Exercise to reduce the escalation of cocaine self-administration in adolescent and adult rats

Psychopharmacology

Volumn 224, Issue 3, 2012, Pages 387-400

  Zlebnik, Natalie E ^a   Anker, Justin J ^a   Carroll, Marilyn E ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Adolescence; Cocaine; Escalation; Exercise; Individual differences; Self administration; Wheel running

Indexed keywords

COCAINE;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COCAINE DEPENDENCE; CONTROLLED STUDY; DRUG ABUSE; DRUG SEEKING BEHAVIOR; DRUG SELF ADMINISTRATION; FEMALE; KINESIOTHERAPY; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; RAT; THERAPY EFFECT; TREADMILL EXERCISE;

AGE FACTORS; ANIMALS; BEHAVIOR, ADDICTIVE; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM STIMULANTS; COCAINE; COCAINE-RELATED DISORDERS; CONDITIONING, OPERANT; DRUG-SEEKING BEHAVIOR; FEMALE; INFUSIONS, INTRAVENOUS; PHYSICAL EXERTION; RATS; RATS, WISTAR; REINFORCEMENT (PSYCHOLOGY); RUNNING; SELF ADMINISTRATION; TIME FACTORS;

EID: 84871647575     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-012-2760-7     Document Type: Article

References (113)

1. Adriani W, Chiarotti F, Laviola G (1998) Elevated novelty seeking and peculiar D-amphetamine sensitization in periadolescent mice compared with adult mice. Behav Neurosci 112:1152-1166
2. Ahmed SH, Koob GF (1998) Transition from moderate to excessive drug intake: change in hedonic set point. Science 282(5387):298-300
3. Ahmed SH, Koob GF (1999) Long-lasting increase in the set point for cocaine self-administration after escalation in rats. Psychopharmacology 146(3):303-312
4. Ahmed SH, Koob GF (2005) Transition to drug addiction: a negative reinforcement model based on an allostatic decrease in reward function. Psychopharmacology 180(3):473-490
5. Anker JJ, Carroll ME (2010) Reinstatement of cocaine seeking induced by drugs, cues, and stress in adolescent and adult rats. Psychopharmacology 208(2):211-222
6. Anker JJ, Carroll ME (2011) Adolescent nicotine exposure sensitizes cue-induced reinstatement of cocaine seeking in rats bred for high and low saccharin intake. Drug Alcohol Depend 118(1):68-72
7. Anker JJ, Perry JL, Gliddon LA, Carroll ME (2009) Impulsivity predicts the escalation of cocaine self-administration in rats. Pharmacol Biochem Behav 93(3):343-348
8. Anker JJ, Zlebnik NE, Carroll ME (2010) Differential effects of allopregnanolone on the escalation of cocaine self-administration and sucrose intake in female rats. Psychopharmacology 212(3):419-429
9. Anker JJ, Zlebnik NE, Navin SF, Carroll ME (2011) Responding during signaled availability and nonavailability of iv cocaine and food in rats: age and sex differences. Psychopharmacology 215(4):785-799
10. Anker JJ, Baron TR, Zlebnik NE, Carroll ME (2012a) Escalation of methamphetamine self-administration in adolescent and adult rats. Drug Alcohol Depend. doi:10.1016/j.drugalcdep.2012.01.004
11. Anker JJ, Holtz NA, Carroll ME (2012b) Effects of progesterone on escalation of intravenous cocaine self-administration in rats selectively bred for high and low saccharin intakes. Behav Pharmacol. doi:10.1097/FBP. 0b013e32834f9e37
12. Badanich KA, Adler KJ, Kirstein CL (2006) Adolescents differ from adults in cocaine conditioned place preference and cocaineinduced dopamine in the nucleus accumbens septi. Eur J Pharmacol 550:95-106
13. Badanich KA, Maldonado AM, Kirstein CL (2008) Early adolescents show enhanced acute cocaine-induced locomotor activity in comparison to late adolescent and adult rats. Dev Psychobiol 50:127-133
