Intermittent access to sweet high-fat liquid induces increased palatability and motivation to consume in a rat model of binge consumption

Physiology and Behavior

Volumn 114-115, Issue , 2013, Pages 21-31

  Lardeux, Sylvie ^a   Kim, James J ^a   Nicola, Saleem M ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Binge eating disorder; Bulimia nervosa; Ingestive behavior; Licking; Motivation; Obesity; Palatability driven consumption; Satiety

Indexed keywords

CORN OIL; SUGAR;

ANIMAL EXPERIMENT; ARTICLE; BINGE EATING DISORDER; CONTROLLED STUDY; FEEDING BEHAVIOR; FOOD INTAKE; LIPID DIET; MALE; MOTIVATION; NONHUMAN; PALATABILITY; PRIORITY JOURNAL; RAT; SWEETNESS;

EID: 84875784409     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2013.03.005     Document Type: Article

References (83)

1. Bulik C.M., Reichborn-Kjennerud T. Medical morbidity in binge eating disorder. Int J Eat Disord 2003, 34(Suppl.):S39-S46.
2. Mathes W.F., Brownley K.A., Mo X., Bulik C.M. The biology of binge eating. Appetite 2009, 52:545-553.
3. Corwin R.L., Avena N.M., Boggiano M.M. Feeding and reward: perspectives from three rat models of binge eating. Physiol Behav 2011, 104:87-97.
4. Corwin R.L., Buda-Levin A. Behavioral models of binge-type eating. Physiol Behav 2004, 82:123-130.
5. Bello N.T., Guarda A.S., Terrillion C.E., Redgrave G.W., Coughlin J.W., Moran T.H. Repeated binge access to a palatable food alters feeding behavior, hormone profile, and hindbrain c-Fos responses to a test meal in adult male rats. Am J Physiol Regul Integr Comp Physiol 2009, 297:R622-R631.
6. Babbs R.K., Wojnicki F.H., Corwin R.L. Assessing binge eating. An analysis of data previously collected in bingeing rats. Appetite 2012, 59:478-482.
7. Colantuoni C., Rada P., McCarthy J., Patten C., Avena N.M., Chadeayne A., et al. Evidence that intermittent, excessive sugar intake causes endogenous opioid dependence. Obes Res 2002, 10:478-488.
8. Colantuoni C., Schwenker J., McCarthy J., Rada P., Ladenheim B., Cadet J.L., et al. Excessive sugar intake alters binding to dopamine and mu-opioid receptors in the brain. Neuroreport 2001, 12:3549-3552.
9. Avena N.M., Rada P., Hoebel B.G. Underweight rats have enhanced dopamine release and blunted acetylcholine response in the nucleus accumbens while bingeing on sucrose. Neuroscience 2008, 156:865-871.
10. Berner L.A., Avena N.M., Hoebel B.G. Bingeing, self-restriction, and increased body weight in rats with limited access to a sweet-fat diet. Obesity (Silver Spring) 2008, 16:1998-2002.
11. Corwin R.L., Wojnicki F.H., Fisher J.O., Dimitriou S.G., Rice H.B., Young M.A. Limited access to a dietary fat option affects ingestive behavior but not body composition in male rats. Physiol Behav 1998, 65:545-553.
12. Dimitriou S.G., Rice H.B., Corwin R.L. Effects of limited access to a fat option on food intake and body composition in female rats. Int J Eat Disord 2000, 28:436-445.
13. Kinzig K.P., Hargrave S.L., Honors M.A. Binge-type eating attenuates corticosterone and hypophagic responses to restraint stress. Physiol Behav 2008, 95:108-113.
14. Rada P., Avena N.M., Hoebel B.G. Daily bingeing on sugar repeatedly releases dopamine in the accumbens shell. Neuroscience 2005, 134:737-744.
15. Wojnicki F.H., Johnson D.S., Corwin R.L. Access conditions affect binge-type shortening consumption in rats. Physiol Behav 2008, 95:649-657.
16. Wong K.J., Wojnicki F.H., Corwin R.L. Baclofen, raclopride, and naltrexone differentially affect intake of fat/sucrose mixtures under limited access conditions. Pharmacol Biochem Behav 2009, 92:528-536.
17. Davis C., Carter J.C. Compulsive overeating as an addiction disorder. A review of theory and evidence. Appetite 2009, 53:1-8.
18. Avena N.M. Binge eating: neurochemical insights from animal models. Eat Disord 2009, 17:89-92.
