Skip to main content
Log in

Conditioned Defensive Responses and Hypoalgesia in Rats Exposed to Defeat and Alpha-Colony Odors

  • Published:
The Psychological Record Aims and scope Submit manuscript

Abstract

This article describes the results of recent studies that examine the effects, in rats, of defeat by a dominant conspecific on subsequent defensive responses and hypoalgesia. In Experiment 1, male subjects were exposed to either aggressive (alpha) or nonaggressive conspecific colonies and tested 24 hr later, with or without alpha-colony odors, for freezing and burying of a wall prod that had been the source of a single electric shock. Although prior exposure to defeat and the presence of alpha-colony odors during testing had no effects, per se, the combination of these factors significantly suppressed prod burying and increased freezing. In Experiment 2, a 12-hr exposure session to the alpha-colony odors, for previously defeated intruders, resulted in the extinction of the fear-mediated suppressions in burying and increments in freezing during later prod-shock tests with alpha-colony odors present. In Experiment 3, male rats were either defeated as colony intruders by alpha conspecifics or had no defeat experience, and 24 hr later they were given a paw injection of formalin prior to observational tests with or without alpha-colony odors. The combination of defeat and tests with these odors produced conditioned hypoalgesia (i.e., a suppression in paw licking) and freezing. In Experiment 4, an injection of naltrexone prior to a defeat session increased freezing during defeat and during formalin testing 24 hr later, whereas injecting naltrexone prior to testing did not affect freezing but significantly reduced conditioned hypoalgesia. In Experiment 5, a 12-hr pretest exposure session to alpha-colony odors extinguished this conditioned hypoalgesic response for previously defeated rats. These fear-induced alterations in defensive behavior and pain sensitivity are discussed in terms of associative, opioid/nonopioid, and adaptive evolutionary processes.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • AMIR, S., & AMIT, Z. (1978). Endogenous opioid ligands may mediate stress-induced changes in affective properties of pain-related behaviour in rats. Life Sciences, 23, 1143–1152.

    Article  PubMed  Google Scholar 

  • AMIR, S., & AMIT, Z. (1979). The pituitary gland mediated acute and chronic pain responsiveness in stressed and non-stressed rats. Life Sciences, 24, 439–448.

    Article  PubMed  Google Scholar 

  • AMIR, Z., & GALINA, H. (1986). Stress-induced analgesia: Adaptive pain suppression. Physiological Reviews, 66, 1091–1119.

    Google Scholar 

  • BARNETT, S. A. (1958). An analysis of social behaviour in wild rats. Proceedings of the Zoological Society of London, 130, 107–152.

    Article  Google Scholar 

  • BAUM, M. (1970). Extinction of avoidance responding through response prevention (flooding). Psychological Bulletin, 74, 276–284.

    Article  PubMed  Google Scholar 

  • BLANCHARD, R. J., & BLANCHARD, D. C. (1977). Aggressive behavior in the rat. Behavioral Biology 21, 197–224.

    Article  PubMed  Google Scholar 

  • BLANCHARD, R. J., & BLANCHARD, D. C. (1981). The organization and modelling of aggressive behavior. In P. F. Brain & D. Benton (Eds.), The biology of aggression (pp. 529–561). Alphen aan den Rijn: Noordhoof/Sijthoff Press.

    Chapter  Google Scholar 

  • BLANCHARD, R. J., BLANCHAD, 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 (pp. 114–136). Dordrecht: Martinus Nijhoff.

    Chapter  Google Scholar 

  • BOLLES, R. C., & FANSELOW, M. S. (1980). A perceptual-defensive-recuperative model of fear and pain. Behavioral and Brain Sciences, 3, 291–323.

    Article  Google Scholar 

  • FANSELOW, M. S. (1984). Shock-induced analgesia on the formalin test: Effects of shock severity, naloxone, hypophysectomy, and associative variables. Behavioral Neuroscience, 98, 79–95.

