Reversible suppression of food reward behavior by chronic mu-opioid receptor antagonism in the nucleus accumbens

Neuroscience

Volumn 170, Issue 2, 2010, Pages 580-588

  Shin, A C ^a   Pistell, P J ^a   Phifer, C B ^b   Berthoud, H R ^a  

^a PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^b NORTHWESTERN STATE UNIVERSITY   (United States)

Author keywords

Hedonic value; Obesity; Reward; Taste reactivity; Ventral striatum; Working for food

Indexed keywords

BETA FUNALTREXAMINE; CORN OIL; MU OPIATE RECEPTOR; SUCROSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEEDING BEHAVIOR; FOOD INTAKE; HYPERPHAGIA; MALE; NEUROPATHOLOGY; NONHUMAN; NUCLEUS ACCUMBENS; OBESITY; PALATABILITY; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; REINFORCEMENT; REWARD; SIGNAL TRANSDUCTION;

ANIMALS; APPETITIVE BEHAVIOR; MALE; MICROINJECTIONS; MOTIVATION; NALTREXONE; NUCLEUS ACCUMBENS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, MU; REINFORCEMENT (PSYCHOLOGY); REWARD; SUCROSE;

EID: 77956181460     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.07.017     Document Type: Article

References (63)

1. Arjune D., Standifer K.M., Pasternak G.W., Bodnar R.J. Reduction by central beta-funaltrexamine of food intake in rats under freely-feeding, deprivation and glucoprivic conditions. Brain Res 1990, 535:101-109.
2. Berridge K.C. Food reward: brain substrates of wanting and liking. Neurosci Biobehav Rev 1996, 20:1-25.
3. Berridge K.C. Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns. Neurosci Biobehav Rev 2000, 24:173-198.
4. Berridge K.C. The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology (Berl) 2007, 191:391-431.
5. Berridge K.C., Kringelbach M.L. Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology (Berl) 2008, 199:457-480.
6. Berridge K.C., Robinson T.E. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?. Brain Res Brain Res Rev 1998, 28:309-369.
7. Berridge K.C., Robinson T.E. Parsing reward. Trends Neurosci 2003, 26:507-513.
8. Cardinal R.N., Everitt B.J. Neural and psychological mechanisms underlying appetitive learning: links to drug addiction. Curr Opin Neurobiol 2004, 14:156-162.
9. Cardinal R.N., Parkinson J.A., Hall J., Everitt B.J. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 2002, 26:321-352.
10. Carelli R.M. The nucleus accumbens and reward: neurophysiological investigations in behaving animals. Behav Cogn Neurosci Rev 2002, 1:281-296.
11. Cole J.L., Berman N., Bodnar R.J. Evaluation of chronic opioid receptor antagonist effects upon weight and intake measures in lean and obese Zucker rats. Peptides 1997, 18:1201-1207.
12. Cole J.L., Leventhal L., Pasternak G.W., Bowen W.D., Bodnar R.J. Reductions in body weight following chronic central opioid receptor subtype antagonists during development of dietary obesity in rats. Brain Res 1995, 678:168-176.
13. Cooper S.J., Jackson A., Morgan R., Carter R. Evidence for opiate receptor involvement in the consumption of a high palatability diet in nondeprived rats. Neuropeptides 1985, 5:345-348.
14. Ettenberg A. The runway model of drug self-administration. Pharmacol Biochem Behav 2009, 91:271-277.
15. Everitt B.J., Robbins T.W. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 2005, 8:1481-1489.
16. Glass M.J., Billington C.J., Levine A.S. Opioids and food intake: distributed functional neural pathways?. Neuropeptides 1999, 33:360-368.
17. 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.
18. Grill H.J., Norgren R. The taste reactivity test. II. Mimetic responses to gustatory stimuli in chronic thalamic and chronic decerebrate rats. Brain Res 1978, 143:281-297.
19. Heyman J.S., Jiang Q., Rothman R.B., Mosberg H.I., Porreca F. Modulation of mu-mediated antinociception by delta agonists: characterization with antagonists. Eur J Pharmacol 1989, 169:43-52.