19. Avena N.M., Rada P., Moise N., Hoebel B.G. Sucrose sham feeding on a binge schedule releases accumbens dopamine repeatedly and eliminates the acetylcholine satiety response. Neuroscience 2006, 139:813-820.
20. Liang N.C., Hajnal A., Norgren R. Sham feeding corn oil increases accumbens dopamine in the rat. Am J Physiol Regul Integr Comp Physiol 2006, 291:R1236-R1239.
21. Bello N.T., Sweigart K.L., Lakoski J.M., 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 2003, 284:R1260-R1268.
22. Bello N.T., Lucas L.R., Hajnal A. Repeated sucrose access influences dopamine D2 receptor density in the striatum. Neuroreport 2002, 13:1575-1578.
23. Berridge K.C. 'Liking' and 'wanting' food rewards: brain substrates and roles in eating disorders. Physiol Behav 2009, 97:537-550.
24. Kelley A.E., Bakshi V.P., Haber S.N., Steininger T.L., Will M.J., Zhang M. Opioid modulation of taste hedonics within the ventral striatum. Physiol Behav 2002, 76:365-377.
25. Taha S.A. Preference or fat? Revisiting opioid effects on food intake. Physiol Behav 2010, 100:429-437.
26. Katsuura Y., Heckmann J.A., Taha S.A. mu-Opioid receptor stimulation in the nucleus accumbens elevates fatty tastant intake by increasing palatability and suppressing satiety signals. Am J Physiol 2011, 301:R244-R254.
27. Smith G.P. John Davis and the meanings of licking. Appetite 2001, 36:84-92.
28. Warwick Z.S. Dietary fat dose dependently increases spontaneous caloric intake in rat. Obes Res 2003, 11:859-864.
29. Warwick Z.S., McGuire C.M., Bowen K.J., Synowski S.J. Behavioral components of high-fat diet hyperphagia: meal size and postprandial satiety. Am J Physiol Regul Integr Comp Physiol 2000, 278:R196-R200.
30. Grill H.J., Norgren R. The taste reactivity test. I. Mimetic responses to gustatory stimuli in neurologically normal rats. Brain Res 1978, 143:263-279.
31. Hodos W. Progressive ratio as a measure of reward strength. Science 1961, 134:943-944.
32. Hodos W., Kalman G. Effects of increment size and reinforcer volume on progressive ratio performance. J Exp Anal Behav 1963, 6:387-392.
33. Stewart W.J. Progressive reinforcement schedules: a review and evaluation. Aust J Psychol 1975, 27:9-22.
34. Davis J.D., Smith G.P. Learning to sham feed: behavioral adjustments to loss of physiological postingestional stimuli. Am J Physiol Regul Integr Comp Physiol 1990, 259:R1228-R1235.
35. Bocarsly M.E., Berner L.A., Hoebel B.G., Avena N.M. Rats that binge eat fat-rich food do not show somatic signs or anxiety associated with opiate-like withdrawal: implications for nutrient-specific food addiction behaviors. Physiol Behav 2011, 104:865-872.
36. Davis J.D., Perez M.C. Food deprivation- and palatability-induced microstructural changes in ingestive behavior. Am J Physiol 1993, 264:R97-R103.
37. Spector A.C., Klumpp P.A., Kaplan J.M. Analytical issues in the evaluation of food deprivation and sucrose concentration effects on the microstructure of licking behavior in the rat. Behav Neurosci 1998, 112:678-694.
38. Baird J.P., St John S.J., Nguyen E.A. Temporal and qualitative dynamics of conditioned taste aversion processing: combined generalization testing and licking microstructure analysis. Behav Neurosci 2005, 119:983-1003.
39. Cottone P., Sabino V., Steardo L., Zorrilla E.P. Opioid-dependent anticipatory negative contrast and binge-like eating in rats with limited access to highly preferred food. Neuropsychopharmacology 2008, 33:524-535.
40. Wojnicki F.H., Stine J.G., Corwin R.L. Liquid sucrose bingeing in rats depends on the access schedule, concentration and delivery system. Physiol Behav 2007, 92:566-574.