    Article  PubMed  Google Scholar 

  • FANSELOW, M. S. (1985). Odors released by stressed rats produce opioid analgesia in unstressed rats. Behavioral Neuroscience, 99, 589–592.

    Article  PubMed  Google Scholar 

  • FANSELOW, M. S. (1986). Conditioned fear-induced opiate analgesia: A competing motivational state theory of stress analgesia. In D. D. Kelley (Ed.), Annals of the New York Academy of Sciences (Vol. 476, pp. 40–54).

    Article  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 and Motivation, 13, 200–221.

    Article  Google Scholar 

  • FANSELOW, M. S., & BOLLES, R. C. (1979). Naloxone and shock-elicited freezing in the rat. Journal of Comparative and Physiological Psychology, 94, 736–744.

    Article  Google Scholar 

  • FANSELOW, M. S., & HELMSTETTER, F. J. (1988). Conditioned analgesia, defensive freezing, and benzodiazepines. Behavioral Neuroscience, 102, 233–243.

    Article  PubMed  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. Bolies & M. D. Beecher (Eds.), Evolution and learning (pp. 185–212). Hillsdale, NJ: Erlbaum.

    Google Scholar 

  • FANSELOW, M. S., & SIGMUNDI, R. A. (1986). Species-specific danger signals, endogenous opioid analgesia, and defensive behavior. Journal of Experimental Psychology: Animal Behavior Processes, 12, 301–309.

    PubMed  Google Scholar 

  • FANSELOW, M. S., SIGMUNDI, R. A., & WILLIAMS, J. L. (1987). Response selection and hierarchical organization of species-specific defensive reactions: The relationship between freezing, flight, and defensive burying. The Psychological Record, 37, 381–386.

    Google Scholar 

  • FLANNELLY, K. J., FLANNELLY, L., & BLANCHARD, R. J. (1984). Adult experience and the expression of aggression: A comparative analysis. In K. J. Flannelly, R. J. Blanchard, & D. C. Blanchard (Eds.), Biological perspectives on aggression (pp. 207–259). New York: Alan Liss.

    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 

  • LESTER, L. S., & FANSELOW, M. A. (1985). Exposure to a cat produces opioid analgesia in rats. Behavioral Neuroscience, 99, 756–759.

    Article  PubMed  Google Scholar 

  • LEVIS, D. J. (1989). The case for a return to two-factor theory of avoidance: The failure of non-fear interpretations. In S. B. Klein & R. R. Mowrer (Eds.), Contemporary learning theories: Pavlovian conditioning and the status of traditional learning theory (pp. 227–278). Hillsdale, NJ: Erlbaum.

    Google Scholar 

  • MACLENNAN, A. J., JACKSON, R. L., & MAIER, S. F. (1980). Conditioned analgesia in the rat. Bulletin of the Psychonomic Society, 15, 387–390.

    Article  Google Scholar 

  • MAIER, S. F. (1986). Stressor controllability and stress-induced analgesia. In D. D. Kelley (Ed.), Annals of the New York Academy of Sciences (Vol. 467, pp. 55–71).

    Article  PubMed  Google Scholar 

  • MAIER, S. F. (1989). Determinants of the nature of environmentally induced hypoalgesia. Behavioral Neuroscience, 103, 131–143.

    Article  PubMed  Google Scholar 

  • MAIER, S. F., DAVIES, S., GRAU, J. W., JACKSON, R. L., MORRISON, D., MOYE, T., MADDEN, J., & BARCHAS, J. D. (1980). Opiate antagonists and the long-term analgesia reaction induced by inescapable shock. Journal of Comparative and Physiological Psychology, 94, 1172–1184.

    Article  PubMed  Google Scholar 

  • MAIER, S. F., DRUGAN, R., GRAU, J. W., HYSON, R., MACLENNAN, A. J., MOYE, T., MADDEN, J., & BARCHAS, J. D. (1983). Learned helplessness, pain inhibition and the endogenous opiates. In M. D. Zeiler & P. Harzern (Eds.), Advances in animal behavior (Vol. 3, pp. 275–323). New York: Wiley & Sons.

