The paradox of drug taking: The role of the aversive effects of drugs

Physiology and Behavior

Volumn 103, Issue 1, 2011, Pages 69-78

  Riley, Anthony L ^a  

^a AMERICAN UNIVERSITY   (United States)

Author keywords

Balance of reward and aversion; Drugs of abuse; Taste aversions

Indexed keywords

ALCOHOL; COCAINE; MORPHINE;

ADAPTATION; ARTICLE; DRUG ABUSE; DRUG USE; EATING; FOOD INTAKE; GENETIC MODEL; HUMAN; PRIORITY JOURNAL; REWARD; TASTE AVERSION;

ANIMALS; AVOIDANCE LEARNING; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG TOXICITY; EATING; HUMANS; MODELS, PSYCHOLOGICAL; RATS; REWARD; SPECIES SPECIFICITY; SUBSTANCE-RELATED DISORDERS;

EID: 79952486511     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2010.11.021     Document Type: Article

References (108)

1. Woods S.C. The eating paradox: how we tolerate food. Psychol Rev 1991, 98:488-505.
2. Koob G.F., Le Moal M. Neurobiology of addiction 2006, Academic Press, Boston.
3. Meyer J.S., Quenzer L.F. Psychopharmacology: drugs, the brain, and behavior 2005, Sinauer Associates, Inc., Sunderland, MA.
4. Koob G.F., Le Moal M. Addiction and the brain antireward system. Annu Rev Psychol 2008, 59:29-53.
5. Koob G.F., Volkow N.D. Neurocircuitry of addiction. Neuropsychopharmacol Rev 2009, 1-22.
6. Hyman S.E., Malenka R.C., Nestler E.J. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 2006, 29:565-598.
7. Nestler E.J. Historical review: molecular and cellular mechanisms of opiate and cocaine addiction. Trends Pharmacol Sci 2004, 25:210-218.
8. Baker T.B., Cannon D.S. Alcohol and taste-mediated learning. Addict Behav 1982, 7:211-230.
9. Gaiardi M., Bartoletti M., Bacchi A., et al. Role of repeated exposure to morphine in determining its affective properties: place and taste conditioning studies in rats. Psychopharmacol Berl 1991, 103:183-186.
10. Riley A.L., Davis C.M., Roma P.G. Strain differences in taste aversion learning: implications for animal models of drug abuse. Conditioned taste aversion: behavioral and neural processes 2009, 226-261. Oxford University Press, New York. S. Reilly, T.R. Schachtman (Eds.).
11. Riley A.L., Simpson G.R. The attenuating effects of drug preexposure on taste aversion conditioning: generality, experimental parameters, underlying mechanisms and implications for drug use and abuse. Contemporary learning theory 2001, 505-559. Lawrence Erlbaum Associates, Hillsdale, NJ. 2nd ed. R.R. Mowrer, S.B. Klein (Eds.).
12. Stolerman I.P., D'Mello G.D. Oral self-administration and the relevance of conditioned taste aversions. Advances in behavioral pharmacology 1981, 169-214. L. Erlbaum, Hillsdale, NJ. T. Thompson, P.B. Dews, W.A. McKim (Eds.).
13. Weeks J.R. Experimental morphine addiction: method for automatic intravenous injections in unrestrained rats. Science 1962, 138:143-144.
14. Cappell H., LeBlanc A.E. Gustatory avoidance conditioning by drugs of abuse: relationships to general issues in research on drug dependence. Food aversion learning 1977, 133-167. Plenum Publishing, New York. N.W. Milgram, L. Krames, T.M. Alloway (Eds.).
15. Hunt T., Amit Z. Conditioned taste aversion induced by self-administered drugs: paradox revisited. Neurosci Biobehav Rev 1987, 11:107-130.
16. Riley A.L., Tuck D.L. Conditioned taste aversions: a behavioral index of toxicity. Experimental assessments and clinical applications of conditioned food aversions 1985, 272-292. The New York Academy of Sciences, New York. N.S. Braveman, P. Bronstein (Eds.).