14. Bardo MT, Klebaur JE, Valone JM, Deaton C (2001) Environmental enrichment decreases intravenous self-administration of amphetamine in female and male rats. Psychopharmacology 155(3):278-284
15. Belluzzi JD, Wang R, Leslie FM (2005) Acetaldehyde enhances acquisition of nicotine self-administration in adolescent rats. Neuropsychopharmacology 30(4):705-712
16. Boakes RA, Mills KJ, Single JP (1999) Sex differences in the relationship between activity and weight loss in the rats. Behav Neurosci 113(5):1080-1089
17. Brenhouse HC, Andersen SL (2008) Delayed extinction and stronger reinstatement of cocaine conditioned place preference in adolescent rats, compared to adults. Behav Neurosci 122:460-465
18. Brenhouse HC, Sonntag KC, Andersen SL (2008) Transient D1 dopamine receptor expression on prefrontal cortex projection neurons: relationship to enhanced motivational salience of drug cues in adolescence. J Neurosci 28:2375-2382
19. Buchowski MS, Meade NN, Charboneau E, Park S, Dietrich MS, Cowan RL, Martin PR (2011) Aerobic exercise training reduces cannabis craving and use in non-treatment seeking cannabisdependent adults. PLoS One 6(3):e17465
20. Camarini R, Griffin WC, Yanke AB, dos Santos BR, Olive MF (2008) Effects of adolescent exposure to cocaine on locomotor activity and extracellular dopamine and glutamate levels in nucleus accumbens of DBA/2J mice. Brain Res 1193:34-42
21. Campbell UC, Carroll ME (2000) Reduction of drug selfadministration by an alternative non-drug reinforcer in rhesus monkeys: magnitude and temporal effects. Psychopharmacology 147(4):418-425
22. Campbell UC, Morgan AD, Carroll ME (2002) Sex differences in the effects of baclofen on the acquisition of intravenous cocaine selfadministration in rats. Drug Alcohol Depend 66(1):61-69
23. Carroll KM (1996) Relapse prevention as a psychosocial treatment: a review of controlled clinical trials. Exp Clin Psychopharmacol 4 (1):46-54
24. Carroll ME, Boe IN (1982) Increased intravenous drug self-administration during deprivation of other reinforcers. Pharmacol Biochem Behav 17(3):563-567
25. Carroll ME, Bickel WK, Higgins ST (2001a) Nondrug incentives to treat drug abuse: laboratory and clinical developments. In: Carroll ME, Overmier JB (eds) Animal research and human psychological health: advancing human welfare through behavioral science. American Psychological Association, Washington, pp 139-154
26. Carroll ME, Campbell UC, Heideman P (2001b) Ketoconazole suppresses food restriction-induced increases in heroin selfadministration in rats: sex differences. ExpClin Psychopharm 9:307-316
27. Carroll ME, Batulis DK, Landry KL, Morgan AD (2005) Sex differences in the escalation of oral phencyclidine (PCP) self-administration under FR and PR schedules in rhesus monkeys. Psychopharmacology 180 (3):414-426
28. Carroll ME, Morgan AD, Anker JJ, Perry JL, Dess NK (2008) Selective breeding for differential saccharin intake as an animal model of drug abuse. Behav Pharmacol 19(5-6):435-460
29. Carroll, ME, Anker JJ, Perry JL (2009) Modeling risk factors for nicotine and other drug abuse in the preclinical laboratory, Drug and Alcohol Dependence, Supplemental Issue:Women and smoking: understanding socioeconomic influences, 104S:S70-S78
30. Carroll ME, Anker JJ, Mach JL, Newman JL, Perry JL (2010) Delay discounting as a predictor of drug abuse. In: Madden GJ, Bickel WK (eds) Impulsivity: the behavioral and neurological science of discounting. American Psychological Association, Washington, pp 243-272
31. Carroll ME, Gao Y, Brimijoin S, Anker JJ (2011) Effects of cocaine hydrolase on cocaine self-administration under a PR schedule and during extended access (escalation) in rats. Psychopharmacology 213(4):817-829
