Intermittent access to preferred food reduces the reinforcing efficacy of chow in rats

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 295, Issue 4, 2008, Pages

  Cottone, Pietro ^a,b   Sabino, Valentina ^a   Steardo, Luca ^b   Zorrilla, Eric P ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Deprivation; Food intake; Limited access; Negative contrast; Palatability

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEEDING BEHAVIOR; FOOD INTAKE; FOOD PREFERENCE; HYPOPHAGIA; MALE; MOTOR DYSFUNCTION; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RAT; REINFORCEMENT; SATIETY; WEIGHT GAIN;

ANIMALS; BODY WEIGHT; DIET; EATING; ENERGY INTAKE; FEEDING BEHAVIOR; FOOD DEPRIVATION; FOOD PREFERENCES; HYPERPHAGIA; MALE; RATS; RATS, WISTAR; REINFORCEMENT (PSYCHOLOGY);

EID: 57349128832     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.90309.2008     Document Type: Article

References (102)

1. Ahmed SH, Kenny PJ, Koob GF, Markou A. Neurobiological evidence for hedonic allostasis associated with escalating cocaine use. Nat Neurosci 5: 625-626, 2002.
2. Ahmed SH, Koob GF. Transition from moderate to excessive drug intake: change in hedonic set point. Science 282: 298-300, 1998.
3. Ahmed SH, Walker JR, Koob GF. Persistent increase in the motivation to take heroin in rats with a history of drug escalation. Neuropsychopharmacology 22: 413-421, 2000.
4. Archer ZA, Rayner DV, Barrett P, Balik A, Duncan JS, Moar KM, Mercer JG. Hypothalamic energy balance gene responses in the Sprague-Dawley rat to supplementation of high-energy diet with liquid ensure and subsequent transfer to chow. J Neuroendocrinol 17: 711-719, 2005.
5. Aujla H, Martin-Fardon R, Weiss F. Rats with extended access to cocaine exhibit increased stress reactivity and sensitivity to the anxiolytic-like effects of the mGluR 2/3 agonist LY379268 during abstinence. Neuropsychopharmacology 33: 1818-1826, 2007.
6. Avena NM, Hoebel BG. A diet promoting sugar dependency causes behavioral cross-sensitization to a low dose of amphetamine. Neuroscience 122: 17-20, 2003.
7. Avena NM, Long KA, Hoebel BG. Sugar-dependent rats show enhanced responding for sugar after abstinence: evidence of a sugar deprivation effect. Physiol Behav 84: 359-362, 2005.
8. Avena NM, Rada P, Hoebel BG. Evidence for sugar addiction: Behavioral and neurochemical effects of intermittent, excessive sugar intake. Neurosci Biobehav Rev 32: 20-39, 2008.
9. Avena NM, Rada P, Moise N, Hoebel BG. Sucrose sham feeding on a binge schedule releases accumbens dopamine repeatedly and eliminates the acetylcholine satiety response. Neuroscience 139: 813-820, 2006.
10. Barr AM, Phillips AG. Withdrawal following repeated exposure to D-amphetamine decreases responding for a sucrose solution as measured by a progressive ratio schedule of reinforcement. Psychopharmacology 141: 99-106, 1999.
11. Bello NT, Hajnal A. Acute methylphenidate treatments reduce sucrose intake in restricted-fed bingeing rats. Brain Res Bull 70: 422-429, 2006.
12. Bello NT, Sweigart KL, Lakoski JM, Norgren R, Hajnal A. Restricted feeding with scheduled sucrose access results in an upregulation of the rat dopamine transporter. Am J Physiol Regul Integr Comp Physiol 284: R1260-R1268, 2003.
13. Booth DA. Conditioned satiety in the rat. J Comp Physiol Psychol 81: 457-471, 1972.
14. Cabeza de Vaca S, Krahne LL, Carr KD. A progressive ratio schedule of self-stimulation testing in rats reveals profound augmentation of D-amphetamine reward by food restriction but no effect of a " sensitizing" regimen of D-amphetamine. Psychopharmacology (Berl) 175: 106-113, 2004.
15. Cheeta S, Brooks S, Willner P. Effects of reinforcer sweetness and the D2/D3 antagonist raclopride on progressive ratio operant performance. Behav Pharmacol 6: 127-132, 1995.