17. Garcia J., Kimeldorf D.J., Koelling R.A. Conditioned aversion to saccharin resulting from exposure to gamma radiation. Science 1955, 122:157-158.
18. Garcia J., Ervin F.R. Gustatory-visceral and telereceptor-cutaneous conditioning: adaptation in internal and external milieus. Commun Behav Biol A 1968, 1:389-415.
19. Revusky S., Garcia J. Learned associations over long delays. Psychology of learning and motivation: advances in research and theory 1970, Volume 4:1-84. Academic Press, New York. G. Bower, J. Spence (Eds.).
20. Riley A.L., Freeman K.B. Conditioned flavor aversions: assessment of drug-induced suppression of food intake. Current protocols in neuroscience 2004, 8.5E.1-8.6R.12. Wiley, New York. J.N. Crawley, C. Gerfen, R. McKay, M. Rogawski, D.R. Sibley, P. Skolnick (Eds.).
21. Rozin P., Kalat J.W. Specific hungers and poison avoidance as adaptive specializations of learning. Psychol Rev 1971, 78:459-486.
22. Freeman K.B., Riley A.L. The origins of conditioned taste aversion learning: a historical analysis. Conditioned taste aversion: behavioral and neural processes 2009, 9-33. Oxford University Press, New York. S. Reilly, T.R. Schachtman (Eds.).
23. Gamzu E. The multifaceted nature of taste-aversion-inducing agents: is there a single common factor?. Learning mechanisms in food selection 1977, 477-510. Baylor University Press, Waco, TX. L.M. Barker, M.R. Best, M. Domjan (Eds.).
24. Gamzu E., Vincent G., Boff E. A pharmacological perspective of drugs used in establishing conditioned food aversions. Experimental assessments and clinical applications of conditioned food aversions 1985, 231-249. The New York Academy of Sciences, New York. N.S. Braveman, P. Bronstein (Eds.).
25. Goudie A.J. Aversive stimulus properties of drugs. Neuropharmacology 1979, 18:971-979.
26. White N., Sklar L., Amit Z. The reinforcing action of morphine and its paradoxical side effect. Psychopharmacol Berl 1977, 52:63-66.
27. Wise R.A., Yokel R.A., DeWit H. Both positive reinforcement and conditioned aversion from amphetamine and from apomorphine in rats. Science 1976, 191:1273-1275.
28. Martin G.M., Bechara A., van der Kooy D. Morphine preexposure attenuates the aversive properties of opiates without preexposure to the aversive properties. Pharmacol Biochem Behav 1988, 30:687-692.
29. Simpson G.R., Riley A.L. Morphine preexposure facilitates morphine place preference and attenuates morphine taste aversion. Pharmacol Biochem Behav 2005, 80:471-479.
30. Wang Y.C., Huang A.C., Hsiao S. Paradoxical simultaneous occurrence of amphetamine-induced conditioned taste aversion and conditioned place preference with the same single drug injection: a new "pre- and post-association" experimental paradigm. Pharmacol Biochem Behav 2010, 95:80-87.
31. Lynch W.J., Carroll M.E. Regulation of drug intake. Exp Clin Psychopharmacol 2001, 9:131-143.
32. Cunningham C.L., Gremel C.M., Groblewski P.A. Genetic influences on conditioned taste aversion. Conditioned taste aversion: behavioral and neural processes 2009, 387-421. Oxford University Press, New York. S. Reilly, T.R. Schachtman (Eds.).
33. Elkins R.L. Separation of taste-aversion-prone and taste-aversion-resistant rats through selective breeding: implications for individual differences in conditionability and aversion-therapy alcoholism treatment. Behav Neurosci 1986, 100:121-124.
34. Horowitz G.P., Whitney G. Alcohol-induced conditioned aversion: genotypie specificity in mice (Mus musculus). J Comp Physiol Psychol 1975, 89:340-346.