    Google Scholar 

  • MAIER, S. F., & SELIGMAN, M. E. P. (1976). Learned helplessness: Theory and evidence. Journal of Experimental Psychology: General, 105, 3–46.

    Article  Google Scholar 

  • MEEK, L. R., GIBSON, B. M., & KEMBLE, E. D. (1989). Effects of fluprazine hydrochloride on reactivity to a nonconspecific intruder. The Psychological Record, 39, 203–210.

    Google Scholar 

  • MICZEK, K. A., THOMPSON, M. L., & SHUSTER, L. (1982). Opioid-like analgesia in defeated mice. Science, 215, 1520–1522.

    Article  PubMed  Google Scholar 

  • MICZEK, K. A., THOMPSON, M. L., & SHUSTER, L. (1986). Analgesia following defeat in an aggressive encounter: Development of tolerance and changes in opioid receptors. In D. D. Kelly (Ed.), Annals of the New York Academy of Sciences (Vol. 467, pp. 14–29).

    Article  PubMed  Google Scholar 

  • MINEKA, S. (1979). The role of fear in theories of avoidance learning, flooding, and extinction. Psychological Bulletin, 86, 985–1010.

    Article  Google Scholar 

  • PINEL, J. P. J., & TREIT, D. (1978). Burying as a defensive response in rats. Journal of Comparative & Physiological Psychology, 92, 708–712.

    Article  Google Scholar 

  • PINEL, J. P. J., & TREIT, D. (1981). The conditioned defensive burying paradigm and behavioral neuroscience. In T. E. Robinson (Ed.), Behavioral contributions to brain research (pp. 212–234). Oxford, England: Oxford University Press.

    Google Scholar 

  • RODGERS, R. J. (1989). Ethoexperimental analysis of “stress” analgesia. In R. J. Blanchard, P. F. Brain, D. C. Blanchard, & S. Parmigiani, Ethoexperimental approaches to the study of behavior (pp. 214–228). Dordrecht: Martinus Nijhoff.

    Google Scholar 

  • RODGERS, HENDRIE, C. A. (1982). Agonistic behaviour in rats: Evidence for non-involvement of opioid mechanisms. Physiology & Behavior, 29, 85–90.

    Article  Google Scholar 

  • RODGERS, R. J., & RANDALL, J. I. (1985). Social conflict analgesia: Studies on naloxone antagonism and morphine cross-tolerance in male DBA/2 mice. Pharmacology, Biochemistry, & Behavior, 23, 883–887.

    Article  Google Scholar 

  • RODGERS, R. J., & Randall, J. I. (1986a). Acute non-opioid analgesia in defeated male mice. Physiology & Behavior, 36, 947–950.

    Article  Google Scholar 

  • RODGERS, R. J., & RANDALL, J. I. (1986b). Extended attack from a resident conspecific is critical to the development of long-lasting analgesia in male intruder mice. Physiology & Behavior, 38, 427–430.

    Article  Google Scholar 

  • RODGERS, R. J., & RANDALL, J. I. (1986c). Resident’s scent: A critical factor in acute analgesia reaction to defeat experience in male mice. Physiology & Behavior, 37, 317–322.

    Article  Google Scholar 

  • RODGERS, R. J., & RANDALL, J. I. (1987). Potent inhibition of non-opioid defeat analgesia in male mice by benzodiazepine antagonist Ro15-3505. Physiology & Behavior, 42, 461–464.

    Article  Google Scholar 

  • RODGERS, R. J., & RANDALL, J. I. (1988). Environmentally-induced analgesia: Situational factors, mechanisms and significance. In R. J. Rodgers & S. J. Cooper (Eds.), Endorphins, opiates, and behavioral processes (pp. 107–142). Chichester: J. Wiley.

