Skip to main content
SpringerLink
Log in

The Midbrain Periaqueductal Gray as a Coordinator of Action in Response to Fear and Anxiety

  • Chapter
The Midbrain Periaqueductal Gray Matter

Part of the book series: NATO ASI Series ((NSSA,volume 213))

Abstract

This paper describes a current psychobiological approach to motivated behavior using fear as an illustration. The first part describes the properties of fear motivation and then argues that an amygdala-periaqueductal gray system displays many of these properties. The second half of the paper details the organization of fear related behavior and then presents a model suggesting how the periaqueductal gray may be responsible for much of this organization.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Bandler, R., Brain mechanisms of aggression as revealed by electrical and chemical stimulation: Suggestion of a central role for the midbrain periaqueductal grey region, Prog, psychobiol. physiol. psychol., 13 (1988) 67–154.

    Google Scholar 

  • Bandler, R., Carrive, R, and Zhang, S. P., Integration of somatic and autonomic reactions within the midbrain periaqueductal grey: Viscerotopic, somatotopic and functional organization, Prog. Brain Res., 87 (1991) 269–305.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Blanchard, RJ. and Blanchard, D.C., Defensive reactions in the albino rat, Learn. Motiv., 2(1971) 351–362.

    Article  Google Scholar 

  • Blanchard, D. C. and Blanchard, R. J., Innate and conditioned reactions to threat in rats with amygdaloid lesions, J. Comp. Physiol. Psychol., 81 (1972) 281–290.

    Article  CAS  PubMed  Google Scholar 

  • Blanchard, R.J. and Blanchard, D.C., Ethoexperimental approaches to the biology of emotion, Ann. Rev. Psychol., 39 (1988) 43–68.

    Article  CAS  Google Scholar 

  • Blanchard, R J., Blanchard, D.C. and Hori, K., An ethoexperimental approach to the study of defense, In: Ethoexperimental Approaches to the study of Behavior, Blanchard R. J., Brain P. R., Blanchard D.C. and Parmigiani S. (Eds.), Kluwer, Dordrecht, 1989, pp. 114–136.

    Chapter  Google Scholar 

  • Blanchard, R. J., Fukunaga, K. K. and Blanchard, D. C., Environmental control of defensive reactions to a cat, Bull. Psychon. Soc, 8 (1976) 179–181.

    Google Scholar 

  • Blanchard, D. C., Williams, G., Lee, E. M. C. and Blanchard, R. J., Taming of wild Rattus norvegicus by lesions of the mesencephalic central gray, Physiol. Psychol., 9 (1981) 157–163.

    Google Scholar 

  • Bolles, R. C., Species-specific defense reactions and avoidance learning, Psychol. Rev., 11 (1970) 32–48.

    Article  Google Scholar 

  • Bolles, R.C and Fanselow, M.S., A perceptual-defensive-recuperative model of fear and pain, Behav. Brain Sci., 3 (1980) 291–301.

    Article  Google Scholar 

  • Borszcz, G. S., Cranney, J. and Leaton, R. N., Influence of long-term sensitization on longterm habituation of the acoustic startle response in rats: Central gray lesions, preexposure, and extinction, J. Exper. Psychol.: An. Behav. Pr., 15 (1989) 54–64.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Carrive, P., Bandler, R. and Dampney, A.L., 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 Res., 483 (1989) 251–258.

    Article  CAS  PubMed  Google Scholar 

  • Chance, W.T., Autoanalgesia: Opiate and nonopiate mechanisms, Neurosci. Biobehav. Rev., 4 (1980) 55–67.

    Article  CAS  PubMed  Google Scholar 

  • Criswell, H.E., Analgesia and Hyperreactivity Following Morphine Microinjection into Mouse Brain, Pharmacol. Biochem. Behav., 4 (1975) 23–26.

    Article  Google Scholar 

  • Darwin, C., The expression of the emotions in man and animals, University of Chicago Press, Chicago,1965.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • de Olmos, J., Alheid, G. F. and Beltramino, C. A., Amygdala, In: The rat nervous system. I. Forebrain and midbrain, Paxinos G. (Ed.), Academic Press, New York, 1985, pp. 223–334.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Di Scala, G., Mana, M. J., Jacobs, W. J. and Phillips, A. G., Evidence of Pavlovian conditioned fear following electrical stimulation of the periaqueductal grey in the rat, Physiol. Behav., 40 (1987) 55–63.

    Article  PubMed  Google Scholar 

  • Fanselow, M.S., Conditional and unconditional components of post-shock freezing, Pavlovian J. Biol. Sci., 15 (1980) 177–182.

