Abstract
These studies demonstrated the acquisition and extinction of conditioned tolerance to the analgesic effect of nicotine in rats. In Experiment 1, distinctive environmental cues were either paired or unpaired with nicotine. Following acquisition, the paired group was more tolerant to nicotine than the unpaired and saline groups. Conditioned tolerance was extinguished in the paired group after placebo sessions in the distinctive environment. Experiment 2 examined whether the distinctive environment functioned as a CS or as an occasion setter for injection cues. After acquisition, exposure to the distinctive environment, with or without placebo injections, resulted in extinction. This demonstrates that the distinctive environment served as a CS, not as an occasion setter for injection cues.
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References
Baker, T. B., &Tiffany, S. T. (1985). Morphine tolerance as habituation.Psychological Review,92, 78–108.
Bevins, R. A., Besheer, J., &Pickett, K. S. (2001). Nicotine-conditioned locomotor activity in rats: Dopaminergic and GABAergic influences on conditioned expression.Pharmacology Biochemistry & Behavior,68, 135–145.
Bevins, R. A., &Palmatier, M. I. (2003). Nicotine-conditioned locomotor sensitization in rats: Assessment of the US-preexposure effect.Behavioural Brain Research,143, 65–74.
Bouton, M. E., &Swartzentruber, D. (1986). Analysis of the associative and occasion-setting properties of contexts participating in a Pavlovian discrimination.Journal of Experimental Psychology: Animal Behavior Processes,12, 333–350.
Bouton, M. E., &Swartzentruber, D. (1991). Sources of relapse after extinction in Pavlovian and instrumental learning.Clinical Psychology Review,11, 123–140.
Brooks, D. C., Karamanlian, B. R., &Foster, V. L. (2001). Extinction and spontaneous recovery of ataxic tolerance to ethanol in rats.Psychopharmacology,153, 491–496.
Caggiula, A. R., Donny, E. C., Chaudhri, N., Perkins, K. A., Evans-Martin, F. F., &Sved, A. F. (2002). Importance of nonpharmacological factors in nicotine self-administration.Physiology & Behavior,77, 683–687.
Caggiula, A. R., Donny, E. C., White, A. R., Chaudhri, N., Booth, S., Gharib, M. A., et al. (2001). Cue dependency of nicotine self-administration and smoking.Pharmacology Biochemistry & Behavior,70, 515–530.
Caggiula, A. R., Donny, E. C., White, A. R., Chaudhri, N., Booth, S., Gharib, M. A., et al. (2002). Environmental stimuli promote the acquisition of nicotine self-administration in rats.Psychopharmacology,163, 230–237.
Caggiula, A. R., Epstein, L. H., Antelman, S. M., Saylor, S. S., Knopf, S., Perkins, K. A., &Stiller, R. (1993). Acute stress or corticosterone administration reduces responsiveness to nicotine: Implications for a mechanism of conditioned tolerance.Psychopharmacology,111, 499–507.
Caggiula, A. R., Epstein, L. H., Antelman, S. M., Saylor, S. S., Perkins, K. A., Knopf, S., &Stiller, R. (1991). Conditioned tolerance to the anorectic effect and corticosterone-elevating effects of nicotine.Pharmacology Biochemistry & Behavior,40, 53–59.
Caggiula, A. R., Epstein, L. H., &Stiller, R. L. (1989). Changing environmental cues reduces tolerance to nicotine-induced anorexia.Psychopharmacology,99, 389–392.
Cepeda-Benito, A., Davis, K. W., Reynoso, J. T., &Harraid, J. H. (2005). Associative and behavioral tolerance to the analgesic effects of nicotine in rats: Tail-flick and paw-lick assays.Psychopharmacology,180, 224–233.
Cepeda-Benito, A., Reynoso, J. [T.], &Erath, S. A. (2000). Dose-response analyses of associative tolerance to nicotine analgesia in the rat: Tail-flick and hot-plate tests.Experimental & Clinical Psychopharmacology,8, 112–116.
Cepeda-Benito, A., Reynoso, J. [T.], &McDaniel, E. H. (1998). Associative tolerance to nicotine analgesia in the rat: Tail-flick and hot-plate tests.Experimental & Clinical Psychopharmacology,6, 248–254.
