Neural integration of satiation and food reward: Role of GLP-1 and orexin pathways

Physiology and Behavior

Volumn 136, Issue , 2014, Pages 194-199

  Williams, Diana L ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Food reward; Glucagon like peptide 1; Orexin; Satiation

Indexed keywords

GLUCAGON LIKE PEPTIDE 1; OREXIN; NEUROPEPTIDE; SIGNAL PEPTIDE;

AREA POSTREMA; ASSOCIATION; ENERGY; FOOD; FOOD INTAKE; HUMAN; LATERAL HYPOTHALAMUS; MEAL; MOTIVATION; NERVE CELL NETWORK; NERVE TRACT; NUCLEUS ACCUMBENS; PALATABILITY; REVIEW; REWARD; RHOMBENCEPHALON; SATIETY; SOLITARY TRACT NUCLEUS; VENTRAL TEGMENTUM; ANIMAL; FOOD PREFERENCE; METABOLISM; PHYSIOLOGY; PSYCHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; FOOD PREFERENCES; GLUCAGON-LIKE PEPTIDE 1; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; NEUROPEPTIDES; OREXINS; REWARD; SATIATION; SIGNAL TRANSDUCTION;

EID: 84917686694     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2014.03.013     Document Type: Review

References (74)

1. Schwartz M.W. Central nervous system regulation of food intake. Obesity (Silver Spring) 2006, 14(Suppl. 1):1S-8S.
2. Berridge K.C., Ho C.Y., Richard J.M., DiFeliceantonio A.G. The tempted brain eats: pleasure and desire circuits in obesity and eating disorders. Brain Res 2010, 1350:43-64.
3. Berthoud H.R. Homeostatic and non-homeostatic pathways involved in the control of food intake and energy balance. Obesity (Silver Spring) 2006, 14(Suppl. 5):197S-200S.
4. Guyenet S.J., Schwartz M.W. Clinical review: regulation of food intake, energy balance, and body fat mass: implications for the pathogenesis and treatment of obesity. J Clin Endocrinol Metab 2012, 97:745-755.
5. Berthoud H.R., Lenard N.R., Shin A.C. Food reward, hyperphagia, and obesity. Am J Physiol Regul Integr Comp Physiol 2011, 300:R1266-R1277.
6. Lutter M., Nestler E.J. Homeostatic and hedonic signals interact in the regulation of food intake. J Nutr 2009, 139:629-632.
7. Morton G.J., Cummings D.E., Baskin D.G., Barsh G.S., Schwartz M.W. Central nervous system control of food intake and body weight. Nature 2006, 443:289-295.
8. Gautron L., Elmquist J.K. Sixteen years and counting: an update on leptin in energy balance. J Clin Invest 2011, 121:2087-2093.
9. Moran T.H. Gut peptides in the control of food intake. Int J Obes (Lond) 2009, 33(Suppl. 1):S7-S10.
10. Cummings D.E., Overduin J. Gastrointestinal regulation of food intake. J Clin Invest 2007, 117:13-23.
11. Woods S.C., D'Alessio D.A. Central control of body weight and appetite. J Clin Endocrinol Metab 2008, 93:S37-S50.
12. Woods S.C. Gastrointestinal satiety signals I. An overview of gastrointestinal signals that influence food intake. Am J Physiol Gastrointest Liver Physiol 2004, 286:G7-G13.
13. Grill H.J., Hayes M.R. Hindbrain neurons as an essential hub in the neuroanatomically distributed control of energy balance. Cell Metab 2012, 16:296-309.
14. Moran T.H., Ladenheim E.E. Adiposity signaling and meal size control. Physiol Behav 2011, 103:21-24.
15. Narayanan N.S., Guarnieri D.J., DiLeone R.J. Metabolic hormones, dopamine circuits, and feeding. Front Neuroendocrinol 2010, 31:104-112.
16. Zhang M., Kelley A.E. Enhanced intake of high-fat food following striatal mu-opioid stimulation: microinjection mapping and fos expression. Neuroscience 2000, 99:267-277.
17. 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.
18. Kelley A.E. Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev 2004, 27:765-776.
19. Figlewicz D.P., Sipols A.J. Energy regulatory signals and food reward. Pharmacol Biochem Behav 2010, 97:15-24.
20. Davis J.F., Choi D.L., Schurdak J.D., Fitzgerald M.F., Clegg D.J., Lipton J.W., et al. Leptin regulates energy balance and motivation through action at distinct neural circuits. Biol Psychiatry 2011, 69:668-674.
21. Berthoud H.R., Munzberg H. The lateral hypothalamus as integrator of metabolic and environmental needs: from electrical self-stimulation to opto-genetics. Physiol Behav 2011, 104:29-39.
22. Berthoud H.R. Metabolic and hedonic drives in the neural control of appetite: who is the boss?. Curr Opin Neurobiol 2011, 21:888-896.
23. Larsen P.J., Tang-Christensen M., Holst J.J., Orskov C. Distribution of glucagon-like peptide-1 and other preproglucagon-derived peptides in the rat hypothalamus and brainstem. Neuroscience 1997, 77:257-270.