    CAS  Google Scholar 

  • Fanselow, M.S., Naloxone and Pavlovian fear conditioning, Learn. Motiv, 12 (1981) 398–419.

    Article  Google Scholar 

  • Fanselow, M.S., The post-shock activity burst, Anim. Learn. Behav., 10 (1982) 448–454.

    Article  Google Scholar 

  • Fanselow, M.S., What is conditioned fear?, Trends Neurosci., 7 (1984a) 460–462.

    Article  Google Scholar 

  • Fanselow, M.S., Shock-induced analgesia on the Formalin Test: Effects of shock severity, naloxone, hypophysectomy and associative variables, Behav. Neurosci., 98 (1984b) 79–95.

    Article  CAS  PubMed  Google Scholar 

  • Fanselow, M. S., Odors released by stressed rats produce opioid analgesia in unstressed rats, Behav. Neurosci., 99 (1985) 589–592.

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Fanselow, M. S., The Adaptive Function of Conditioned Defensive Behavior: An Ecological Approach to Pavlovian Stimulus Substitution Theory, In: Ethoexperimental Approaches to the study of Behavior, Blanchard R.J., Brain P.F., Blanchard D.C., and Parmigiani S. (Eds.), Kluwer, Dordrecht, 1989, pp.151–166.

    Chapter  Google Scholar 

  • Fanselow, M. S., Analgesia as a response to aversive Pavlovian conditional stimuli: Cognitive and emotional mediators, In: Fear, Avoidance, and Phobias: A fundamental analysis, Denny M.R. (Ed.), Erlbaum, Hillsdale, 1991, pp. 61–86.

    Google Scholar 

  • Fanselow, M. and Baackes, M.P., Conditioned Fear-Induced Opiate Analgesia on the Formalin Test: Evidence for Two Aversive Motivational Systems, Learn. Motiv, 13 (1982) 200–221.

    Article  Google Scholar 

  • Fanselow, M. S., Calcagnetti, D. J. and Helmstetter, F. J., The Role of µ, and k Opioid Receptors in Conditional-Fear Induced Analgesia: The Antagonistic Actions of Nor-Binaltorphimine and the Cyclic Somatostatin Octapeptide, Cys2Tyr3Orn5Pen7-Amide, J. Pharmacol. Exp. Ther., 250 (1989) 825–830.

    CAS  PubMed  Google Scholar 

  • Fanselow, M.S. and Helmstetter, F.J., Conditional Analgesia, Defensive Freezing and Benzodiazepines, Behav. Neurosci., 102 (1988) 233–243.

    Article  CAS  PubMed  Google Scholar 

  • Fanselow, M. S., Helmstetter, F. J. and Calcagnetti, D. J., Parallels between the behavioral effects of Dimethoxy-S-Carboline (DMCM) and conditional fear stimuli, In: Current Topics in Animal Learning: Brain, Emotion, and Cognition, Dachowski L. and Flaherty C.F. (Eds.), Erlbaum, Hillsdale, 1991, pp. 187–206,

    Google Scholar 

  • Fanselow, M. S. and Lester, L. S., A functional behavioristic approach to aversively motivated behavior: Predatory imminence as a determinant of the topography of defensive behavior, In: Evolution and Learning, Bolles R. C. and Beecher M. D. (Eds.), Erlbaum, Hillsdale,1988, pp. 185–212.

    Google Scholar 

  • Fanselow, M. S., Lester, L. S. and Helmstetter, F. J., Changes in Feeding and Foraging Patterns as an Antipredator Defensive Strategy: A Laboratory Simulation using aversive stimulation in a Closed Economy, J. Exper. Anal. Behav., 50 (1988) 361–374.

    Article  CAS  Google Scholar 

  • Fanselow, M. S. and Sigmundi, R. A., Species specific danger signals, endogenous opioid analgesia, and defensive behavior, J. Exper. Psychol.: An. Behav. Proc., 12 (1986) 301–309.

    Article  CAS  Google Scholar 

  • Fanselow, M. S. and Sigmundi, R. A., Functional behaviorism and aversively motivated behavior: A role for endogenous opioids in the defensive behavior of the rat, Psychol. Rec, 37 (1987) 317–334.

    Google Scholar 

  • Gloor, P., Inputs and outputs of the amygdala: What the amygdala is trying to tell to the rest of the brain, In: Limbic mechanisms: The continuing evolution of the limbic system concept, Livingston K. and Hornykiewicz O. (Eds.), Plenum, New York, 1978, pp. 196–206.