20. Holtzman S.G. Behavioral effects of separate and combined administration of naloxone and d-amphetamine. J Pharmacol Exp Ther 1974, 189:51-60.
21. 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.
22. Kelley A.E., Berridge K.C. The neuroscience of natural rewards: relevance to addictive drugs. J Neurosci 2002, 22:3306-3311.
23. Kelley A.E., Bless E.P., Swanson C.J. Investigation of the effects of opiate antagonists infused into the nucleus accumbens on feeding and sucrose drinking in rats. J Pharmacol Exp Ther 1996, 278:1499-1507.
24. Kringelbach M.L. Food for thought: hedonic experience beyond homeostasis in the human brain. Neuroscience 2004, 126:807-819.
25. Lenard N.R., Zheng H., Berthoud H.R. Chronic suppression of mu-opioid receptor signaling in the nucleus accumbens attenuates development of diet-induced obesity in rats. Int J Obes (Lond) 2010, 34:1001-1010.
26. Martin T.J., Dworkin S.I., Smith J.E. Alkylation of mu opioid receptors by beta-funaltrexamine in vivo: comparison of the effects on in situ binding and heroin self-administration in rats. J Pharmacol Exp Ther 1995, 272:1135-1140.
27. Martin W.R., Wikler A., Eades C.G., Pescor F.T. Tolerance to and physical dependence on morphine in rats. Psychopharmacologia 1963, 4:247-260.
28. McFarland K., Ettenberg A. Haloperidol does not affect motivational processes in an operant runway model of food-seeking behavior. Behav Neurosci 1998, 112:630-635.
29. Mogenson G.J., Jones D.L., Yim C.Y. From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol 1980, 14:69-97.
30. Morley J.E., Levine A.S., Yim G.K., Lowy M.T. Opioid modulation of appetite. Neurosci Biobehav Rev 1983, 7:281-305.
31. Mucha R.F., Iversen S.D. Increased food intake after opioid microinjections into nucleus accumbens and ventral tegmental area of rat. Brain Res 1986, 397:214-224.
32. Nicholson C. Diffusion from an injected volume of a substance in brain tissue with arbitrary volume fraction and tortuosity. Brain Res 1985, 333:325-329.
33. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic Press, San Diego, CA.
34. Pecina S., Berridge K.C. Opioid site in nucleus accumbens shell mediates eating and hedonic "liking" for food: map based on microinjection Fos plumes. Brain Res 2000, 863:71-86.
35. Pecina S., Berridge K.C. Hedonic hot spot in nucleus accumbens shell: where do mu-opioids cause increased hedonic impact of sweetness?. J Neurosci 2005, 25:11777-11786.
36. Pecina S., Cagniard B., Berridge K.C., Aldridge J.W., Zhuang X. Hyperdopaminergic mutant mice have higher "wanting" but not "liking" for sweet rewards. J Neurosci 2003, 23:9395-9402.
37. Ragnauth A., Moroz M., Bodnar R.J. Multiple opioid receptors mediate feeding elicited by mu and delta opioid receptor subtype agonists in the nucleus accumbens shell in rats. Brain Res 2000, 876:76-87.
38. Rothman R.B., Long J.B., Bykov V., Jacobson A.E., Rice K.C., Holaday J.W. beta-FNA binds irreversibly to the opiate receptor complex: in vivo and in vitro evidence. J Pharmacol Exp Ther 1988, 247:405-416.
39. Salamone J.D., Correa M., Farrar A.M., Nunes E.J., Pardo M. Dopamine, behavioral economics, and effort. Front Behav Neurosci 2009, 3:13.
40. Schultz W., Dayan P., Montague P.R. A neural substrate of prediction and reward. Science 1997, 275:1593-1599.
41. South T., Deng C., Huang X.F. AM 251 and beta-Funaltrexamine reduce fat intake in a fat-preferring strain of mouse. Behav Brain Res 2007, 181:153-157.
42. Spector A.C., Redman R., Garcea M. The consequences of gustatory nerve transection on taste-guided licking of sucrose and maltose in the rat. Behav Neurosci 1996, 110:1096-1109.
43. Statnick M.A., Tinsley F.C., Eastwood B.J., Suter T.M., Mitch C.H., Heiman M.L. Peptides that regulate food intake: antagonism of opioid receptors reduces body fat in obese rats by decreasing food intake and stimulating lipid utilization. Am J Physiol Regul Integr Comp Physiol 2003, 284:R1399-R1408.