16. Collier G, Johnson DF, Morgan C. The magnitude-of-reinforcement function in closed and open economies. J Exp Anal Behav 57: 81-89, 1992.
17. Cooper SJ. Palatability-dependent appetite and benzodiazepines: new directions from the pharmacology of GABA(A) receptor subtypes. Appetite 44: 133-150, 2005.
18. Corwin RL. Binge-type eating induced by limited access in rats does not require energy restriction on the previous day. Appetite 42: 139-142, 2004.
19. Corwin RL. Bingeing rats: a model of intermittent excessive behavior? Appetite 46: 11-15, 2006.
20. Corwin RL, Buda-Levin A. Behavioral models of binge-type eating. Physiol Behav 82: 123-130, 2004.
21. Corwin RL, Wojnicki FH, Fisher JO, Dimitriou SG, Rice HB, Young MA. Limited access to a dietary fat option affects ingestive behavior but not body composition in male rats. Physiol Behav 65: 545-553, 1998.
22. Cottone P, Sabino V, Nagy TR, Coscina DV, Zorrilla EP. Feeding microstructure in diet-induced obesity susceptible versus resistant rats: central effects of urocortin 2. J Physiol 583: 487-504, 2007.
23. Cottone P, Sabino V, Steardo L, Zorrilla EP. FG 7142 specifically reduces meal size and the rate and regularity of sustained feeding in female rats: evidence that benzodiazepine inverse agonists reduce food palatability. Neuropsychopharmacology 32: 1069-1081, 2007.
24. Cottone P, Sabino V, Steardo L, Zorrilla EP. Opioid-dependent anticipatory negative contrast and binge-like eating in rats with limited access to highly preferred food. Neuropsychopharmacology 33: 524-535, 2008.
25. Dalley JW, Laane K, Pena Y, Theobald DE, Everitt BJ, Robbins TW. Attentional and motivational deficits in rats withdrawn from intravenous self-administration of cocaine or heroin. Psychopharmacology (Berl) 182: 579-587, 2005.
26. de Castro JM. The relationship of cognitive restraint to the spontaneous food and fluid intake of free-living humans. Physiol Behav 57: 287-295, 1995.
27. de Villiers PA, Herrnstein RJ. Toward a law of response strength. Psychol Bull 83: 1131-1153, 1976.
28. Dimitriou SG, Rice HB, Corwin RL. Effects of limited access to a fat option on food intake and body composition in female rats. Int J Eat Disord 28: 436-445, 2000.
29. Files FJ, Lewis RS, Samson HH. Effects of continuous versus limited access to ethanol on ethanol self-administration. Alcohol 11: 523-531, 1994.
30. Flaherty CF. Effect of anxiolytics and antidepressants on extinction and negative contrast. Pharmacol Ther 46: 309-320, 1990.
31. Flaherty CF, Coppotelli C, Grigson PS, Mitchell C, Flaherty JE. Investigation of the devaluation interpretation of anticipatory negative contrast. J Exp Psychol 21: 229-247, 1995.
32. Foltin RW. "Tasting and wasting" behavior in non-human primates: aberrant behavior or normal behavior in "times of plenty". Physiol Behav 89: 587-597, 2006.
33. Foltin RW, Haney M. Effects of the cannabinoid antagonist SR141716 (rimonabant) and D-amphetamine on palatable food and food pellet intake in non-human primates. Pharmacol Biochem Behav 86: 766-773, 2007.
34. Gardner EL. What we have learned about addiction from animal models of drug self-administration. Am J Addict 9: 285-313, 2000.
35. George O, Ghozland S, Azar MR, Cottone P, Zorrilla EP, Parsons LH, O'Dell LE, Richardson HN, Koob GF. CRF-CRF1 system activation mediates withdrawal-induced increases in nicotine self-administration in nicotine-dependent rats. Proc Natl Acad Sci USA 104: 17198-17203, 2007.
36. Ghitza UE, Gray SM, Epstein DH, Rice KC, Shaham Y. The anxiogenic drug yohimbine reinstates palatable food seeking in a rat relapse model: a role of CRF1 receptors. Neuropsychopharmacology 31: 2188-2196, 2006.