Cepeda-Benito, A., &Tiffany, S. T. (1995). Role of drug-administration cues in the associative control of morphine tolerance in the rat.Psychopharmacology,122, 312–316.
Dafters, R., Hetherington, M., &McCartney, H. (1983). Blocking and sensory preconditioning effects in morphine analgesic tolerance: Support for a Pavlovian conditioning model of drug tolerance.Quarterly Journal of Experimental Psychology,35B, 1–11.
Davis, K. W., Cepeda-Benito, A., Harraid, J. H., &Wellman, P. J. (2005). Plasma corticosterone in the rat in response to nicotine and saline injections in a context previously paired or unpaired with nicotine.Psychopharmacology,180, 466–472.
Deffner-Rappold, C., Azorlosa, J. L., &Baker, J. D. (1996). Acquisition and extinction of context-specific morphine withdrawal.Psychobiology,24, 219–226.
Epstein, L. H., Caggiula, A. R., Perkins, K. A., McKenzie, S. J., &Smith, J. A. (1991). Conditioned tolerance to the heart rate effects of smoking.Pharmacology Biochemistry & Behavior,39, 15–19.
Epstein, L. H., Caggiula, A. R., &Stiller, R. L. (1989). Environmentspecific tolerance to nicotine.Psychopharmacology,97, 235–237.
Falls, W. A., &Kelsey, J. E. (1989). Procedures that produce contextspecific tolerance to morphine in rats also produce context-specific withdrawal.Behavioral Neuroscience,103, 842–849.
Fanselow, M. S., &German, C. (1982). Explicitly unpaired delivery of morphine and the test situation: Extinction and retardation of tolerance to the suppressing effects of morphine on locomotor activity.Behavioral & Neural Biology,35, 231–241.
Grahame, N. J., Hallam, S. C., Geier, L., &Miller, R. R. (1990). Context as an occasion setter following either CS acquisition and extinction or CS acquisition alone.Learning & Motivation,21, 237–265.
Greeley, J., &Cappell, H. (1985). Associative control of tolerance to the sedative and hypothermic effects of chlordiazepoxide.Psychopharmacology,86, 487–493.
Griffiths, J. W., &Goudie, A. J. (1986). Analysis of the role of drugpredictive environmental stimuli in tolerance to the hypothermic effects of the benzodiazepine midazolam.Psychopharmacology,90, 513–521.
Grisel, J. E., Wiertelak, E. P., Watkins, L. R., &Maier, S. F. (1994). Route of morphine administration modulates conditioned analgesic tolerance and hyperalgesia.Pharmacology Biochemistry & Behavior,49, 1029–1035.
Holland, P. C. (1983). Occasion setting in Pavlovian feature positive discriminations. In M. L. Commons, R. J. Herrnstein, & A. R. Wagner (Eds.),Quantitative analyses of behavior: Discrimination processes (Vol. 4, pp. 183–206). New York: Ballinger.
Holland, P. C. (1986). Temporal determinants of occasion setting in feature-positive discriminations.Animal Learning & Behavior,14, 111–120.
Kamin, L. J. (1969). {bcPredictability, surprise, attention, and conditioning}. In B. A. Campbell & R. M. Church (Eds.),Punishment and aversive Behavior (pp. 279–296). New York: Appleton-Century-Crofts.
Kim, J. A., Siegel, S., &Patenall, V. R.A. (1999). Drug-onset cues as signals: Intraadministration associations and tolerance.Journal of Experimental Psychology: Animal Behavior Processes,25, 491–504.
King, D. A., Bouton, M. E., &Musty, R. E. (1987). Associative control of tolerance to the sedative effect of a short-acting benzodiazepine.Behavioral Neuroscience,101, 104–114.
Krank, M. D. (1987). Conditioned hyperalgesia depends on the pain sensitivity measure.Behavioral Neuroscience,101, 854–857.
MacRae, J. R., &Siegel, S. (1987). Extinction of tolerance to the analgesic effect of morphine: Intracerebroventricular administration and effects of stress.Behavioral Neuroscience,101, 790–796.
Mansfield, J. G., &Cunningham, C. L. (1980). Conditioning and extinction of tolerance to the hypothermic effect of ethanol in rats.Journal of Comparative & Physiological Psychology,94, 962–969.