32. Carroll ME, Holtz NA, Zlebnik NE (2012) Saccharin preference in rats: relation to impulsivity and comorbid drug intake. In: Avena NM (ed) Animal models of eating disorders. Springer-Verlag, New York, p 380
33. Caster JM, Walker QD, Kuhn CM (2007) A single high dose of cocaine induces differential sensitization to specific behaviors across adolescence. Psychopharmacology 193:247-260
34. Catlow BJ, Kirstein CL (2005) Heightened cocaine-induced locomotor activity in adolescent compared to adult female rats. J Psychopharmacol 19(5):443-447
35. Charilaou M, Karekla M, Constantinou M, Price S (2009) Relationship between physical activity and type of smoking behavior among adolescents and young adults in Cyprus. Nicotine Tob Res 11 (8):969-976
36. Chen H, Matta SG, Sharp BM (2007) Acquisition of nicotine selfadministration in adolescent rats given prolonged access to the drug. Neuropsychopharmacology 32:700-709
37. Collingwood TR, Sunderlin J, Reynolds R, Kohl HW III (2000) Physical training as a substance abuse prevention intervention for youth. J Drug Educ 30(4):435-451
38. Comer SD, Lac ST, Wyvell CL, Curtis LK, Carroll ME (1995a) Food deprivation affects extinction and reinstatement of responding in rats. Psychopharmacology 121(2):150-157
39. Comer SD, Turner DM, Carroll ME (1995b) Effects of food deprivation on cocaine base smoking in rhesus monkeys. Psychopharmacology 119(2):127-132
40. Cosgrove KP, Carroll ME (2004) Differential effects of bremazocine on oral phencyclidine (PCP) self-administration in male and female rhesus monkeys. Exp Clin Psychopharmacol 12(2):111-117
41. Cosgrove KP, Hunter R, Carroll ME (2002) Wheel-running attenuates intravenous cocaine self-administration in rats: sex differences. Pharm Biochem Behav 73:663-667
42. Cummins E, Leri F (2008) Unreinforced responding during limited access to heroin self-administration. Pharmacol Biochem Behav 90(3):420-427
43. Dalley JW, Everitt BJ, Robbins TW (2011) Impulsivity, compulsivity, and top-down cognitive control. Neuron 69(4):680-694
44. Daniel J, Cropley M, Ussher M, West R (2004) Acute effects of a short bout of moderate versus light intensity exercise versus inactivity on tobacco withdrawal symptoms in sedentary smokers. Psychopharmacology 174(3):320-326
45. de Wit H (2009) Impulsivity as a determinant and consequence of drug use: a review of underlying processes. Addict Biol 14(1):22-31
46. Desor JA, Beauchamp GK (1987) Longitudinal changes in sweet preferences in humans. Physiol Behav 39(5):639-641
47. Doremus-Fitzwater TL, Varlinskaya EI, Spear LP (2010) Motivational systems in adolescence: possible implications for age differences in substance abuse and other risk-taking behaviors. Brain Cogn 72 (1):114-123
48. Eikelboom R, Mills R (1988) A microanalysis of wheel running in male and female rats. Physiol Behav 43(5):625-630
49. Flagel SB, Watson SJ, Akil H, Robinson TE (2008) Individual differences in the attribution of incentive salience to a reward-related cue: influence on cocaine sensitization. Behav Brain Res 186(1):48-56
50. Frantz KJ, O'Dell LE, Parsons LH (2007) Behavioral and neurochemical responses to cocaine in periadolescent and adult rats. Neuropsychopharmacology 32(3):625-637
51. Friemel CM, Spanagel R, Schneider M (2010) Reward sensitivity for a palatable food reward peaks during pubertal developmental in rats. Front Behav Neurosci 4:39
52. Fullgrabe MW, Vengeliene V, Spanagel R (2007) Influence of age at drinking onset on the alcohol deprivation effect and stress-induced drinking in female rats. Pharmacol Biochem Behav 86:320-326
53. Green L, Freed DE (1993) The substitutability of reinforcers. J Exp Anal Behav 60(1):141-158
