The gut-brain dopamine axis: A regulatory system for caloric intake

Physiology and Behavior

Volumn 106, Issue 3, 2012, Pages 394-399

  De Araujo, Ivan E ^a,b   Ferreira, Jozélia G ^a,b   Tellez, Luis A ^a,b   Ren, Xueying ^a,b   Yeckel, Catherine W ^a,b  

^a JOHN B PIERCE LABORATORY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calorie intake; Dopamine; Flavor; Gastrointestinal tract

Indexed keywords

CHOLECYSTOKININ; DOPAMINE; DOPAMINE RECEPTOR; GHRELIN; GLUCOSE; INSULIN;

ARTICLE; BRAIN; CALORIC DENSITY; CALORIC INTAKE; CHEMICAL COMPOSITION; CORPUS STRIATUM; DIETARY INTAKE; DOPAMINE RELEASE; FEEDING; FEEDING BEHAVIOR; GASTROINTESTINAL ABSORPTION; GASTROINTESTINAL TRACT; GLUCOSE METABOLISM; GLUCOSE UTILIZATION; HUMAN; INTESTINE; MESENCEPHALON; MICRODIALYSIS; NONHUMAN; NUTRIENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; STOMACH DISTENSION; STOMACH EMPTYING; STOMACH MOTILITY; STOMACH SECRETION; SUBSTANTIA NIGRA;

ANIMALS; BRAIN; DOPAMINE; EATING; ENERGY INTAKE; FEEDING BEHAVIOR; GASTROINTESTINAL TRACT; HUMANS; SENSATION;

EID: 84860441219     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2012.02.026     Document Type: Article

References (70)