Millin, P. M., &Riccio, D. C. (2002). Spontaneous recovery of tolerance to the analgesic effect of morphine.Physiology & Behavior,75, 465–471.
Paletta, M. S., &Wagner, A. R. (1986). Development of context-specific tolerance to morphine: Support for a dual-process interpretation.Behavioral Neuroscience,100, 611–623.
Poulos, C. X., &Cappell, H. (1991). Homeostatic theory of drug tolerance: A general model of physiological adaptation.Psychological Review,98, 390–408.
Ramos, B. M. C., Siegel, S., &Bueno, J. L. O. (2002). Occasion setting and drug tolerance.Integrative Physiological & Behavioral Science, 37, 165–177.
Ramsay, D. S., &Woods, S. C. (1997). Biological consequences of drug administration: Implications for acute and chronic tolerance.Psychological Review,104, 170–193.
Rescorla, R. A. (1985). Conditioned inhibition and facilitation. In R. R. Miller & N. E. Spears (Eds.), Information processing in animals: Conditioned inhibition (pp. 299–326). Hillsdale, NJ: Erlbaum.
Rescorla, R. A. (1986). Extinction of facilitation.Journal of Experimental Psychology: Animal Behavior Processes,12, 16–24.
Siegel, S. (1975). Evidence from rats that morphine tolerance is a learned response.Journal of Comparative & Physiological Psychology,89, 498–506.
Siegel, S. (1977). Morphine tolerance acquisition as an associative process.Journal of Experimental Psychology: Animal Behavior Processes,3, 1–13.
Siegel, S. (1978). Tolerance to the hyperthermic effect of morphine in the rat is a learned response.Journal of Comparative & Physiological Psychology,92, 1137–1149.
Siegel, S. (1987). Pavlovian conditioning and ethanol tolerance. In K. O. Lindros, R. Ylikahri, & K. Kiianmaa (Eds.), Advances in biomedical alcohol research (pp. 25–36). Oxford: Pergamon.
Siegel, S., &Allan, L. G. (1998). Learning and homeostasis: Drug addiction and the McCollough effect.Psychological Bulletin,124, 230–239.
Siegel, S., Baptista, M. A. S., Kim, J. A., McDonald, R. V., &Weise-Kelly, L. (2000). Pavlovian psychopharmacology: The associative basis of tolerance.Experimental & Clinical Psychopharmacology,8, 276–293.
Siegel, S., Hinson, R. E., &Krank, M. D. (1981). Morphine-induced attenuation of morphine tolerance.Science,212, 1533–1534.
Siegel, S., &Ramos, B. M. C. (2002). Applying laboratory research: Drug anticipation and the treatment of drug addiction.Experimental & Clinical Psychopharmacology,10, 162–183.
Siegel, S., Sherman, J. E., &Mitchell, D. (1980). Extinction of morphine analgesic tolerance.Learning & Motivation,11, 289–301.
Swartzentruber, D. (1991). Blocking between occasion setters and contextual stimuli.Journal of Experimental Psychology: Animal Behavior Processes,17, 163–173.
Swartzentruber, D. (1995). Modulatory mechanisms in Pavlovian conditioning.Animal Learning & Behavior,23, 123–143.
Tiffany, S. T., Drobes, D. J., &Cepeda-Benito, A. (1992). Contribution of associative and nonassociative processes to the development of morphine tolerance.Psychopharmacology,109, 185–190.
U. S. Department of Health & Human Services (1997). Preliminary results from the 1996 National Household Survey on Drug Abuse. Washington, DC: Substance Abuse & Mental Health Administration.
Walter, T. A., &Riccio, D. C. (1983). Overshadowing effects in stimulus control of morphine analgesic tolerance.Behavioral Neuroscience,97, 658–662.
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We dedicate this article to the memory of Jim McConnell. This research was funded by a College of Arts and Sciences Support and Development Award to the first author.
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Azorlosa, J.L., Johnson, C.E. & McConnell, J.J. Acquisition and extinction of conditioned nicotine analgesic tolerance. Learning & Behavior 34, 262–268 (2006). https://doi.org/10.3758/BF03192882
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DOI: https://doi.org/10.3758/BF03192882