35. Risinger F.O., Cunningham C.L. Genetic differences in ethanol-induced hyperglycemia and conditioned taste aversion. Life Sci 1992, 50:PL113-PL118.
36. Risinger F.O., Cunningham C.L. Ethanol-induced conditioned taste aversion in BXD recombinant inbred mice. Alcohol Clin Exp Res 1998, 22:1234-1244.
37. McClearn G.E., Rodgers D.A. Differences in alcohol preference among inbred strains of mice. Q J Stud Alcohol 1959, 20:691-695.
38. Broadbent J., Muccino K.J., Cunningham C.L. Ethanol-induced conditioned taste aversion in 15 inbred mouse strains. Behav Neurosci 2002, 116:138-148.
39. Cannon D.S., Leeka J.K., Block A.K. Ethanol self-administration patterns and taste aversion learning across inbred rat strains. Pharmacol Biochem Behav 1994, 47:795-802.
40. Kosten T.A., Ambrosio E. HPA axis function and drug addictive behaviors: insights from studies with Lewis and Fischer 344 inbred rats. Psychoneuroendocrinology 2002, 27:35-69.
41. Stohr T., Schulte Wermeling D., Weiner I., Feldon J. Rat strain differences in open-field behavior and the locomotor stimulating and rewarding effects of amphetamine. Pharmacol Biochem Behav 1998, 59:813-818.
42. Stohr T., Szuran T., Welzl H., et al. Lewis/Fischer rat strain differences in endocrine and behavioural responses to environmental challenge. Pharmacol Biochem Behav 2000, 67:809-819.
43. Ambrosio E., Goldberg S.R., Elmer G.I. Behavior genetic investigation of the relationship between spontaneous locomotor activity and the acquisition of morphine self-administration behavior. Behav Pharmacol 1995, 6:229-237.
44. Martin S., Manzanares J., Corchero J., et al. Differential basal proenkephalin gene expression in dorsal striatum and nucleus accumbens, and vulnerability to morphine self-administration in Fischer 344 and Lewis rats. Brain Res 1999, 821:350-355.
45. Suzuki T., George F.R., Meisch R.A. Differential establishment and maintenance of oral ethanol reinforced behavior in Lewis and Fischer 344 inbred rat strains. J Pharmacol Exp Ther 1988, 245:164-170.
46. Taylor A.N., Tio D.L., Bando J.K., Romeo H.E., Prolo P. Differential effects of alcohol consumption and withdrawal on circadian temperature and activity rhythms in Sprague-Dawley, Lewis, and Fischer male and female rats. Alcohol Clin Exp Res 2006, 30:438-447.
47. Grakalic I., Schindler C.W., Baumann M.H., Rice K.C., Riley A.L. Effects of stress modulation on morphine-induced conditioned place preferences and plasma corticosterone levels in Fischer, Lewis, and Sprague-Dawley rat strains. Psychopharmacol Berl 2006, 189:277-286.
48. Guitart X., Beitner-Johnson D., Marby D.W., Kosten T.A., Nestler E.J. Fischer and Lewis rat strains differ in basal levels of neurofilament proteins and their regulation by chronic morphine in the mesolimbic dopamine system. Synapse 1992, 12:242-253.
49. Kosten T.A., Miserendino M.J., Chi S., Nestler E.J. Fischer and Lewis rat strains show differential cocaine effects in conditioned place preference and behavioral sensitization but not in locomotor activity or conditioned taste aversion. J Pharmacol Exp Ther 1994, 269:137-144.
50. Beitner-Johnson D., Guitart X., Nestler E.J. Dopaminergic brain reward regions of Lewis and Fischer rats display different levels of tyrosine hydroxylase and other morphine- and cocaine-regulated phosphoproteins. Brain Res 1991, 561:147-150.
51. Nestler E.J., Guitart X., Ortiz J., Trevisan L. Second messenger and protein phosphorylation mechanisms underlying possible genetic vulnerability to alcoholism. Ann NY Acad Sci 1994, 708:108-118.