54. Griffiths RR, Bigelow GE, Henningfield JE (1980) Similarities in animal and human drug-taking behavior. In: Mello NK (ed) Advances in substance abuse: behavioral and biological research, vol. 1. JAI, Greenwich, pp 1-90
55. Holtz NA, Carroll ME (2011) Baclofen has opposite effects on escalation of cocaine self-administration: increased intake in rats selectively bred for high (HiS) saccharin intake and decreased intake in those selected for low (LoS) saccharin intake. Pharmacol Biochem Behav 100(2):275-283
56. Jones LC, Bellingham WP, Ward LC (1990) Sex differences in voluntary locomotor activity of food-restricted and ad libitum-fed rats. Implications for the maintenance of a body weight set-point. Comp Biochem Physiol A Comp Physiol 96(2):287-290
57. Kantak KM, Goodrich CM, Uribe V (2007) Influence of sex, estrous cycle, and drug-onset age on cocaine self-administration in rats (Rattus norvegicus). Exp Clin Psychopharmacol 15(1):37-47
58. Kerstetter KA, Kantak KM (2007) Differential effects of selfadministered cocaine in adolescent and adult rats on stimulusreward learning. Psychopharmacology 194(3):403-411
59. Klebaur JE, Phillips SB, Kelly TH, Bardo MT (2001) Exposure to novel environmental stimuli decreases amphetamine selfadministration in rats. Exp Clin Psychopharmacol 9(4):372-379
60. Koelch M, Schnoor K, Fegert JM (2008) Ethical issues in psychopharmacology of children and adolescents. Curr Opin Psychiatry 21 (6):598-605
61. Koob GF, Le Moal M (2001) Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24(2):97-129
62. Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35(1):217-238
63. Korhonen T, Kujala UM, Rose RJ, Kaprio J (2009) Physical activity in adolescence as a predictor of alcohol and illicit drug use in early adulthood: a longitudinal population based twin study. Twin Res Hum Genet 12(3):261-268
64. Lambert KG, Kinsley CH (1993) Sex differences and gonadal hormones influence susceptibility to the activity-stress paradigm. Physiol Behav 53(6):1085-1090
65. Larson EB, Carroll ME (2005) Wheel running as a predictor of cocaine self-administration and reinstatement in female rats. Pharmacol Biochem Behav 82(3):590-600
66. Larson EB, Anker JJ, Gliddon LA, Fons KS, Carroll ME (2007) Effects of estrogen and progesterone on the escalation of cocaine self-administration in female rats during extended access. Exp Clin Psychopharmacol 15(5):461-471
67. Laviola G, Wood RD, Kuhn C, Francis R, Spear LP (1995) Cocaine sensitization in periadolescent and adult rats. J Pharmacol Exp Ther 275:345-357
68. Leslie FM, Loughlin SE, Wang R, Perez L, Lotfipour S, Belluzzi JD (2004) Adolescent development of forebrain stimulant responsiveness: insights from animal studies. Ann N YAcad Sci 1021:148-159
69. Levin ED, Rezvani AH, Montoya D, Rose JE, Swartzwelder HS (2003) Adolescent-onset nicotine self-administration modeled in female rats. Psychopharmacology (Berl) 169:141-149
70. Levin ED, Lawrence SS, Petro A, Horton K, Rezvani AH, Seidler FJ, Slotkin TA (2007) Adolescent vs. adult-onset nicotine selfadministration in male rats: duration of effect and differential nicotinic receptor correlates. Neurotoxicol Teratol 29:458-465
71. Lynch WJ, Piehl KB, Acosta G, Peterson AB, Hemby SE (2010) Aerobic exercise attenuates reinstatement of cocaine-seeking behavior and associated neuroadaptations in the prefrontal cortex. Biol Psychiatry 68(8):774-777
72. McVoy M, Findling R (2009) Child and adolescent psychopharmacology update. Psychiatr Clin North Am 32(1):111-133