    Google Scholar 

  • WILLIAMS, J. L. (1982). Influence of shock controllability by dominant rats on subsequent attack and defense behaviors toward colony intruders. Animal Learning and Behavior, 10, 305–313.

    Article  Google Scholar 

  • WILLIAMS, J. L. (1984). Influence of postpartum shock controllability on subsequent maternal behavior in rats. Animal Learning & Behavior, 12, 209–216.

    Article  Google Scholar 

  • WILLIAMS, J. L. (1987a). Effects of shock controllability on alpha male aggression and defense, defeat of intruders, and defensive burying. The Psychological Record, 37, 369–380.

    Article  Google Scholar 

  • WILLIAMS, J. L. (1987b). Influence of conspecific stress odors and shock controllability on conditioned defensive burying. Animal Learning and Behavior, 15, 333–341.

    Article  Google Scholar 

  • WILLIAMS, J. L. (1989). Ethoexperimental analysis of stress, contextual odors, and defensive behaviors. In R. J. Blanchard, P. F. Brain, D. C. Blanchard, & S. Parmigiani, Ethoexperimental approaches to the study of behavior. (pp. 214–228). Dordrecht: Martinus Nijhoff.

    Chapter  Google Scholar 

  • WILLIAMS, J. L., JUST, J. M., & WORLAND, P. D. (1990). Effects of repeated defeat as a colony intruder on subsequent conditioned and sensitization hypoalgesic reactions and their reversibility by naltrexone. Manuscript submitted for publication.

    Google Scholar 

  • WILLIAMS, J. L., & LIERLE, D. M. (1986). Effects of stress controllability, immunization, and therapy on the subsequent defeat of colony intruders. Animal Learning and Behavior, 14(3), 305–314.

    Article  Google Scholar 

  • WILLIAMS, J. L., & LIERLE, D. M. (1988). Effects of repeated defeat by a dominant conspecific on subsequent pain sensitivity, open-field activity, and escape learning. Animal Learning & Behavior, 16, 477–485.

    Article  Google Scholar 

  • WILLIAMS, J. L., ROGERS, A. G., & ADLER, A. P. (1990). Exposure to conspecific and predatory odors reduce subsequent fear reactions following prod shock. Animal Learning & Behavior, 18(4), 453–461.

    Article  Google Scholar 

  • WILLIAMS, J. L., & SCOTT, D. K. (1989). Influence of conspecific and predatory stressors and the associated odors on defensive burying and freezing. Animal Learning & Behavior, 17, 383–393.

    Article  Google Scholar 

  • WILLIAMS, J. L., WORLAND, P. D., & SMITH, M. G. (1990a). Defeat-induced hypoalgesia in the rat: Effects conditioned odors, naltrexone, and extinction. Journal of Experimental Psychology: Animal Behavioral Processes 16, 4 345–357.

    Google Scholar 

  • WILLIAMS, J. L., WORLAND, P. D., & SMITH, M. G. (1990b). Effects of shock controllability and odors from shocked conspecifics on formalin-induced hypoalgesia. Manuscript submitted for publication.

    Google Scholar 

  • WORLAND, P. D., JUST, J. M., & WILLIAMS, J. L. (1990). Effects of conspecific, predatory, and shock-induced stress, and their associated odors, on hypoalgesia and freezing: Conditioning versus sensitization. Manuscript submitted for publication.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

I acknowledge the invaluable assistance of Paul Worland, Marc Just, Melinda Smith, Amy Rogers, Allison Adler, and David Scott. This research was supported by USPHS Research Grant 1-RO1-MH43815-03 and endowment funds from the Samual B. Cummings Professorship in Psychology.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Williams, J.L. Conditioned Defensive Responses and Hypoalgesia in Rats Exposed to Defeat and Alpha-Colony Odors. Psychol Rec 41, 271–297 (1991). https://doi.org/10.1007/BF03395110

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF03395110

Navigation