52. Davis C.M., Riley A.L. Conditioned taste aversion learning: implications for animal models of drug abuse. Ann NY Acad Sci 2010, 1187:247-275.
53. Kohut S.J., Riley A.L. Conditioned taste aversions. Encyclopedia of Psychopharmacology 2010, 336-340. Springer Verlag. I.P. Stolerman (Ed.).
54. Riley A.L., Jacobs W.J., LoLordo V.M. Drug exposure and the acquisition and retention of a conditioned taste aversion. J Comp Physiol Psychol 1976, 90:799-807.
55. Lancellotti D., Bayer B.M., Glowa J.R., Houghtling R.A., Riley A.L. Morphine-induced conditioned taste aversions in the LEW/N and F344/N rat strains. Pharmacol Biochem Behav 2001, 68:603-610.
56. Rzóska J. Bait shyness, a study in rat behavior. Br J Anim Behav 1953, 1:128-135.
57. Reilly S. Central gustatory system lesions and conditioned taste aversion. Conditioned taste aversion: behavioral and neural processes 2009, 309-327. Oxford University Press, New York. S. Reilly, T.R. Schachtman (Eds.).
58. Glowa J.R., Shaw A.E., Riley A.L. Cocaine-induced conditioned taste aversions: comparisons between effects in LEW/N and F344/N rat strains. Psychopharmacol Berl 1994, 114:229-232.
59. Grigson P.S., Freet C.S. The suppressive effects of sucrose and cocaine, but not lithium chloride, are greater in Lewis than in Fischer rats: evidence for the reward comparison hypothesis. Behav Neurosci 2000, 114:353-363.
60. Roma P.G., Riley A.L. Cross-fostering and the extinction of cocaine's conditioned aversive effects: evidence for gene-environment interaction. Pharmacol Biochem Behav 2007, 88:1-8.
61. Berger B.D. Conditioning of food aversions by injections of psychoactive drugs. J Comp Physiol Psychol 1972, 81:21-26.
62. Parker L.A. Taste avoidance and taste aversion: evidence for two different processes. Learn Behav 2003, 31:165-172.
63. Parker L.A., Limebeer C.L., Rana S.A. Conditioned disgust, but not conditioned taste avoidance, may reflect conditioned nausea in rats. Conditioned taste aversion: behavioral and neural processes 2009, 92-113. Oxford University Press, New York. S. Reilly, T.R. Schachtman (Eds.).
64. Parker L.A. Rewarding drugs produce taste avoidance, but not taste aversion. Neurosci Biobehav Rev 1995, 19:143-157.
65. Grigson P.S. Conditioned taste aversions and drugs of abuse: a reinterpretation. Behav Neurosci 1997, 111:129-136.
66. Grigson P.S., Twining R.C., Freet C.S., Wheeler R.A., Geddes R.I. Drug-induced suppression of conditioned stimulus intake: reward, aversion, and addiction. Conditioned taste aversion: behavioral and neural processes 2009, 74-91. Oxford University Press, New York. S. Reilly, T.R. Schachtman (Eds.).
67. Davis C.M., Rice K.C., Riley A.L. Opiate-agonist induced taste aversion learning in the Fischer 344 and Lewis inbred rat strains: evidence for differential mu opioid receptor activation. Pharmacol Biochem Behav 2009, 93:397-405.
68. Grabus S.D., Glowa J.R., Riley A.L. Morphine- and cocaine-induced c-Fos levels in Lewis and Fischer rat strains. Brain Res 2004, 998:20-28.
69. Barki-Harrington L., Belelovsky K., Doron G., Rosenblum K. Molecular mechanisms of taste learning in the insular cortex and amygdala. Conditioned taste aversion: behavioral and neural processes 2009, 341-363. Oxford University Press, New York. S. Reilly, T.R. Schachtman (Eds.).
70. Bernstein I.L., Koh M.T. Molecular signaling during taste aversion learning. Chem Senses 2007, 32:99-103.