1. Sclafani A. Post-ingestive positive controls of ingestive behavior. Appetite 2001, 36(1):79-83.
2. Mobini S., Chambers L.C., Yeomans M.R. Effects of hunger state on flavour pleasantness conditioning at home: flavour-nutrient learning vs. flavour-flavour learning. Appetite 2007, 48(1):20-28.
3. Yeomans M.R., Gould N.J., Leitch M., Mobini S. Effects of energy density and portion size on development of acquired flavour liking and learned satiety. Appetite 2009, 52(2):469-478.
4. de Araujo I.E., Oliveira-Maia A.J., Sotnikova T.D., Gainetdinov R.R., Caron M.G., Nicolelis M.A., et al. Food reward in the absence of taste receptor signaling. Neuron 2008, 57(6):930-941.
5. Ren X., Ferreira J.G., Zhou L., Shammah-Lagnado S.J., Yeckel C.W., De Araujo I.E. Nutrient Selection in the Absence of Taste Receptor Signaling. J Neurosci 2010, 30:8012-8023.
6. Sclafani A., Touzani K., Bodnar R.J. Dopamine and learned food preferences. Physiol Behav 2011, 104(1):64-68.
7. Sotak B.N., Hnasko T.S., Robinson S., Kremer E.J., Palmiter R.D. Dysregulation of dopamine signaling in the dorsal striatum inhibits feeding. Brain Res 2005, 1061(2):88-96.
8. Hernandez L., Hoebel B.G. Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. Life Sci 1988, 42(18):1705-1712.
9. Small D.M., Jones-Gotman M., Dagher A. Feeding-induced dopamine release in dorsal striatum correlates with meal pleasantness ratings in healthy human volunteers. Neuroimage 2003, 19(4):1709-1715.
10. Hajnal A., Smith G.P., Norgren R. Oral sucrose stimulation increases accumbens dopamine in the rat. Am J Physiol Regul Integr Comp Physiol 2004, 286(1):R31-R37.
11. 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(5):R1236-R1239.
12. Ferreira J.G., Tellez L.A., Ren X., Yeckel C.W., de Araujo I.E. Regulation of fat intake in the absence of flavor signaling. J Physiol 2012, 590:953-972.
13. Schultz W., Dayan P., Montague P.R. A neural substrate of prediction and reward. Science 1997, 275:1593-1599.
14. Wise R.A. Role of brain dopamine in food reward and reinforcement. Philos Trans R Soc Lond B Biol Sci 2006, 361(1471):1149-1158.
15. Ackroff K., Sclafani A. Energy density and macronutrient composition determine flavor preference conditioned by intragastric infusions of mixed diets. Physiol Behav 2006, 89:250-260.
16. Palmiter R.D. Is dopamine a physiologically relevant mediator of feeding behavior?. Trends Neurosci 2007, 30(8):375-381.
17. Malik S., McGlone F., Bedrossian D., Dagher A. Ghrelin modulates brain activity in areas that control appetitive behavior. Cell Metab 2008, 7(5):400-409.
18. Grill H.J., Norgren R. Chronically decerebrate rats demonstrate satiation but not bait shyness. Science 1978, 201(4352):267-269.
19. Kaplan J.M., Seeley R.J., Grill H.J. Daily caloric intake in intact and chronic decerebrate rats. Behav Neurosci 1993, 107(5):876-881.
20. Norgren R. Gustatory afferents to ventral forebrain. Brain Res 1974, 81:285-295.
21. Norgren R. Projections from the nucleus of the solitary tract in the rat. Neuroscience 1978, 3:207-218.
22. Cannon C.M., Palmiter R.D. Reward without Dopamine. J Neurosci 2003, 23(34):10827-10831.
23. Johnson P.M., Kenny P.J. Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci 2010, 13(5):635-641.
24. Geiger B.M., Haburcak M., Avena N.M., Moyer M.C., Hoebel B.G., Pothos E.N. Deficits of mesolimbic dopamine neurotransmission in rat dietary obesity. Neuroscience 2009, 159(4):1193-1199.
25. Rada P., Bocarsly M.E., Barson J.R., Hoebel B.G., Leibowitz S.F. Reduced accumbens dopamine in Sprague-Dawley rats prone to overeating a fat-rich diet. Physiol Behav 2010, 101(3):394-400.
26. Stice E., Spoor S., Bohon C., Small D.M. Relation between obesity and blunted striatal response to food is moderated by TaqIA A1 allele. Science 2008, 322(5900):449-452.
27. McHugh P.R. The control of gastric emptying. J Auton Nerv Syst 1983, 9(1):221-231.
28. McHugh P.R., Moran T.H. Calories and gastric emptying: a regulatory capacity with implications for feeding. Am J Physiol 1979, 236(5):R254-R260.
29. Kaplan J.M., Spector A.C., Grill H.J. Dynamics of gastric emptying during and after stomach fill. Am J Physiol 1992, 263(4 Pt 2):R813-R819.
30. Kaplan J.M., Siemers W.H., Smedh U., Schwartz G.J., Grill H.J. Gastric branch vagotomy and gastric emptying during and after intragastric infusion of glucose. Am J Physiol 1997, 273(5 Pt 2):R1786-R1792.
31. Tschöp M., Smiley D.L., Heiman M.L. Ghrelin induces adiposity in rodents. Nature 2000, 407:908-913.
32. Andrews Z.B., Erion D., Beiler R., Liu Z.W., Abizaid A., Zigman J., et al. Ghrelin promotes and protects nigrostriatal dopamine function via a UCP2-dependent mitochondrial mechanism. J Neurosci 2009, 29(45):14057-14065.
33. Jerlhag E., Engel J.A. Ghrelin receptor antagonism attenuates nicotine-induced locomotor stimulation, accumbal dopamine release and conditioned place preference in mice. Drug Alcohol Depend 2011, 117(2-3):126-131.
34. Skibicka K.P., Hansson C., Egecioglu E., Dickson S.L. Role of ghrelin in food reward: impact of ghrelin on sucrose self-administration and mesolimbic dopamine and acetylcholine receptor gene expression. Addict Biol 2011, 17:95-107.
35. Jerlhag E., Egecioglu E., Dickson S.L., Engel J.A. Ghrelin receptor antagonism attenuates cocaine- and amphetamine-induced locomotor stimulation, accumbal dopamine release, and conditioned place preference. Psychopharmacology (Berl) 2010, 211(4):415-422.
36. Schwartz G.J., Berkow G., McHugh P.R., Moran T.H. Gastric branch vagotomy blocks nutrient and cholecystokinin-induced suppression of gastric emptying. Am J Physiol 1993, 264(3 Pt 2):R630-R637.
37. Beglinger C., Degen L. Fat in the intestine as a regulator of appetite-role of CCK. Physiol Behav 2004, 83:617-621.