73. Miller ML, Vaillancourt BD, Wright MJ Jr, Aarde SM, Vandewater SA, Creehan KM, Taffe MA (2012) Reciprocal inhibitory effects of intravenous d-methamphetamine self-administration and wheel activity in rats. Drug Alcohol Depend 121(1-2):90-96
74. National Research Council (2003) Guidelines for the care and use of mammals in neuroscience and behavioral research. Washington, DC: The National Academies Press, p 209
75. Ojeda SR, Andrews WW, Advis JP, White SS (1980) Recent advances in the endocrinology of puberty. Endocr Rev 1(3):228-257
76. Parylak SL, Caster JM,Walker QD, Kuhn CM (2008) Gonadal steroids mediate the opposite changes in cocaine-induced locomotion across adolescence in male and female rats. Pharmacol Biochem Behav 89(3):314-323
77. Perry JL, Carroll ME (2008) The role of impulsive behavior in drug abuse. Psychopharmacology 200(1):1-26
78. Perry JL, Morgan AD, Anker JJ, Dess NK, Carroll ME (2006) Escalation of i.v. cocaine self-administration and reinstatement of cocaine-seeking behavior in rats bred for high and low saccharin intake. Psychopharmacology 186(2):235-245
79. Perry JL, Anderson MM, Nelson SE, Carroll ME (2007) Acquisition of i.v. cocaine self-administration in adolescent and adult male rats selectively bred for high and low saccharin intake. Physiol Behav 91(1):126-133
80. Roth ME, Carroll ME (2004) Sex differences in the escalation of intravenous cocaine intake following long- or short-access to cocaine self-administration. Pharmacol Biochem Behav 78 (2):199-207
81. Schenk S, Lacelle G, Gorman K, Amit Z (1987) Cocaine selfadministration in rats influenced by environmental conditions: implications for the etiology of drug abuse. Neurosci Lett 81(1-2): 227-231
82. Schramm-Sapyta NL, Walker QD, Caster JM, Levin ED, Kuhn CM (2009) Are adolescents more vulnerable to drug addiction than adults? Evidence from animal models. Psychopharmacology 206 (1):1-21
83. Schramm-Sapyta NL, Cauley MC, Stangl DK, Glowacz S, Stepp KA, Levin ED, Kuhn CM (2011) Role of individual and developmental differences in voluntary cocaine intake in rats. Psychopharmacology 215(3):493-504
84. Shahbazi M, Moffett AM, Williams BF, Frantz KJ (2008) Age- and sex-dependent amphetamine self-administration in rats. Psychopharmacology 196:71-81
85. Smith MA, Pitts EG (2011) Access to a running wheel inhibits the acquisition of cocaine self-administration. Pharmacol Biochem Behav 100(2):237-243
86. Smith MA, Schmidt KT, Iordanou JC, Mustroph ML (2008) Aerobic exercise decreases the positive-reinforcing effects of cocaine. Drug Alcohol Depend 98:129-135
87. Smith MA, Walker KL, Cole KT, Lang KC (2011) The effects of aerobic exercise on cocaine self-administration in male and female rats. Psychopharmacology 218(2):357-369
88. Smith MA, Pennock MM, Walker KL, Lang KC (2012) Access to a running wheel decreases cocaine-primed and cue-induced reinstatement in male and female rats. Drug Alcohol Depend 121(1-2):54-61
89. Snyder KJ, Katovic NM, Spear LP (1998) Longevity of the expression of behavioral sensitization to cocaine in preweanling rats. Pharmacol Biochem Behav 60(4):909-914
90. Spear LP (2000a) Neurobehavioral changes in adolescence. Curr Dir Psychol Sci 9:111-114
91. Spear LP (2000b) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24(4):417-463
92. Spear LP (2009) Heightened stress responsivity and emotional reactivity during pubertal maturation: implications for psychopathology. Dev Psychopathol 21:87-97
93. Spear LP (2011) Rewards, aversions and affect in adolescence: emerging convergences across laboratory animal and human data. Dev Cogn Neurosci 1(4):390-403
94. Spear LP, Brake SC (1983) Periadolescence: age-dependent behavior and psychopharmacological responsivity in rats. Dev Psychobiol 16:83-109