    Google Scholar 

  • Grau, J. W., The Central Representation of an Aversive Event Maintains the Opioid and Nonopioid Forms of Analgesia, Behav. Neurosci., 101 (1987) 272–288.

    Article  CAS  PubMed  Google Scholar 

  • Griffith, C., The behavior of white rats in the presence of cats, Psychobiol., 2 (1920) 19–28

    Article  Google Scholar 

  • Grossen, N.E. and Kelley, M.J., Species-specific behavior and acquisition of avoidance behavior in rats, J. Comp. Physiol. Psychol., 81 (1972) 307–310.

    Article  CAS  PubMed  Google Scholar 

  • Hagen, H. S. and Green, K. F., Effects of time of testing, stress level, and number of conditioning days on naloxone sensitivity of conditioned stress-induced analgesia in rats, Behav. Neurosci., 102 (1988) 906–914.

    Article  CAS  PubMed  Google Scholar 

  • Helmstetter, F. J., Calcagnetti, D. J. and Fanselow, M. S., The beta-carboline DMCM produces hypoalgesia after central administration, Psychobiol., 18 (1990) 293–297.

    CAS  Google Scholar 

  • Helmstetter, F. J. and Fanselow, M. S., Differential second-order aversive conditioning using contextual stimuli, An. Learn. Behav., 17 (1989) 205–212.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Helmstetter, F. J., Leaton, R. N., Fanselow, M. S. and Calcagnetti, D. J., The amygdala is involved in the expression of conditional analgesia, Soc. Neurosci. Abst., 14 (1988) 1227.

    Google Scholar 

  • Hirsch, S.M. and Bolles, R.C., On the ability of prey to recognize predators, Z. Tierpsychol., 54 (1980) 71–84.

    Google Scholar 

  • Hofer, M. A., Cardiac and respiratory function during sudden prolonged immobility in wild rodents, Psychosom. Med., 32 (1980) 633–647.

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jacquet, Y. F. and Lajtha, A., Paradoxical Effects after Microinjection of Morphine in the Periaqueductal Gray Matter in the Rat, Science, 185 (1974) 1055–1057.

    Article  CAS  PubMed  Google Scholar 

  • Kavaliers, M., Brief Exposure to a Natural Predator, the Short-tail Weasel, Induces Benzodiazepine Sensitive Analgesia in White-footed Mice, Physiol. Behav., 43 (1988) 187–193.

    Article  CAS  PubMed  Google Scholar 

  • Krettek, j.E. and Price, J. L., Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat, J. Comp. Neurol., 178 (1978) 225–254.

    Article  CAS  PubMed  Google Scholar 

  • Leaton, R. N. and Borszcz, G. S., Potentiated startle: Its relation to freezing and shock intensity in rats, J. Exper. Psychol.: An. Behav.Proc., 2 (1985) 248–259.

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • LeDoux, J. E., Iwata, J., Pearl, D., and Reis, D. J., Disruption of auditory but not visual learning by destruction of intrinsic neurons in the rat medial geniculate body, Brain Res., 371 (1986) 395–399.

    Article  CAS  PubMed  Google Scholar 

  • Lester, L. S. and Fanselow, M. S., Exposure to a cat produces opioid analgesia in rats, Behav. Neurosci., 99 (1985) 756–759.

    Article  CAS  PubMed  Google Scholar 

  • Lichtman, A. H. and Fanselow, M. S., Yohimbine administered intrathecally (i.th.) reverses both opioid and nonopioid conditional antinociception (CA) in rats, Soc. Neurosci. Abst., 15 (1989) 372.

    Google Scholar 

  • Lichtman, A. H. and Fanselow, M. S., Cats produce analgesia in rats on the tail-flick test: Naltrexone sensitivity is determined by the nociceptive test stimulus, Brain Res., 533 (1990) 91–94.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Maier, S. F., Determinants of the nature of environmentally-induced hypoalgesia, Behav. Neurosci., 103 (1989) 131–143.

    CAS  Google Scholar 

  • Maier, S. F., Diazepam modulation of stress-induced analgesia depends on the type of analgesia, Behav. Neurosci., 104 (1990) 339–347.

    Article  CAS  PubMed  Google Scholar 

  • Mayer, D. J. and Liebeskind, J. C., Pain reduction by focal electrical stimulation of the brain: An anatomical and behavioral analysis, Brain Res., 68 (1974) 73–93.

    Article  CAS  PubMed  Google Scholar 

  • Morgan, M. M. and Liebeskind, J. C., Site specificity in the development of tolerance to stimulation-produced analgesia from the periaqueductal gray matter of the rat, Brain Res., 425 (1987) 356–359.