38. De Jonghe B.C., Hajnal A., Covasa M. Decreased gastric mechanodetection, but preserved gastric emptying, in CCK-1 receptor-deficient OLETF rats. Am J Physiol Gastrointest Liver Physiol 2006, 291(4):G640-G649.
39. Aviello G., Matias I., Capasso R., Petrosino S., Borrelli F., Orlando P., et al. Inhibitory effect of the anorexic compound oleoylethanolamide on gastric emptying in control and overweight mice. J Mol Med (Berl) 2008, 86(4):413-422.
40. Feifel D., Shilling P.D., Kuczenski R., Segal D.S. Altered extracellular dopamine concentration in the brains of cholecystokinin-A receptor deficient rats. Neurosci Lett 2003, 348:147-150.
41. Schwartz G.J. Gut fat sensing in the negative feedback control of energy balance - Recent advances. Physiol Behav 2011, 104:621-623.
42. Sclafani A., Ackroff K., Schwartz G.J. Selective effects of vagal deafferentation and celiac- superior mesenteric ganglionectomy on the reinforcing and satiating action of intestinal nutrients. Physiol Behav 2003, 78(2):285-294.
43. Ackroff K., Yiin Y.M., Sclafani A. Post-oral infusion sites that support glucose-conditioned flavor preferences in rats. Physiol Behav 2010, 99:402-411.
44. Margolskee R.F., Dyer J., Kokrashvili Z., Salmon K.S., Ilegems E., Daly K., et al. T1R3 and gustducin in gut sense sugars to regulate expression of Na+-glucose cotransporter 1. Proc Natl Acad Sci U S A 2007, 104:15075-15080.
45. Hass N., Schwarzenbacher K., Breer H. T1R3 is expressed in brush cells and ghrelin- producing cells of murine stomach. Cell Tissue Res 2010, 339(3):493-504.
46. Janssen S., Laermans J., Verhulst P.J., Thijs T., Tack J., Depoortere I. Bitter taste receptors and alpha-gustducin regulate the secretion of ghrelin with functional effects on food intake and gastric emptying. Proc Natl Acad Sci U S A 2011, 108(5):2094-2099.
47. Nakagawa Y., Nagasawa M., Yamada S., Hara A., Mogami H., Nikolaev V.O., et al. Sweet taste receptor expressed in pancreatic beta-cells activates the calcium and cyclic AMP signaling systems and stimulates insulin secretion. PLoS One 2009, 4(4):e5106.
48. Ren X., Zhou L., Terwilliger R., Newton S.S., de Araujo I.E. Sweet taste signaling functions as a hypothalamic glucose sensor. Front Integr Neurosci 2009, 3:12.
49. Swartz T.D., Duca F.A., de Wouters T., Sakar Y., Covasa M. Up-regulation of intestinal type 1 taste receptor 3 and sodium glucose luminal transporter-1 expression and increased sucrose intake in mice lacking gut microbiota. Br J Nutr 2012, 107(5):621-630.
50. Zhang Y., Hoon M.A., Chandrashekar J., Mueller K.L., Cook B.W.D., Zucker C.S., et al. Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 2003, 112:293-301.
51. Zhao G.Q., Zhang Y., Hoon M.A., Chandrashekar J., Erienbach I., Ryba N.J.P., et al. The receptors for mammalian sweet and umami taste. Cell 2003, 115:255-266.
52. Sclafani A., Glass D.S., Margolskee R.F., Glendinning J.I. Gut T1R3 sweet taste receptors do not mediate sucrose-conditioned flavor preferences in mice. Am J Physiol Regul Integr Comp Physiol 2010, 299(6):R1643-R1650.
53. de Araujo I.E., Ren X., Ferreira J.G. Metabolic sensing in brain dopamine systems. Results Probl Cell Differ 2010, 52:69-86.
54. McCrimmon R. The mechanisms that underlie glucose sensing during hypoglycaemia in diabetes. Diabet Med 2008, 5:513-522.
55. Figlewicz D.P. Adiposity signals and food reward: expanding the CNS roles of insulin and leptin. Am J Physiol Regul Integr Comp Physiol 2003, 284(4):R882-R892.
56. Pardini A.W., Nguyen H.T., Figlewicz D.P., Baskin D.G., Williams D.L., Kim F., et al. Distribution of insulin receptor substrate-2 in brain areas involved in energy homeostasis. Brain Res 2006, 1112(1):169-178.
57. Hommel J.D., Trinko R., Sears R.M., Georgescu D., Liu Z.W., Gao X.B., et al. Leptin receptor signaling in midbrain dopamine neurons regulates feeding. Neuron 2006, 51(6):801-810.
58. Ackroff K., Sclafani A., Axen K.V. Diabetic rats prefer glucose-paired flavors over fructose- paired flavors. Appetite 1997, 28:73-83.
59. Liu J., Perez S.M., Zhang W., Lodge D.J., Lu X.Y. Selective deletion of the leptin receptor in dopamine neurons produces anxiogenic-like behavior and increases dopaminergic activity in amygdala. Mol Psychiatry 2011, 16(10):1024-1038.
60. Horvath T.L., Andrews Z.B., Diano S. Fuel utilization by hypothalamic neurons: roles for ROS. Trends Endocrinol Metab 2009, 20(2):78-87.
61. Li A.J., Wang Q., Ritter S. Participation of hindbrain AMP-activated protein kinase in glucoprivic feeding. Diabetes 2011, 60(2):436-442.
62. Levin B.E. Glucose-regulated dopamine release from substantia nigra neurons. Brain Res 2000, 874:158-164.
63. Hudson B., Ritter S. Hindbrain catecholamine neurons mediate consummatory responses to glucoprivation. Physiol Behav 2004, 82(2-3):241-250.
64. Ritter R.C., Slusser P.G., Stone S. Glucoreceptors controlling feeding and blood glucose: location in the hindbrain. Science 1981, 213(4506):451-452.
65. Watts A.G., Donovan C.M. Sweet talk in the brain: Glucosensing, neural networks, and hypoglycemic counterregulation. Front Neuroendrocrinology 2009, 31:32-43.
66. Ritter S., Dinh T.T., Li A.J. Hindbrain catecholamine neurons control multiple glucoregulatory responses. Physiol Behav 2006, 89(4):490-500.
67. Blouet C., Schwartz G.J. Hypothalamic nutrient sensing in the control of energy homeostasis. Behav Brain Res 2010, 209(1):1-12.
68. 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.
69. Lam T.K. Neuronal regulation of homeostasis by nutrient sensing. Nat Med 2010, 16(4):392-395.
70. Wang P.Y., Caspi L., Lam C.K., Chari M., Li X., Light P.E., et al. Upper intestinal lipids trigger a gut-brain-liver axis to regulate glucose production. Nature 2008, 452(7190):1012-1016.