37. Gonzalez VM, Vitousek KM. Feared food in dieting and non-dieting young women: a preliminary validation of the Food Phobia Survey. Appetite 43: 155-173, 2004.
38. Grigson PS, Spector AC, Norgren R. Microstructural analysis of successive negative contrast in free-feeding and deprived rats. Physiol Behav 54: 909-916, 1993.
39. Hagan MM, Chandler PC, Wauford PK, Rybak RJ, Oswald KD. The role of palatable food and hunger as trigger factors in an animal model of stress induced binge eating. Int J Eat Disord 34: 183-197, 2003.
40. Hagan MM, Moss DE. Persistence of binge-eating patterns after a history of restriction with intermittent bouts of refeeding on palatable food in rats: implications for bulimia nervosa. Int J Eat Disord 22: 411-420, 1997.
41. Hagan MM, Wauford PK, Chandler PC, Jarrett LA, Rybak RJ, Blackburn K. A new animal model of binge eating: key synergistic role of past caloric restriction and stress. Physiol Behav 77: 45-54, 2002.
42. Heyser CJ, Moc K, Koob GF. Effects of naltrexone alone and in combination with acamprosate on the alcohol deprivation effect in rats. Neuropsychopharmacology 28: 1463-1471, 2003.
43. Hodos W. Progressive ratio as a measure of reward strength. Science 134: 943-944, 1961.
44. Hodos W, Kalman G. Effects of increment size and reinforcer volume on progressive ratio performance. J Exp Anal Behav 6: 387-392, 1963.
45. Hoefer ME, Voskanian SJ, Koob GF, Pulvirenti L. Effects of terguride, ropinirole, and acetyl-L-carnitine on methamphetamine withdrawal in the rat. Pharmacol Biochem Behav 83: 403-409, 2006.
46. Kales EF. Macronutrient analysis of binge eating in bulimia. Physiol Behav 48: 837-840, 1990.
47. Killeen PR. Economics, ecologics, and mechanics: The dynamics of responding under conditions of varying motivation. J Exp Anal Behav 64: 405-431, 1995.
48. Kitamura O, Wee S, Specio SE, Koob GF, Pulvirenti L. Escalation of methamphetamine self-administration in rats: a dose-effect function. Psychopharmacology 186: 48-53, 2006.
49. Knackstedt LA, Kalivas PW. Extended access to cocaine self-administration enhances drug-primed reinstatement but not behavioral sensitization. J Pharmacol Exp Ther 322: 1103-1109, 2007.
50. Knight LJ, Boland FJ. Restrained eating: an experimental disentanglement of the disinhibiting variables of perceived calories and food type. J Abnorm Psychol 98: 412-420, 1989.
51. Koob GF. Alcoholism: allostasis and beyond. Alcoholism Clin Exp Res 27: 232-243, 2003.
52. Koob GF. Animal models of craving for ethanol. Addiction 95 Suppl 2: S73-S81, 2000.
53. Koob GF, Le Moal M. Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24: 97-129, 2001.
54. Koob GF, Le Moal M. Plasticity of reward neurocircuitry and the 'dark side' of drug addiction. Nat Neurosci 8: 1442-1444, 2005.
55. Laessle RG, Tuschl RJ, Kotthaus BC, Pirke KM. Behavioral and biological correlates of dietary restraint in normal life. Appetite 12: 83-94, 1989.
56. Lenoir M, Ahmed SH. Heroin-induced reinstatement is specific to compulsive heroin use and dissociable from heroin reward and sensitization. Neuropsychopharmacology 32: 616-624, 2007.
57. LeSage MG, Burroughs D, Pentel PR. Effects of nicotine withdrawal on performance under a progressive-ratio schedule of sucrose pellet delivery in rats. Pharmacol Biochem Behav 83: 585-591, 2006.
58. Levin BE, Dunn-Meynell AA. Defense of body weight depends on dietary composition and palatability in rats with diet-induced obesity. Am J Physiol Regul Integr Comp Physiol 282: R46-R54, 2002.
59. Li TK. Clinical perspectives for the study of craving and relapse in animal models. Addiction 95 Suppl 2: S55-S60, 2000.
60. Loh EA, Roberts DC. Break-points on a progressive ratio schedule reinforced by intravenous cocaine increase following depletion of forebrain serotonin. Psychopharmacology 101: 262-266, 1990.