    Article  CAS  PubMed  Google Scholar 

  • Oliveras, J. L. and Besson, J. M., Stimulation-produced analgesia in animals: behavioural investigations, Prog. Brain Res., 77 (1988) 141–157.

    Article  CAS  PubMed  Google Scholar 

  • Pinel, J. P. J. and Mana, M. J., Adaptive interactions of rats with dangerous inanimate objects: Support for a cognitive theory of defensive behavior, In: Ethoexperimental Approaches to the study of Behavior, Blanchard R. J., Brain P. F., Blanchard D. C. and Parmigiani S. (Eds.), Kluwer, Dordrecht, 1989, pp. 137–150.

    Chapter  Google Scholar 

  • Rescorla, R.A., Effect of Inflation of the Unconditioned Stimulus Value Following Conditioning, J. Comp. Physiol. Psychol., 86 (1974) 101–106.

    Article  Google Scholar 

  • Rescorla, R. A., Pavlovian second-order conditioning, Erlbaum, Hillsdale, 1980.

    Google Scholar 

  • Reynolds, D. V., Surgery in the rat during electrical analgesia induced by focal brain stimulation, Science, 164 (1969) 444–445.

    Article  CAS  PubMed  Google Scholar 

  • Rhoades, R. W., Mooney, R. D., Rohrer, W. H., Nikoletseas, M. M. and Fish, S. E., Organization of the projection from the superficial to the deep layers of the hamster’s superior colliculus as demonstrated by anterograde transport of Phaseolus vulgaris leucoagglutinin, J. Comp. Neurol., 283 (1989) 54–70.

    Article  CAS  PubMed  Google Scholar 

  • Rizley, R. C. and Rescorla, R. A., Associations in second-order conditioning and sensory preconditioning, J. Comp. Physiol. Psychol., 81 (1972) 1–11.

    Article  CAS  PubMed  Google Scholar 

  • Rizvi, T. A., Ennis, M., Behbehani, M. and Shipley, M. T., Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: Topography and reciprocity, J. Comp. Neurol. (1991) in press.

    Google Scholar 

  • Rodgers, R. J. and Randall, J. I., Benzodiazepine ligands, nociception and ‘defeat’ analgesia, Psychopharmacology, 91 (1987) 305–315.

    Article  CAS  PubMed  Google Scholar 

  • Ross, R. T., Pavlovian second-order conditioned analgesia, J. Exper. Psychol.: An. Behav. Proc., 12 (1988) 32–39.

    Article  Google Scholar 

  • Small, W., Notes on the psychic development of the young white rat, Am. J. Psychol., 11 (1899) 80–100.

    Article  Google Scholar 

  • Stephens, D.N. and Kehr, W., β-Carbolines can enhance or antagonize the effects of punishment in mice, Psychopharmacology, 85 (1985) 143–147.

    Article  CAS  PubMed  Google Scholar 

  • Terman, G. W., Shavit, Y., Lewis, J. W., Cannon, J. T. and Liebeskind, J. C., Intrinsic mechanisms of pain inhibition: Activation by stress, Science, 226 (1984) 1270–1277.

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Urca, G., Nahin., R, Liebeskind, J., Glutamate-induced Analgesia: Blockade and Potentiation By Naloxone, Brain Res., 192 (1980) 523–530.

    Article  CAS  PubMed  Google Scholar 

  • Watkins, L. R. and Mayer, D. J., Multiple endogenous opiate and non-opiate analgesia systems: Evidence of their existence and clinical implications, Ann. N. Y. Acad. Sci., 467 (1986) 273–299.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Psychology and Brain Research Institute, University of California-Los Angeles, California, USA

    Michael S. Fanselow

Authors
  1. Michael S. Fanselow
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. L.N.B.C, Centre de Neurochimie du CNRS, 5 rue Blaise Pascal, 67084, Strasbourg Cedex, France

    Antoine Depaulis

  2. Dept. of Anatomy, University of Sydney, 2006, Sydney, NSW, Australia

    Richard Bandler

Rights and permissions

Reprints and permissions

Copyright information

© 1991 Springer Science+Business Media New York

About this chapter

Cite this chapter

Fanselow, M.S. (1991). The Midbrain Periaqueductal Gray as a Coordinator of Action in Response to Fear and Anxiety. In: Depaulis, A., Bandler, R. (eds) The Midbrain Periaqueductal Gray Matter. NATO ASI Series, vol 213. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-3302-3_10

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-3302-3_10

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-6453-5

  • Online ISBN: 978-1-4615-3302-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation