Oral sucrose stimulation increases accumbens dopamine in the rat

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 286, Issue 1 55-1, 2004, Pages

  Hajnal, Andras ^a   Smith, Gerard P ^b   Norgren, Ralph ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Control of food intake; Motivation; Orosensory positive feedback

Indexed keywords

DOPAMINE; SUCROSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORRELATION ANALYSIS; DOPAMINE BRAIN LEVEL; DOPAMINE RELEASE; EXTRACELLULAR SPACE; FOOD INTAKE; MALE; MICRODIALYSIS; MOTIVATION; NEUROPHYSIOLOGY; NONHUMAN; NUCLEUS ACCUMBENS; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROVOCATION TEST; QUANTITATIVE ANALYSIS; RAT; REGULATORY MECHANISM; REWARD; SHAM FEEDING; TASTE; TEST MEAL;

EID: 0346455760     PISSN: 03636119     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpregu.00282.2003     Document Type: Article

References (77)

1. Barr AM and Phillips AG. Chronic mild stress has no effect on responding by rats for sucrose under a progressive ratio schedule. Physiol Behav 64: 591-597, 1998.
2. Bassareo V, De Luca MA, and Di Chiara G. Differential expression of motivational stimulus properties by dopamine in nucleus accumbens shell versus core and prefrontal cortex. J Neurosci 22: 4709-4719, 2002.
3. Bassareo V, De Luca MA, Aresu M, Aste A, Ariu T, and Di Chiara G. Differential adaptive properties of accumbens shell dopamine responses to ethanol as a drug and as a motivational stimulus. Eur J Neurosci 17: 1465-1472, 2003.
4. Bassareo V and Di Chiara G. Differential influence of associative and nonassociative learning mechanisms on the responsiveness of prefrontal and accumbal dopamine transmission to food stimuli in rats fed ad libitum. J Neurosci 17: 851-861, 1997.
5. Bassareo V and Di Chiara G. Differential responsiveness of dopamine transmission to food-stimuli in nucleus accumbens shell/core compartments. Neuroscience 89: 637-641, 1999.
6. Bassareo V and Di Chiara G. Modulation of feeding-induced activation of mesolimbic dopamine transmission by appetitive stimuli and its relation to motivational state. Eur J Neurosci 11: 4389-4397, 1999.
7. Bello NT, Lucas LR, and Hajnal A. Repeated sucrose access influences dopamine D2 receptor density in the striatum. Neuroreport 13: 1575-1578, 2002.
8. Bello NT, Sweigart KL, Lakoski JM, Norgren R, and 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.
9. Berridge KC. Food reward: brain substrates of wanting and liking. Neurosci Biobehav Rev 20: 1-25, 1996.
10. Berridge KC and Robinson TE. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28: 309-369, 1998.
11. Bjorklund A, and Lindvall O. Dopamine-containing systems in the CNS. In: Handbook of Chemical Neuroanatomy: Classical Transmitters in the CNS. New York: Elsevier Science, 1984, vol. 2, part I, chapt. 3, p. 55-122.
12. Brennan K, Roberts DC, Anisman H, and Merali Z. Individual differences in sucrose consumption in the rat: motivational and neurochemical correlates of hedonia. Psychopharmacology (Berl) 157: 269-276, 2001.
13. Brog JS, Salyapongse A, Deutch AY, and Zahm DS. The patterns of afferent innervation of the core and shell in the "accumbens" part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold. J Comp Neurol 338: 255-278, 1993.
14. Cador M, Taylor JR, and Robbins TW. Potentiation of the effects of reward-related stimuli by dopaminergic-dependent mechanisms in the nucleus accumbens. Psychopharmacology (Berl) 104: 377-385, 1991.