61. Lowe MR, Butryn ML. Hedonic hunger: a new dimension of appetite? Physiol Behav 91: 432-439, 2007.
62. Mantsch JR, Baker DA, Francis DM, Katz ES, Hoks MA, Serge JP. Stressor- and corticotropin-releasing factor-induced reinstatement and active stress-related behavioral responses are augmented following long-access cocaine self-administration by rats. Psychopharmacology 195: 591-603, 2008.
63. Markou A, Weiss F, Gold LH, Caine SB, Schulteis G, Koob GF. Animal models of drug craving. Psychopharmacology 112: 163-182, 1993.
64. McGregor A, Roberts DC. Dopaminergic antagonism within the nucleus accumbens or the amygdala produces differential effects on intravenous cocaine self-administration under fixed and progressive ratio schedules of reinforcement. Brain Res 624: 245-252, 1993.
65. Moreau JL, Jenck F, Martin JR, Mortas P, Haefely WE. Antidepressant treatment prevents chronic unpredictable mild stress-induced anhedonia as assessed by ventral tegmentum self-stimulation behavior in rats. Eur Neuropsychopharmacol 2: 43-49, 1992.
66. O'Dell LE, Koob GF. 'Nicotine deprivation effect' in rats with intermittent 23-hour access to intravenous nicotine self-administration. Pharmacol Biochem Behav 86: 346-353, 2007.
67. O'Dell LE, Roberts AJ, Smith RT, Koob GF. Enhanced alcohol self-administration after intermittent versus continuous alcohol vapor exposure. Alcohol Clin Exp Res 28: 1676-1682, 2004.
68. Orsini C, Koob GF, Pulvirenti L. Dopamine partial agonist reverses amphetamine withdrawal in rats. Neuropsychopharmacology 25: 789-792, 2001.
69. Paterson NE, Markou A. Increased motivation for self-administered cocaine after escalated cocaine intake. Neuroreport 14: 2229-2232, 2003.
70. Pinel JP, Huang E. Effects of periodic withdrawal on ethanol and saccharin selection in rats. Physiol Behav 16: 693-698, 1976.
71. Pinel JP, Mucha RF, Rovner LI. Temporary effects of periodic alcohol availability. Behav Biol 16: 227-232, 1976.
72. Polivy J, Herman CP. Dieting and binging. A causal analysis. Am Psychol 40: 193-201, 1985.
73. Roberts DC, Andrews MM, Vickers GJ. Baclofen attenuates the reinforcing effects of cocaine in rats. Neuropsychopharmacology 15: 417-423, 1996.
74. Roberts DC, Bennett SA, Vickers GJ. The estrous cycle affects cocaine self-administration on a progressive ratio schedule in rats. Psychopharmacology 98: 408-411, 1989.
75. Rodd ZA, Bell RL, Sable HJ, Murphy JM, McBride WJ. Recent advances in animal models of alcohol craving and relapse. Pharmacol Biochem Behav 79: 439-450, 2004.
76. Rodefer JS, Carroll ME. Progressive ratio and behavioral economic evaluation of the reinforcing efficacy of orally delivered phencyclidine and ethanol in monkeys: effects of feeding conditions. Psychopharmacology 128: 265-273, 1996.
77. Rogers PJ. Returning 'cafeteria-fed' rats to a chow diet: negative contrast and effects of obesity on feeding behaviour. Physiol Behav 35: 493-499, 1985.
78. Rygula R, Abumaria N, Flugge G, Fuchs E, Ruther E, Havemann-Reinecke U. Anhedonia and motivational deficits in rats: impact of chronic social stress. Behav Brain Res 162: 127-134, 2005.
79. Schroy PL, Wheeler RA, Davidson C, Scalera G, Twining RC, Grigson PS. Role of gustatory thalamus in anticipation and comparison of rewards over time in rats. Am J Physiol Regul Integr Comp Physiol 288: R966-R980, 2005.
80. Schwabe K, Koch M. Effects of aripiprazole on operant responding for a natural reward after psychostimulant withdrawal in rats. Psychopharmacology 191: 759-765, 2007.
81. Sclafani A, Ackroff K. Reinforcement value of sucrose measured by progressive ratio operant licking in the rat. Physiol Behav 79: 663-670, 2003.