41. Boggiano M.M., Artiga A.I., Pritchett C.E., Chandler-Laney P.C., Smith M.L., Eldridge A.J. High intake of palatable food predicts binge-eating independent of susceptibility to obesity: an animal model of lean vs obese binge-eating and obesity with and without binge-eating. Int J Obes (Lond) 2007, 31:1357-1367.
42. Rao R.E., Wojnicki F.H., Coupland J., Ghosh S., Corwin R.L. Baclofen, raclopride, and naltrexone differentially reduce solid fat emulsion intake under limited access conditions. Pharmacol Biochem Behav 2008, 89:581-590.
43. R Development Core Team R: a language and environment for statistical computing 2012, R foundation for Statistical, Computing, Vienna, Austria.
44. Taha S.A., Katsuura Y., Noorvash D., Seroussi A., Fields H.L. Convergent, not serial, striatal and pallidal circuits regulate opioid-induced food intake. Neuroscience 2009, 161:718-733.
45. Engelberg M.J., Gauvin L., Steiger H. A naturalistic evaluation of the relation between dietary restraint, the urge to binge, and actual binge eating: a clarification. Int J Eat Disord 2005, 38:355-360.
46. Fedoroff I.D.C., Polivy J., Herman C.P. The effect of pre-exposure to food cues on the eating behavior of restrained and unrestrained eaters. Appetite 1997, 28:33-47.
47. Bartholome L.T., Raymond N.C., Lee S.S., Peterson C.B., Warren C.S. Detailed analysis of binges in obese women with binge eating disorder: comparisons using multiple methods of data collection. Int J Eat Disord 2006, 39:685-693.
48. Guss J.L., Kissileff H.R., Devlin M.J., Zimmerli E., Walsh B.T. Binge size increases with body mass index in women with binge-eating disorder. Obes Res 2002, 10:1021-1029.
49. Kales E.F. Macronutrient analysis of binge eating in bulimia. Physiol Behav 1990, 48:837-840.
50. Bello N.T., Patinkin Z.W., Moran T.H. Opioidergic consequences of dietary-induced binge eating. Physiol Behav 2011, 104:98-104.
51. Castonguay T.W., Burdick S.L., Guzman M.A., Collier G.H., Stern J.S. Self-selection and the obese Zucker rat: the effect of dietary fat dilution. Physiol Behav 1984, 33:119-126.
52. Lucas F., Ackroff K., Sclafani A. Dietary fat-induced hyperphagia in rats as a function of fat type and physical form. Physiol Behav 1989, 45:937-946.
53. Lucas F., Sclafani A. Hyperphagia in rats produced by a mixture of fat and sugar. Physiol Behav 1990, 47:51-55.
54. Lucas F., Ackroff K., Sclafani A. High-fat diet preference and overeating mediated by postingestive factors in rats. Am J Physiol 1998, 275:R1511-R1522.
55. Synowski S.J., Smart A.B., Warwick Z.S. Meal size of high-fat food is reliably greater than high-carbohydrate food across externally-evoked single-meal tests and long-term spontaneous feeding in rat. Appetite 2005, 45:191-194.
56. Warwick Z.S., Synowski S.J., Bell K.R. Dietary fat content affects energy intake and weight gain independent of diet caloric density in rats. Physiol Behav 2002, 77:85-90.
57. Warwick Z.S., Synowski S.J., Rice K.D., Smart A.B. Independent effects of diet palatability and fat content on bout size and daily intake in rats. Physiol Behav 2003, 80:253-258.
58. Warwick Z.S., Weingarten H.P. Determinants of high-fat diet hyperphagia: experimental dissection of orosensory and postingestive effects. Am J Physiol 1995, 269:R30-R37.
59. Avena N.M., Rada P., Hoebel B.G. Sugar and fat bingeing have notable differences in addictive-like behavior. J Nutr 2009, 139:623-628.
60. Buda-Levin A., Wojnicki F.H., Corwin R.L. Baclofen reduces fat intake under binge-type conditions. Physiol Behav 2005, 86:176-184.
61. Corwin R.L., Wojnicki F.H. Binge eating in rats with limited access to vegetable shortening. Curr Protoc Neurosci 2006, 9. 23B1-9.23B11.
62. Wojnicki F.H., Charny G., Corwin R.L. Binge-type behavior in rats consuming trans-fat-free shortening. Physiol Behav 2008, 94:627-629.
