Abstract
Three experiments are reported that explore the opioid/nonopioid nature of environmentally induced antinociception in pentobarbital-anesthetized rats. In Experiment 1, the minimum shock intensity and duration that elicits antinociception was established and two alternative descriptions of the tradeoff between shock intensity and duration were evaluated: the coulometric relationship (duration × intensity) and an extension of Stevens’s power law (duration × intensity3.5). The results support the power law. In Experiments 2 and 3, the relationship between shock severity and the form of the antinociception elicited was examined. It was found that the least severe shock schedules produced a naltrexone-insensitive “nonopioid” antinociception. Increasing shock severity elicited an “opioid” antinociception that was attenuated by naltrexone. When shock severity was increased further, the antinociception again became naltrexone insensitive. Implications of the results are discussed.
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Basbaum, A. I., & Fields, H. L. (1984). Endogenous pain control systems: Brainstem spinal pathways and endorphin circuitry. Annual Review of Neuroscience, 7, 309–338.
Campbell, B. A., & Masterson, F. A. (1969). Psychophysics of punishment. In B. A. Campbell & R. M. Church (Eds.), Punishment and aversive behavior (pp. 3–42). New York: Appleton-Century-Crofts.
Cannon, J. T., Prieto, G. J., Lee, A., & Liebeskind, J. C. (1982). Evidence for opioid and non-opioid forms of stimulation-produced analgesia in rat. Brain Research, 243, 315–321.
Cannon, J. T., Terman, G. W., Lewis, J. W., & Liebeskind, J. C. (1984). Body region shocked need not critically define the neurochemical basis of stress analgesia. Brain Research, 323, 316–319.
Chance, W. T. (1980). Autoanalgesia: Opiate and non-opiate mechanisms. Neuroscience & Biobehavioral Reviews, 4, 55–67.
Church, R. M., Raymond, G. A., & Bauchamp, R. D. (1967). Response suppression as a function of intensity and duration of punishment. Journal of Comparative & Physiological Psychology, 63, 39–44.
D’Amour, F. E., & Smith, D. L. (1941). A method for determining loss of pain sensation. Journal of Pharmacology & Experimental Therapeutics, 72, 74–79.
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.
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 gray matter: Functional, anatomical and immunohistochemical organization (NATO ASI Series, pp. 151–173). New York: Plenum.
Grau, J. W. (1984). The influence of naloxone on shock-induced freezing and analgesia. Behavioral Neuroscience, 98, 278–292.
Grau, J. W. (1987a). The central representation of an aversive event maintains the opioid and nonopioid forms of analgesia. Behavioral Neuroscience, 101, 272–288.
Grau, J. W. (1987b). The variables which control the activation of analgesic systems: Evidence for a memory hypothesis and against the coulometric hypothesis. Journal of Experimental Psychology: Animal Behavior Processes, 13, 215–225.
Grau, J. W., Biles, M. K., & Illich, P. A. (1991). The impact of naltrexone and morphine tolerance on mild shock-induced hypoalgesia. Psychobiology, 19, 85–90.
Grau, J. W., Hyson, R. L., Maier, S. F., Madden, J., & Barchas, J. D. (1981). Long-term stress-induced analgesia and activation of the opiate system. Science, 213, 1409–1411.
Grau, J. W., Illich, P. A., Chen, P.-S., & Meagher, M. W. (1991). Role of cholinergic systems in pain modulation: I. Impact of scopolamine on environmentally induced hypoalgesia and pain reactivity. Behavioral Neuroscience, 105, 62–81.
Grau, J. W., Salinas, J. A., Illich, P. A., & Meagher, M. W. (1990). Associative learning and memory for an antinociceptive response in the spinalized rat. Behavioral Neuroscience, 104, 489–494.
Grisel, J. E., Fleshner, M., Watkins, L. R., & Maier, S. F. (1993). Opioid and nonopioid interactions in two forms of stress-induced analgesia. Pharmacology, Biochemistry & Behavior, 45, 161–172.
Hyson, R. L., Ashcraft, L. J., Drugan, R. C., Grau, J. W., & Maier, S. F. (1982). Extent and control of shock affects naltrexone sensitivity of stress-induced analgesia and reactivity to morphine. Pharmacology, Biochemistry & Behavior, 17, 1019–1025.
Kahneman, D., Frederickson, B. L., Schreiber, C. A., & Redelmeier, D. A. (1993). When more pain is preferred to less: Adding a better end. Psychological Science, 4, 401–405.
Kirchgessner, A. L., Bodnar, R. J., & Pasternak, G. W. (1982). Naloxazone and pain-inhibitory systems: Evidence for a collateral inhibition model. Pharmacology, Biochemistry, & Behavior, 17, 1175–1179.
Klein, M. V., Lovaas, K. M., Terman, G. W., & Liebeskind, J. C. (1983). The effects of decerebration and spinal transection on three discrete forms of stress-induced analgesia. Neuroscience Abstracts, 9, 795.