82. Smith A, Piercey M, Roberts DC. Effect of (-)-DS 121 and (+)-UH 232 on cocaine self-administration in rats. Psychopharmacology 120: 93-98, 1995.
83. Snowdon CT. Motivation, regulation, and the control of meal parameters with oral and intragastric feeding. J Comp Physiol Psychol 69: 91-100, 1969.
84. Solomon RL, Corbit JD. An opponent-process theory of motivation. I. Temporal dynamics of affect. Psychol Rev 81: 119-145, 1974.
85. Spear DJ, Katz JL. Cocaine and food as reinforcers: effects of reinforcer magnitude and response requirement under second-order fixedratio and progressive-ratio schedules. J Exp Anal Behav 56: 261-275, 1991.
86. Stirling LJ, Yeomans MR. Effect of exposure to a forbidden food on eating in restrained and unrestrained women. Int J Eat Disord 35: 59-68, 2004.
87. Teegarden SL, Bale TL. Decreases in dietary preference produce increased emotionality and risk for dietary relapse. Biol Psychiatry 61: 1021-1029, 2007.
88. Thorndike EL. Animal Intelligence. New York: Macmillan, 1911.
89. Tolkamp BJ, Kyriazakis II. To split behaviour into bouts, log-transform the intervals. Anim Behav 57: 807-817, 1999.
90. Treit D, Spetch ML. Caloric regulation in the rat: control by two factors. Physiol Behav 36: 311-317, 1986.
91. Wayner MJ, Fraley S. Enhancement of the consumption of acclimated sapid solutions following periodic and prolonged withdrawal. Physiol Behav 9: 463-474, 1972.
92. Weatherly JN, Nurnberger JT, Hanson BC. Investigating the procedural variables that determine whether rats will display negative anticipatory contrast or positive induction. Behav Proc 70: 10-18, 2005.
93. Weatherly JN, Nurnberger JT, Kristiansen-Moen LA. The role of place of reinforcer delivery in the appearance of positive induction when rats respond for 1% sucrose. Behav Proc 73: 156-163, 2006.
94. Wee S, Mandyam CD, Lekic DM, Koob GF. alpha(1)-noradrenergic system role in increased motivation for cocaine intake in rats with prolonged access. Eur Neuropsychopharmacol 18: 303-311, 2007.
95. Wee S, Specio SE, Koob GF. Effects of dose and session duration on cocaine self-administration in rats. J Pharmacol Exp Ther 320: 1134-1143, 2007.
96. Wee S, Wang Z, Woolverton WL, Pulvirenti L, Koob GF. Effect of aripiprazole, a partial dopamine D2 receptor agonist, on increased rate of methamphetamine self-administration in rats with prolonged session duration. Neuropsychopharmacology 32: 2238-2247, 2007.
97. Wojnicki FH, Roberts DC, Corwin RL. Effects of baclofen on operant performance for food pellets and vegetable shortening after a history of binge-type behavior in non-food deprived rats. Pharmacol Biochem Behav 84: 197-206, 2006.
98. Yach D, Stuckler D, Brownell KD. Epidemiologic and economic consequences of the global epidemics of obesity and diabetes. Nat Med 12: 62-66, 2006.
99. Zernig G, Ahmed SH, Cardinal RN, Morgan D, Acquas E, Foltin RW, Vezina P, Negus SS, Crespo JA, Stockl P, Grubinger P, Madlung E, Haring C, Kurz M, Saria A. Explaining the escalation of drug use in substance dependence: models and appropriate animal laboratory tests. Pharmacology 80: 65-119, 2007.
100. Zhang D, Zhou X, Wang X, Xiang X, Chen H, Hao W. Morphine withdrawal decreases responding reinforced by sucrose self-administration in progressive ratio. Addiction Biol 12: 152-157, 2007.
101. Zorrilla EP, Inoue K, Fekete EM, Tabarin A, Valdez GR, Koob GF. Measuring meals: structure of prandial food and water intake of rats. Am J Physiol Regul Integr Comp Physiol 288: R1450-R1467, 2005.
102. Zorrilla EP, Inoue K, Valdez GR, Tabarin A, Koob GF. Leptin and post-prandial satiety: acute central leptin more potently reduces meal frequency than meal size in the rat. Psychopharmacology 177: 324-335, 2005.