71. Bernstein I.L., Wilkins E.E., Barot S.K. Mapping conditioned taste aversion associations through patterns of c-fos expression. Conditioned taste aversion: behavioral and neural processes 2009, 328-340. Oxford University Press, New York. S. Reilly, T.R. Schachtman (Eds.).
72. Swank M.W., Bernstein I.L. c-Fos induction in response to a conditioned stimulus after single trial taste aversion learning. Brain Res 1994, 636:202-208.
73. Yamamoto T. Neural mechanisms of taste aversion learning. Neurosci Res 1993, 16:181-185.
74. Yamamoto T., Yuyama N. On a neural mechanism for cortical processing of taste quality in the rat. Brain Res 1987, 400:312-320.
75. Bermúdez-Rattoni F., Yamamoto T. Neuroanatomy of conditioned taste aversion. Lesion studies. Conditioned taste aversion: memory of a special kind 1998, 26-45. Oxford University Press, Oxford, UK. J. Bureš, F. Bermúdez-Rattoni, T. Yamamoto (Eds.).
76. Sakai N., Yamamoto T. Conditioned taste aversion and c-fos expression in the rat brainstem after administration of various USs. NeuroReport 1997, 8:2215-2220.
77. Bardo M.T., Bevins R.A. Conditioned place preference: what does it add to our preclinical understanding of drug reward?. Psychopharmacol Berl 2000, 153:31-43.
78. Tzschentke T.M. Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog Neurobiol 1998, 56:613-672.
79. Bornstein S.R., Webster E.L., Torpy D.J., et al. Chronic effects of a nonpeptide corticotropin-releasing hormone type I receptor antagonist on pituitary-adrenal function, body weight, and metabolic regulation. Endocrinology 1998, 139:1546-1555.
80. Lu L., Liu D., Ceng X. Corticotropin-releasing factor receptor type 1 mediates stress-induced relapse to cocaine-conditioned place preference in rats. Eur J Pharmacol 2001, 415:203-208.
81. Stephens D.N., Schneider H.H., Kehr W., et al. Modulation of anxiety by beta-carbolines and other benzodiazepine receptor ligands: relationship of pharmacological to biochemical measures of efficacy. Brain Res Bull 1987, 19:309-318.
82. Will M.J., Watkins L.R., Maier S.F. Uncontrollable stress potentiates morphine's rewarding properties. Pharmacol Biochem Behav 1998, 60:655-664.
83. Gomez-Serrano M.A., Kearns D.N., Riley A.L. The effects of light cycle phase on morphine-induced conditioned taste aversions in the Lewis, Fischer and Sprague-Dawley rat strains. Behav Brain Res 2009, 196:116-122.
84. Dhabhar F.S., McEwen B.S., Spencer R.L. Stress response, adrenal steroid receptor levels and corticosteroid-binding globulin levels - a comparison between Sprague-Dawley, Fischer 344 and Lewis rats. Brain Res 1993, 616:89-98.
85. Windle R.J., Wood S.A., Shanks N., Lightman S.L., Ingram C.D. Ultradian rhythm of basal corticosterone release in the female rat: dynamic interaction with the response to acute stress. Endocrinology 1998, 139:443-450.
86. Gomez-Serrano, M., Riley, A. L. The effects of cross-fostering on morphine-induced conditioned taste aversion in Fischer and Lewis rats. Unpublished manuscript.
87. Gomez-Serrano M.A., Sternberg E.M., Riley A.L. Maternal behavior in F344/N and LEW/N rats. Effects on carrageenan-induced inflammatory reactivity and body weight. Physiol Behav 2002, 75:493-505.
88. Gomez-Serrano M., Tonelli L., Listwak S., Sternberg E., Riley A.L. Effects of cross fostering on open-field behavior, acoustic startle, lipopolysaccharide-induced corticosterone release, and body weight in Lewis and Fischer rats. Behav Genet 2001, 31:427-436.