63. Corwin R.L., Wojnicki F.H. Baclofen, raclopride, and naltrexone differentially affect intake of fat and sucrose under limited access conditions. Behav Pharmacol 2009, 20:537-548.
64. Davis J.D., Smith G.P. Analysis of the microstructure of the rhythmic tongue movements of rats ingesting maltose and sucrose solutions. Behav Neurosci 1992, 106:217-228.
65. Weingarten H.P. Conditioned cues elicit feeding in sated rats: a role for learning in meal initiation. Science 1983, 220:431-433.
66. Ikemoto S., Panksepp J. The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res Brain Res Rev 1999, 31:6-41.
67. Nicola S.M. The flexible approach hypothesis: unification of effort and cue-responding hypotheses for the role of nucleus accumbens dopamine in the activation of reward-seeking behavior. J Neurosci 2010, 30:16585-16600.
68. Parkinson J.A., Olmstead M.C., Burns L.H., Robbins T.W., Everitt B.J. Dissociation in effects of lesions of the nucleus accumbens core and shell on appetitive pavlovian approach behavior and the potentiation of conditioned reinforcement and locomotor activity by d-amphetamine. J Neurosci 1999, 19:2401-2411.
69. Yun I.A., Wakabayashi K.T., Fields H.L., Nicola S.M. The ventral tegmental area is required for the behavioral and nucleus accumbens neuronal firing responses to incentive cues. J Neurosci 2004, 24:2923-2933.
70. Wojnicki F.H., Babbs R.K., Corwin R.L. Reinforcing efficacy of fat, as assessed by progressive ratio responding, depends upon availability not amount consumed. Physiol Behav 2010, 100:316-321.
71. Bari A.A., Pierce R.C. D1-like and D2 dopamine receptor antagonists administered into the shell subregion of the rat nucleus accumbens decrease cocaine, but not food, reinforcement. Neuroscience 2005, 135:959-968.
72. Kelley A.E., Baldo B.A., Pratt W.E., Will M.J. Corticostriatal-hypothalamic circuitry and food motivation: integration of energy, action and reward. Physiol Behav 2005, 86:773-795.
73. Smith K.S., Tindell A.J., Aldridge J.W., Berridge K.C. Ventral pallidum roles in reward and motivation. Behav Brain Res 2009, 196:155-167.
74. Yamamoto T. Central mechanisms of roles of taste in reward and eating. Acta Physiol Hung 2008, 95:165-186.
75. Bakshi V.P., Kelley A.E. Feeding induced by opioid stimulation of the ventral striatum: role of opiate receptor subtypes. J Pharmacol Exp Ther 1993, 265:1253-1260.
76. Taha S.A., Norsted E., Lee L.S., Lang P.D., Lee B.S., Woolley J.D., et al. Endogenous opioids encode relative taste preference. Eur J Neurosci 2006, 24:1220-1226.
77. Zhang M., Gosnell B.A., Kelley A.E. Intake of high-fat food is selectively enhanced by mu opioid receptor stimulation within the nucleus accumbens. J Pharmacol Exp Ther 1998, 285:908-914.
78. Zhang M., Kelley A.E. Opiate agonists microinjected into the nucleus accumbens enhance sucrose drinking in rats. Psychopharmacology (Berl) 1997, 132:350-360.
79. Shin A.C., Townsend R.L., Patterson L.M., Berthoud H.R. "Liking" and "wanting" of sweet and oily food stimuli as affected by high-fat diet-induced obesity, weight loss, leptin, and genetic predisposition. Am J Physiol Regul Integr Comp Physiol 2011, 301:R1267-R1280.
80. Furnes M., Zhao C.-M., Chen D. Development of obesity is associated with increased calories per meal rather than per day. A study of high-fat diet-induced obesity in young rats. Obes Surg 2009, 19:1430-1438.
81. Johnson A.W. Dietary manipulations influence sucrose acceptance in diet induced obese mice. Appetite 2012, 58:215-221.
82. Marco A., Schroeder M., Weller A. Microstructural pattern of palatable food intake from weaning to adulthood in male and female OLETF rats. Behav Neurosci 2009, 123:1251-1260.
83. Zimmerli E.J., Devlin M.J., Kissileff H.R., Walsh B.T. The development of satiation in bulimia nervosa. Physiol Behav 2010, 100:346-349.