Lewis, J. W., Cannon, J. T., & Liebeskind, J. C. (1980). Opioid and nonopioid mechanisms of stress analgesia. Science, 208, 623–625.
Lichtman, A. H., & Fanselow, M. S. (1991). Opioid and nonopioid conditioned analgesia: The role of spinal opioid, noradrenergic, and serotonergic systems. Behavioral Neuroscience, 105, 687–698.
Maier, S. F. (1989). Determinants of the nature of environmentally induced hypoalgesia. Behavioral Neuroscience, 103, 131–143.
Maier, S. F., Davies, S., Grau, J. W., Jackson, R. L., Morrison, D. H., Moye, T., Madden, J., & Barchas, J. D. (1980). Opiate antagonists and long-term analgesic reaction induced by inescapable shock in rats. Journal of Comparative & Physiological Psychology, 94, 1172–1183.
Meagher, M. W., Barter, J., King, T. E., & Grau, J. W. (1995). Presentation of a distractor speeds the decay of a pentobarbital-insensitive nonopioid hypoalgesia in rats. Psychobiology, 23, 314–321.
Meagher, M. W., Chen, P.-S., Salinas, J. A., & Grau, J. W. (1993). Activation of the opioid and nonopioid hypoalgesic systems at the level of the brainstem and spinal cord: Does a coulometric relation predict the emergence or form of environmentally induced hypoalgesia? Behavioral Neuroscience, 107, 493–505.
Meagher, M. W., Grau, J. W., & King, R. A. (1989). The role of the frontal cortex in analgesia: Lesions of the frontal cortex block the analgesia observed after brief, but not long, shocks. Behavioral Neuroscience, 103, 1366–1371.
Meagher, M. W., Grau, J. W., & King, R. A. (1990). The role of supraspinal systems in environmentally induced antinociception: The effects of spinalization and decerebration on brief and long shock-induced antinociception. Behavioral Neuroscience, 104, 328–338.
Melzack, R., & Wall, P. D. (1965). Pain mechanisms: A new theory. Science, 150, 971–979.
Steinman, J. L., Faris, P. L., Mann, P. E., Olney, J. W., Komisaruk, B. R., Willis, W. D., & Bodnar, R. J. (1990). Antagonism of morphine analgesia by nonopioid cold-water swim analgesia: Direct evidence for collateral inhibition. Neuroscience & Biobehavioral Reviews, 14, 1–7.
Stevens, S. S. (1962). The surprising simplicity of sensory metrics. American Psychologist, 17, 29–39.
Stevens, S. S., Carton, A. S., & Shickman, G. M. (1958). A scale of apparent intensity of electric shock. Journal of Experimental Psychology, 56, 328–334.
Terman, G. W., Shavit, Y., Lewis, J. W., Cannon, J. T., & Liebeskind, J. C. (1984). Intrinsic mechanisms of pain inhibition: Activation by stress. Science, 226, 1270–1277.
Watkins, L. R., Drugan, R., Hyson, R. L., Moye, T. B., Ryan, S. M., Mayer, D. J., & Maier, S. F. (1984). Opiate and non-opiate analgesia induced by inescapable tail-shock: Effects of dorsolateral funiculus lesions and decerebration. Brain Research, 291, 325–336.
Watkins, L. R., Kinscheck, I. B., & Mayer, D. J. (1983). The neural basis of footshock analgesia: The effect of periaqueductal gray lesions and decerebration. Brain Research, 276, 317–324.
Watkins, L. R., & Mayer, D. J. (1982). Organization of endogenous opiate and nonopiate pain control systems. Science, 216, 1185–1192.
Watkins, L. R., & Mayer, D. J. (1986). Multiple endogenous opiate and nonopiate analgesic systems: Evidence of their existence and clinical implications. In D. D. Kelly (Ed.), Stress-induced analgesia (Annals of the New York Academy of Sciences, Vol. 467, pp. 273–299). New York: New York Academy of Sciences.
Watkins, L. R., Wiertelak, E. P., Grisel, J. E., Silbert, L. H., & Maier, S. F. (1992). Parallel activation of multiple spinal opiate systems appears to mediate ‘non-opiate’ stress-induced analgesias. Brain Research, 594, 99–108.
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This research was supported in part by grants from the National Science Foundation (BNS 881981) and National Institute of Mental Health (R01 MH48994) to J. W. G. and M. W. M.
The authors thank Robin Joynes and Paul Illich for their help and advice.
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Grau, J.W., King, T.E., Burks, K.D. et al. The relationship between shock severity and the form of the antinociception observed in pentobarbital-anesthetized rats. Psychobiology 24, 71–84 (1996). https://doi.org/10.3758/BF03331957
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DOI: https://doi.org/10.3758/BF03331957