15. Caltabiano ML and Shellshear J. Palatability versus healthiness as determinants of food preferences in young adults: a comparison of nomothetic and idiographic analytic approaches. Aust NZ J Public Health 22: 547-551, 1998.
16. Cheeta S, Brooks S, and Willner P. Effects of reinforcer sweetness and the D2/D3 antagonist raclopride on progressive ratio operant performance. Behav Pharmacol 6: 127-132, 1995.
17. Church WH, Justice JB Jr., and Neill DB. Detecting behaviorally relevant changes in extracellular dopamine with microdialysis. Brain Res 412: 397-399, 1987.
18. Cross AT, Babicz D, and Cushman LF. Snacking patterns among 1,800 adults and children. J Am Diet Assoc 94: 1398-1403, 1994.
19. Davis JD. The effectiveness of some sugars in stimulating licking behavior in the rat. Physiol Behav 11: 39-45, 1973.
20. Davis JD and Smith GP. Learning to sham feed: behavioral adjustments to loss of physiological postingestional stimuli. Am J Physiol Regul Integr Comp Physiol 259: R1228-R1235, 1990.
21. Di Chiara G. A motivational learning hypothesis of the role of mesolimbic dopamine in compulsive drug use. J Psychopharmacol (Oxf) 12: 54-67, 1998.
22. Duong A and Weingarten HP. Dopamine antagonists act on central, but not peripheral, receptors to inhibit sham and real feeding. Physiol Behav 54: 449-454, 1993.
23. Figlewicz DP, Szot P, Chavez M, Woods SC, and Veith RC. Intraventricular insulin increases dopamine transporter mRNA in rat VTA/substantia nigra. Brain Res 644: 331-334, 1994.
24. Flaherty CF, Turovsky J, and Krauss KL. Relative hedonic value modulates anticipatory contrast. Physiol Behav 55: 1047-1054, 1994.
25. Geary N and Smith GP. Pimozide decreases the positive reinforcing effect of sham fed sucrose in the rat. Pharmacol Biochem Behav 22: 787-790, 1985.
26. Glanz K, Basil M, Maibach E, Goldberg J, and Snyder D. Why Americans eat what they do: taste, nutrition, cost, convenience, and weight control concerns as influences on food consumption. J Am Diet Assoc 98: 1118-1126, 1998.
27. Grigson PS, Spector AC, and Norgren R. Microstructural analysis of successive negative contrast in free-feeding and deprived rats. Physiol Behav 54: 909-916, 1993.
28. Grill HJ and Norgren R. The taste reactivity test. I. Mimetic responses to gustatory stimuli in neurologically normal rats. Brain Res 143: 263-279, 1978.
29. Hajnal A and Norgren R. Accumbens dopamine mechanisms in sucrose intake. Brain Res 904: 76-84, 2001.
30. Hajnal A and Norgren R. Repeated access to sucrose augments dopamine turnover in the nucleus accumbens. Neuroreport 13: 2213-2216, 2002.
31. Hajnal A, Smith GP, and Norgren R. Sham-feeding of sucrose increases accumbens dopamine in concentration-dependent manner: a microdialysis study in behaving rats. SSIB annual meeting 2001 (Abstract). Appetite 37: 141-142, 2001.
32. Hajnal A, Smith GP, and Norgren R. Sham-feeding of sucrose increases dopamine and decreases norepinephrine in the nucleus accumbens of the rat. SSIB annual meeting 2003 (Abstract). Appetite 40: 336, 2003.
33. Hall WG and Bryan TE. The ontogeny of feeding in rats: IV. Taste development as measured by intake and behavioral responses to oral infusions of sucrose and quinine. J Comp Physiol Psychol 95: 240-251, 1981.
34. Hsiao S and Smith GP. Raclopride reduces sucrose preference in rats. Pharmacol Biochem Behav 50: 121-125, 1995.
35. Ikemoto S and 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 31: 6-41. 1999.
36. Ito H and Seki M. Ascending projections from the area postrema and the nucleus of the solitary tract of Suncus murinus: anterograde tracing study using Phaseolus vulgaris leucoagglutinin. Okajimas Folia Anat Jpn 75: 9-31, 1998.