44. Tabarin A., Diz-Chaves Y., Carmona Mdel C., Catargi B., Zorrilla E.P., Roberts A.J., Coscina D.V., Rousset S., Redonnet A., Parker G.C., Inoue K., Ricquier D., Penicaud L., Kieffer B.L., Koob G.F. Resistance to diet-induced obesity in mu-opioid receptor-deficient mice: evidence for a "thrifty gene". Diabetes 2005, 54:3510-3516.
45. Takemori A.E., Larson D.L., Portoghese P.S. The irreversible narcotic antagonistic and reversible agonistic properties of the fumaramate methyl ester derivative of naltrexone. Eur J Pharmacol 1981, 70:445-451.
46. Takemori A.E., Portoghese P.S. Evidence for the interaction of morphine with kappa and delta opioid receptors to induce analgesia in beta-funaltrexamine-treated mice. J Pharmacol Exp Ther 1987, 243:91-94.
47. Volkow N.D., Wang G.J., Fowler J.S., Telang F. Overlapping neuronal circuits in addiction and obesity: evidence of systems pathology. Philos Trans R Soc Lond B Biol Sci 2008, 363:3191-3200.
48. Volkow N.D., Wise R.A. How can drug addiction help us understand obesity?. Nat Neurosci 2005, 8:555-560.
49. Ward H.G., Nicklous D.M., Aloyo V.J., Simansky K.J. Mu-opioid receptor cellular function in the nucleus accumbens is essential for hedonically driven eating. Eur J Neurosci 2006, 23:1605-1613.
50. Ward H.G., Simansky K.J. Chronic prevention of mu-opioid receptor (MOR) G-protein coupling in the pontine parabrachial nucleus persistently decreases consumption of standard but not palatable food. Psychopharmacology (Berl) 2006, 187:435-446.
51. Ward S.J., Portoghese P.S., Takemori A.E. Improved assays for the assessment of kappa- and delta-properties of opioid ligands. Eur J Pharmacol 1982, 85:163-170.
52. Will M.J., Franzblau E.B., Kelley A.E. Nucleus accumbens mu-opioids regulate intake of a high-fat diet via activation of a distributed brain network. J Neurosci 2003, 23:2882-2888.
53. Will M.J., Pratt W.E., Kelley A.E. Pharmacological characterization of high-fat feeding induced by opioid stimulation of the ventral striatum. Physiol Behav 2006, 89:226-234.
54. Wilson C., Nomikos G.G., Collu M., Fibiger H.C. Dopaminergic correlates of motivated behavior: importance of drive. J Neurosci 1995, 15:5169-5178.
55. Wise R.A. Forebrain substrates of reward and motivation. J Comp Neurol 2005, 493:115-121.
56. Woolley J.D., Lee B.S., Fields H.L. Nucleus accumbens opioids regulate flavor-based preferences in food consumption. Neuroscience 2006, 143:309-317.
57. Wyvell C.L., Berridge K.C. Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: enhancement of reward "wanting" without enhanced "liking" or response reinforcement. J Neurosci 2000, 20:8122-8130.
58. Wyvell C.L., Berridge K.C. Incentive sensitization by previous amphetamine exposure: increased cue-triggered "wanting" for sucrose reward. J Neurosci 2001, 21:7831-7840.
59. Zhang M., Balmadrid C., Kelley A.E. Nucleus accumbens opioid, GABaergic, and dopaminergic modulation of palatable food motivation: contrasting effects revealed by a progressive ratio study in the rat. Behav Neurosci 2003, 117:202-211.
60. 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.
61. Zhang M., Kelley A.E. Opiate agonists microinjected into the nucleus accumbens enhance sucrose drinking in rats. Psychopharmacology (Berl) 1997, 132:350-360.
62. Zheng H., Patterson L.M., Berthoud H.R. Orexin signaling in the ventral tegmental area is required for high-fat appetite induced by opioid stimulation of the nucleus accumbens. J Neurosci 2007, 27:11075-11082.
63. Zuberi A.R., Townsend L., Patterson L., Zheng H., Berthoud H.R. Increased adiposity on normal diet, but decreased susceptibility to diet-induced obesity in mu-opioid receptor-deficient mice. Eur J Pharmacol 2008, 585:14-23.