1991). Neurochemical study of PAG control of vocal behavior. In A. Depaulis & R. Bandler (Eds.),The midbrain periaqueductal grey matter: Functional, anatomical and immunohistochemical organization (NATO ASI Series A: Vol. 213, pp. 11–21). New York: Plenum.

    Google Scholar 

  • Kapp, B. S., Whalen, P. J., Supple, W. F., &Pascoe, J. P. (1992). Amygdaloid contributions to conditioned arousal and sensory information processing. In J. P. Aggleton (Ed.),The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction (pp. 229–254). New York: Wiley-Liss.

    Google Scholar 

  • Kiernan, M., &Cranney, J. (1992). Excitotoxic lesions of the central nucleus of the amygdala but not of the periaqueductal gray block integrated fear responding as indexed by both freezing responses and augmentation of startle.Society for Neuroscience Abstracts,18, 1566.

    Google Scholar 

  • Kim, J. J., &Fanselow, M. S. (1992). Modality specific retrograde amnesia of fear following hippocampal lesions.Science,256, 675–677.

    Article  PubMed  Google Scholar 

  • Kim, J. J., Rison, R. A., &Fanselow, M. S. (1993). Effects of amygdala, hippocampus, and periaqueductal gray lesions on short- and long-term contextual fear.Behavioral Neuroscience,107, 1093–1098.

    Article  PubMed  Google Scholar 

  • Larson, C. R. (1991). Activity of PAG neurons during conditioned vocalization in the macaque monkey. In A. Depaulis & R. Bandler (Eds.),The midbrain periaqueductal grey matter: Functional, anatomical and immunohistochemical organization (NATO ASI Series A: Vol. 213, pp. 23–40). New York: Plenum.

    Google Scholar 

  • Leaton, R. N., &Borszcz, G. S. (1985). Potentiated startle: Its relation to freezing and shock intensity in rats.Journal of Experimental Psychology,11, 421–428.

    Google Scholar 

  • LeDoux, J. E. (1992). Emotion and the amygdala. In J. P. Aggleton (Ed.),The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction (pp. 339–351). New York: Wiley-Liss.

    Google Scholar 

  • LeDoux, J. E., Iwata, J., Cicchetti, P., &Reis, D. J. (1988). Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear.Journal of Neuroscience,8, 2517–2529.

    PubMed  Google Scholar 

  • LeDoux, J. E., Sakaguchi, A., &Reis, D. J. (1984). Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli.Journal of Neuroscience,4, 683–698.

    PubMed  Google Scholar 

  • Liebman, J. M., Mayer, D. J., &Liebeskind, J. C. (1970). Mesencephalic central gray lesions and fear-motivated behavior in rats.Brain Research,23, 353–370.

    Article  PubMed  Google Scholar 

  • Lovick, T. A. (1991). Interactions between descending pathways from the dorsal and ventrolateral periaqueductal gray matter in the rat. In A. Depaulis & R. Bandler (Eds.),The midbrain periaqueductal grey matter: Functional, anatomical and immunohistochemical organization (NATO ASI Series A: Vol. 213, pp. 101–120). New York: Plenum.

    Google Scholar 

  • Lyon, M. (1964). The role of central midbrain structures in conditioned responding to aversive noise in the rat.Journal of Comparative Neurology,122, 407–429.

    Article  PubMed  Google Scholar 

  • Maier, S. F. (1989). Determinants of the nature of environmentallyinduced hypoalgesia.Behavioral Neuroscience,103, 131–143.

    Article  PubMed  Google Scholar 

  • Phillips, R. G., &LeDoux, J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning.Behavioral Neuroscience,106, 274–285.

    Article  PubMed  Google Scholar 

  • Redgrave, P., &Dean, P. (1991). Does the PAG learn about emergencies from the superior colliculus? In A. Depaulis & R. Bandler (Eds.),The midbrain periaqueductal grey matter: Functional, anatomical and immunohistochemical organization (NATO ASI Series A: Vol. 213, pp. 199–209). New York: Plenum.

    Google Scholar 

  • Rizvi, T. A., Ennis, M., Behbehani, M., &Shipley, M. T. (1991). Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: Topography and reciprocity.Journal of Comparative Neurology,303, 121–131.

    Article  PubMed  Google Scholar 

  • Shipley, M. T., Ennis, M., Rizvi, T. A., &Behbehani, M. M. (1991). Topographical specificity of forebrain inputs to the midbrain periaqueductal gray: Evidence for discrete longitudinally organized input columns. In A. Depaulis & R. Bandler (Eds.),The midbrain periaqueductal grey matter: Functional, anatomical and immunohistochemical organization (NATO ASI Series A: Vol. 213, pp. 417–448). New York: Plenum.

    Google Scholar 

  • Sigmundi, R. A., &Bolles, R. C. (1983). CS modality, context conditioning, and conditioned freezing.Animal Learning & Behavior,11, 205–212.

    Google Scholar 

  • Timberlake, W. (1993). Behavior systems and reinforcement: An integrative approach.Journal of the Experimental Analysis of Behavior,60, 105–128.

    Article  PubMed  Google Scholar 

  • Timberlake, W., &Lucas, G. A. (1989). Behavior systems and learning: From misbehavior to general principles. In S. B. Klein & R. R. Mowrer (Eds.),Contemporary learning theories: Instrumental conditioning theory and the impact of biological constraints on learning (pp. 237–275). Hillsdale, NJ: Erlbaum.

    Google Scholar 

  • Tolman, E. C. (1932).Purposive behavior in animals and men. New York: Appleton.

    Google Scholar 

  • Watkins, L. R., Cobelli, D. A., &Mayer, D. J. (1982). Classical conditioning of front paw and hind paw footshock induced analgesia (FSIA): Naloxone reversibility and descending pathways.Brain Research,243, 119–132.

    Article  PubMed  Google Scholar 

  • Yeomans, J. S., &Pollard, B. A. (1993). Amygdala efferents mediating electrically evoked startle-like responses and fear potentiation of acoustic startle.Behavioral Neuroscience,107, 596–610.

    Article  PubMed  Google Scholar 

  • Young, S. L., Bohenek, D. L., &Fanselow, M. S. (1994). NMDA processes mediate anterograde amnesia of contextual fear conditioning induced by hippocampal damage: Immunization against amnesia by contextual preexposure.Behavioral Neuroscience,108, 19–29.

    Article  PubMed  Google Scholar 

  • 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, 400–413.

    Article  PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Additional information

This paper is dedicated to the memory of Robert C. Bolles. The research was supported by National Institute of Mental Health Grant MH39786. The article was partly prepared while the author was a fellow at the Center for Advanced Study in the Behavioral Sciences supported by the John D. and Catherine T. MacArthur Foundation Grant 8900078. Thanks are due S. L. Young and J. P. DeCola for helpful comments.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Fanselow, M.S. Neural organization of the defensive behavior system responsible for fear. Psychon Bull Rev 1, 429–438 (1994). https://doi.org/10.3758/BF03210947

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.3758/BF03210947

Keywords

  • Conditional Stimulus
  • Unconditional Stimulus
  • Superior Colliculus
  • Activity Burst
  • Defensive Behavior