95. Terry-McElrath YM, O'Malley PM (2011) Substance use and exercise participation among young adults: parallel trajectories in a national cohort-sequential study. Addiction 106(10):1855-1865
96. Terry-McElrath YM, O'Malley PM, Johnston LD (2011) Exercise and substance use among American youth, 1991-2009. Am J Prev Med 40(5):530-540
97. Thanos PK, Tucci A, Stamos J, Robison L, Wang GJ, Anderson BJ, Volkow ND (2010) Chronic forced exercise during adolescence decreases cocaine conditioned place preference in Lewis rats. Behav Brain Res 215(1):77-82
98. Ussher M, Nunziata P, Cropley M,West R (2001) Effect of a short bout of exercise on tobacco withdrawal symptoms and desire to smoke. Psychopharmacology 158(1):66-72
99. Ussher M, Sampuran AK, Doshi R, West R, Drummond DC (2004) Acute effect of a brief bout of exercise on alcohol urges. Addiction 99(12):1542-1547
100. Ussher M, West R, Doshi R, Sampuran AK (2006) Acute effect of isometric exercise on desire to smoke and tobacco withdrawal symptoms. Hum Psychopharmacol 21(1):39-46
101. Ussher M, Cropley M, Playle S, Mohidin R, West R (2009) Effect of isometric exercise and body scanning on cigarette cravings and withdrawal symptoms. Addiction 104(7):1251-1257
102. Vaidya JG, Grippo AJ, Johnson AK, Watson D (2004) A comparative developmental study of impulsivity in rats and humans: the role of reward sensitivity. Ann N Y Acad Sci 1021:395-398
103. Van Etten ML, Higgins ST, Budney AJ, Badger GJ (1998) Comparison of the frequency and enjoyability of pleasant events in cocaine abusers vs. non-abusers using a standardized behavioral inventory. Addiction 93:1669-1680
104. Vetter CS, Doremus-Fitzwater TL, Spear LP (2007) Time course of elevated ethanol intake in adolescent relative to adult rats under continuous, voluntary-access conditions. Alcohol Clin Exp Res 31:1159-1168
105. Vuchinich RE, Tucker JA (1983) Behavioral theories of choice as a framework for studying drinking behavior. J Abnorm Psychol 92 (4):408-416
106. Vuchinich RE, Tucker JA (1996) The molar context of alcohol abuse. In: Green L, Kagel J (eds) Advances in behavioral economics, vol. 3. Ablex, Norwood, pp 133-162
107. Wichstrøm T, Wichstrøm L (2009) Does sports participation during adolescence prevent later alcohol, tobacco and cannabis use? Addiction 104(1):138-149
108. Williams DM, Dunsiger S, Whiteley JA, Ussher MH, Ciccolo JT, Jennings EG (2011) Acute effects of moderate intensity aerobic exercise on affective withdrawal symptoms and cravings among women smokers. Addict Behav 36(8):894-897
109. Wilmouth CE, Spear LP (2009) Hedonic sensitivity in adolescent and adult rats: taste reactivity and voluntary sucrose consumption. Pharmacol Biochem Behav 92(4):566-573
110. Zakharova E, Leoni G, Kichko I, Sari I (2009) Differential effects of METH and cocaine on conditioned place preference and locomotor activity in adult and adolescentmale rats. Behav Brain Res 198:45-50
111. Zlebnik NE, Anker JJ, Gliddon LA, Carroll ME (2010) Reduction of extinction and reinstatement of cocaine seeking by wheel running in female rats. Psychopharmacology 209(1):113-125
112. Zombeck JA, Gupta T, Rhodes JS (2009) Evaluation of a pharmacokinetic hypothesis for reduced locomotor stimulation from methamphetamine and cocaine in adolescent versus adult male C57BL/6J mice. Psychopharmacology 201(4):589-599
113. Zombeck JA, Lewicki AD, Patel K, Gupta T, Rhodes JS (2010) Patterns of neural activity associated with differential acute locomotor stimulation to cocaine and methamphetamine in adolescent versus adult male C57BL/6J mice. Neuroscience 165:1087-1099