89. Roma P.G., Chen S.A., Barr C.S., Riley A.L. Dissociation between the aversive and pharmacokinetic effects of ethanol in female Fischer and Lewis rats. Behav Brain Res 2007, 182:51-56.
90. Champagne F.A., Francis D.D., Mar A., Meaney M.J. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 2003, 79:359-371.
91. Meaney M.J., Aitken D.H., van Berkel C., Bhatnagar S., Sapolsky R.M. Effect of neonatal handling on age-related impairments associated with the hippocampus. Science 1988, 239:766-768.
92. Szyf M., Meaney M.J. Epigenetics, behaviour, and health. Allergy Asthma Clin Immunol 2008, 4:37-49.
93. Rinker, J. A., Hutchison, M. A., Chen, S. A., Thorsell, A., Heilig, M., Riley, A. L. Exposure to nicotine during periadolescence alters aversive and physiological effects induced by ethanol in adulthood. in preparation.
94. Hutchison, M. A., Albaugh, D. L., Riley, A. L. Exposure to alcohol during adolescence alters the aversive and locomotor-activating effects of cocaine in adult rats. Pharmacol Biochem Behav. 2010;97:370-6.
95. Schramm-Sapyta N.L., Cha Y.M., Chaudhry S., et al. Differential anxiogenic, aversive, and locomotor effects of THC in adolescent and adult rats. Psychopharmacol Berl 2007, 191:867-877.
96. Schramm-Sapyta N.L., Morris R.W., Kuhn C.M. Adolescent rats are protected from the conditioned aversive properties of cocaine and lithium chloride. Pharmacol Biochem Behav 2006, 84:344-352.
97. Schramm-Sapyta N.L., Walker Q.D., Caster J.M., Levin E.D., Kuhn C.M. Are adolescents more vulnerable to drug addiction than adults? Evidence from animal models. Psychopharmacol Berl 2009, 206:1-21.
98. Shram M.J., Funk D., Li Z., Le A.D. Periadolescent and adult rats respond differently in tests measuring the rewarding and aversive effects of nicotine. Psychopharmacol Berl 2006, 186:201-208.
99. Verendeev, A., Riley, A. L. Assessment of individual differences in the rewarding and aversive effects of morphine. Unpublished manuscript.
100. Turenne S.D., Miles C., Parker L.A., Siegel S. Individual differences in reactivity to the rewarding/aversive properties of drugs: assessment by taste and place conditioning. Pharmacol Biochem Behav 1996, 53:511-516.
101. Hertel A., Eikelboom R. Can overeating induce conditioned taste avoidance in previously food restricted rats?. Physiol Behav 2010, 99:482-486.
102. Bernstein I.L., Borson S. Learned food aversion: a component of anorexia syndromes. Psychol Rev 1986, 93:462-472.
103. Roma P.G., Flint W.W., Higley J.D., Riley A.L. Assessment of the aversive and rewarding effects of alcohol in Fischer and Lewis rats. Psychopharmacol Berl 2006, 189:187-199.
104. Pescatore K.A., Glowa J.R., Riley A.L. Strain differences in the acquisition of nicotine-induced conditioned taste aversion. Pharmacol Biochem Behav 2005, 82:751-757.
105. Foynes M.M., Riley A.L. Lithium-chloride-induced conditioned taste aversions in the Lewis and Fischer 344 rat strains. Pharmacol Biochem Behav 2004, 79:303-308.
106. Davis, C. M., Cobuzzi, J. L., Riley, A. L. Modulation of the aversive effects of peripheral mu opioid receptor activation by morphine in the inbred fischer 344 and lewis rats. The College on Problems of Drug Dependence. 2010;72-7.
107. Stephens M.K., Riley A.L. Naloxone-precipitated conditioned taste aversions in morphine-dependent Fischer (F344) and Lewis rat strains. Pharmacol Biochem Behav 2009, 92:60-67.
108. Bureš J., Bermúdez-Rattoni F., Yamamoto T. Conditioned taste aversions: memory of a special kind 1998, Oxford University Press, Oxford, UK.