37. Kant AK. Consumption of energy-dense, nutrient-poor foods by adult Americans: nutritional and health implications. The third National Health and Nutrition Examination Survey, 1988-1994. Am J Clin Nutr 72: 929-936, 2000.
38. Kirouac GJ and Ciriello J. Cardiovascular afferent inputs to ventral tegmental area. Am J Physiol Regul Integr Comp Physiol 272: R1998-R2003, 1997.
39. Kirouac GJ and Ganguly PK. Topographical organization in the nucleus accumbens of afferents from the basolateral amygdala and efferents to the lateral hypothalamus. Neuroscience 67: 625-630, 1995.
40. Koob GF. Hedonic valence, dopamine and motivation. Mol Psychiatry 1: 186-189, 1996.
41. Mark GP, Blander DS, and Hoebel BG. A conditioned stimulus decreases extracellular dopamine in the nucleus accumbens after the development of a learned taste aversion. Brain Res 551: 308-310, 1991.
42. McCrory MA, Fuss PJ, Saltzman E, and Roberts SB. Dietary determinants of energy intake and weight regulation in healthy adults. J Nutr 130: 276S-279S, 2000.
43. McCrory MA, Suen VM, and Roberts SB. Biobehavioral influences on energy intake and adult weight gain. J Nutr 132: 3830S-3834S, 2002.
44. Nissenbaum JW and Sclafani A. Sham-feeding response of rats to Polycose and sucrose. Neurosci Biobehav Rev 11: 215-222, 1987.
45. Norgren R. Gustatory system. In: The Rat Nervous System, edited by Paxinos G. New York: Academic, 1995, p. 751-771.
46. Oades RD and Halliday GM. Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity. Brain Res 434: 117-165, 1987.
47. Park TH and Carr KD. Neuroanatomical patterns of fos-like immunoreactivity induced by a palatable meal and meal-paired environment in saline- and naltrexone-treated rats. Brain Res 805: 169-180, 1998.
48. Paxinos G and Watson C. The Rat Brain in Stereotaxic Coordinates (compact 3rd ed.). Sydney, Australia: Academic, 1997.
49. Phillips AG, Atkinson LJ, Blackburn JR, and Blaha CD. Increased extracellular dopamine in the nucleus accumbens of the rat elicited by a conditional stimulus for food: an electrochemical study. Can J Physiol Pharmacol 71: 387-393, 1993.
50. Phillips PE, Stuber GD, Heien ML, Wightman RM, and Carelli RM. Subsecond dopamine release promotes cocaine seeking. Nature 422: 614-618, 2003.
51. Phillipson OT. Afferent projections to the ventral tegmental area of Tsai and interfascicular nucleus: a horseradish peroxidase study in the rat. J Comp Neurol 187: 117-143, 1979.
52. Potter GM, Moshirfar A, and Castonguay TW. Insulin affects dopamine overflow in the nucleus accumbens and the striatum. Physiol Behav 65: 811-816, 1999.
53. Robbins TW and Everitt BJ. Neurobehavioural mechanisms of reward and motivation. Curr Opin Neurobiol 6: 228-236, 1996.
54. Salamone JD, Correa M, Mingote S, and Weber SM. Nucleus accumbens dopamine and the regulation of effort in food-seeking behavior: implications for studies of natural motivation, psychiatry, and drug abuse. J Pharmacol Exp Ther 305: 1-8, 2003.
55. Salamone JD, Cousins MS, McCullough LD, Carriero DL, and Berkowitz RJ. Nucleus accumbens dopamine release increases during instrumental lever pressing for food but not free food consumption. Pharmacol Biochem Behav 49: 25-31, 1994.
56. Schneider LH. Orosensory self-stimulation by sucrose involves brain dopaminergic mechanisms. Ann NY Acad Sci 575: 307-319, 1989.
57. Schneider LH, Davis JD, Watson CA, and Smith GP. Similar effect of raclopride and reduced sucrose concentration on the microstructure of sucrose sham feeding. Eur J Pharmacol 186: 61-70, 1990.
58. Schultz W. Dopamine neurons and their role in reward mechanisms. Curr Opin Neurobiol 7: 191-197, 1997.
59. Sclafani A. Carbohydrate taste, appetite, and obesity: an overview. Neurosci Biobehav Rev 11: 131-153, 1987.
60. Shi CJ and Cassell MD. Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices. J Comp Neurol 399: 440-468, 1998.
61. Shimura T, Kamada Y, and Yamamoto T. Ventral tegmental lesions reduce overconsumption of normally preferred taste fluid in rats. Behav Brain Res 134: 123-130, 2002.
62. Sills TL and Vaccarino FJ. Individual differences in sugar consumption following systemic or intraaccumbens administration of low doses of amphetamine in nondeprived rats. Pharmacol Biochem Behav 54: 665-670, 1996.
63. Smith GP. Dopamine and food reward. In: Progress in Psychobiology and Physiological Psychology, edited by Morrison A and Fluharty S. New York: Academic, 1995, vol. 15, p. 83-144.
64. Smith GP. Sham feeding in rats with chronic, reversible gastric fistulas. In: Current Protocols in Neuroscience. New York: Wiley, 1999, chapt. 8, unit 8.6D, p. 1-6.
65. Smith GP, Bourbonais KA, Jerome C, and Simansky KJ. Sham feeding of sucrose increases the ratio of 3,4-dihydroxyphenylacetic acid to dopamine in the hypothalamus. Pharmacol Biochem Behav 26: 585-591, 1987.
66. Smith GP and Schneider LH. Relationships between mesolimbic dopamine function and eating behavior. Ann NY Acad Sci 537: 254-261, 1988.
67. Spector AC, Travers SP, and Norgren R. Taste receptors on the anterior tongue and nasoincisor ducts of rats contribute synergistically to behavioral responses to sucrose. Behav Neurosci 107: 694-702, 1993.
68. Stratford TR and Kelley AE. Evidence of a functional relationship between the nucleus accumbens shell and lateral hypothalamus subserving the control of feeding behavior. J Neurosci 19: 11040-11048, 1999.
69. Szczypka MS, Kwok K, Brot MD, Marck BT, Matsumoto AM, Donahue BA, and Palmiter RD. Dopamine production in the caudate putamen restores feeding in dopamine-deficient mice. Neuron 30: 819-828, 2001.
70. Takada M and Hattori T. Organization of ventral tegmental area cells projecting to the occipital cortex and forebrain in the rat. Brain Res 418: 27-33, 1987.
71. Usuda I, Tanaka K, and Chiba T. Efferent projections of the nucleus accumbens in the rat with special reference to subdivision of the nucleus: biotinylated dextran amine study. Brain Res 797: 73-93, 1998.
72. Vigorito M, Kruse CB, and Carretta JC. Differential sensitivity of operant behaviors to changes in the concentration of a sucrose reinforcer: effects of pimozide. Pharmacol Biochem Behav 47: 515-522, 1994.
73. Weatherford SC, Greenberg D, Melville LD, Jerome C, Gibbs J, and Smith GP. Failure to detect increases in brain dopamine metabolism in rats sham feeding sucrose and corn oil. Pharmacol Biochem Behav 39: 1025-1028, 1991.
74. Weingarten HP and Kulikovsky OT. Taste-to-postingestive consequence conditioning: is the rise in sham feeding with repeated experience a learning phenomenon? Physiol Behav 45: 471-476, 1989.
75. Wise RA. Brain reward circuitry: insights from unsensed incentives. Neuron 36: 229-240. 2002.
76. 2 dopamine receptors in the acquisition and expression of flavor-preference conditioning in sham-feeding rats. Pharmacol Biochem Behav 67: 537-544, 2000.
77. Zagon A, Totterdell S, and Jones RS. Direct projections from the ventrolateral medulla oblongata to the limbic forebrain: anterograde and retrograde tract-tracing studies in the rat. J Comp Neurol 340: 445-468, 1994.