24. Turton M.D., O'Shea D., Gunn I., Beak S.A., Edwards C.M., Meeran K., et al. A role for glucagon-like peptide-1 in the central regulation of feeding. Nature 1996, 379:69-72.
25. Williams D.L., Baskin D.G., Schwartz M.W. Evidence that intestinal GLP-1 plays a physiological role in satiety. Endocrinology 2009, 150:1680-1687.
26. Kastin A.J., Akerstrom V., Pan W. Interactions of glucagon-like peptide-1 (GLP-1) with the blood-brain barrier. J Mol Neurosci 2002, 18:7-14.
27. Holst J.J., Deacon C.F. Glucagon-like peptide-1 mediates the therapeutic actions of DPP-IV inhibitors. Diabetologia 2005, 48:612-615.
28. Kanoski S.E., Fortin S.M., Arnold M., Grill H.J., Hayes M.R. Peripheral and central GLP-1 receptor populations mediate the anorectic effects of peripherally administered GLP-1 receptor agonists, liraglutide and exendin-4. Endocrinology 2011, 152:3103-3112.
29. Vrang N., Phifer C.B., Corkern M.M., Berthoud H.R. Gastric distension induces c-fos in medullary GLP-1/2-containing neurons. Am J Physiol Regul Integr Comp Physiol 2003, 285:R470-R478.
30. Gaykema R.P., Daniels T.E., Shapiro N.J., Thacker G.C., Park S.M., Goehler L.E. Immune challenge and satiety-related activation of both distinct and overlapping neuronal populations in the brainstem indicate parallel pathways for viscerosensory signaling. Brain Res 2009, 1294:61-79.
31. Hisadome K., Reimann F., Gribble F.M., Trapp S. Leptin directly depolarizes preproglucagon neurons in the nucleus tractus solitarius: electrical properties of glucagon-like peptide 1 neurons. Diabetes 2010, 59:1890-1898.
32. Meeran K., O'Shea D., Edwards C.M., Turton M.D., Heath M.M., Gunn I., et al. Repeated intracerebroventricular administration of glucagon-like peptide-1-(7-36) amide or exendin-(9-39) alters body weight in the rat. Endocrinology 1999, 140:244-250.
33. Barrera J.G., Jones K.R., Herman J.P., D'Alessio D.A., Woods S.C., Seeley R.J. Hyperphagia and increased fat accumulation in two models of chronic CNS glucagon-like peptide-1 loss of function. J Neurosci 2011, 31:3904-3913.
34. Merchenthaler I., Lane M., Shughrue P. Distribution of pre-pro-glucagon and glucagon-like peptide-1 receptor messenger RNAs in the rat central nervous system. J Comp Neurol 1999, 403:261-280.
35. Rinaman L. Ascending projections from the caudal visceral nucleus of the solitary tract to brain regions involved in food intake and energy expenditure. Brain Res 2010, 1350:18-34.
36. Dossat A.M., Lilly N., Kay K., Williams D.L. Glucagon-like peptide 1 receptors in nucleus accumbens affect food intake. J Neurosci 2011, 31:14453-14457.
37. Alhadeff A.L., Rupprecht L.E., Hayes M.R. GLP-1 neurons in the nucleus of the solitary tract project directly to the ventral tegmental area and nucleus accumbens to control for food intake. Endocrinology 2012, 153:647-658.
38. McMahon L.R., Wellman P.J. PVN infusion of GLP-1-(7-36) amide suppresses feeding but does not induce aversion or alter locomotion in rats. Am J Physiol 1998, 274:R23-R29.
39. Sandoval D.A., Bagnol D., Woods S.C., D'Alessio D.A., Seeley R.J. Arcuate glucagon-like peptide 1 receptors regulate glucose homeostasis but not food intake. Diabetes 2008, 57:2046-2054.
40. Schick R.R., Zimmermann J.P., vorm Walde T., Schusdziarra V. Glucagon-like peptide 1-(7-36) amide acts at lateral and medial hypothalamic sites to suppress feeding in rats. Am J Physiol Regul Integr Comp Physiol 2003, 284:R1427-R1435.
41. Skibicka K.P. The central GLP-1: implications for food and drug reward. Front Neurosci 2013, 7:181.
42. Dossat A.M., Diaz R., Gallo L., Panagos A., Kay K., Williams D.L. Nucleus accumbens GLP-1 receptors influence meal size and palatability. Am J Physiol Endocrinol Metab 2013, 304:E1314-E1320.
43. Rinaman L. A functional role for central glucagon-like peptide-1 receptors in lithium chloride-induced anorexia. Am J Physiol 1999, 277:R1537-R1540.
44. Kinzig K.P., D'Alessio D.A., Seeley R.J. The diverse roles of specific GLP-1 receptors in the control of food intake and the response to visceral illness. J Neurosci 2002, 22:10470-10476.
45. Grill H.J., Carmody J.S., Amanda Sadacca L., Williams D.L., Kaplan J.M. Attenuation of lipopolysaccharide anorexia by antagonism of caudal brain stem but not forebrain GLP-1-R. Am J Physiol Regul Integr Comp Physiol 2004, 287:R1190-R1193.
46. Dickson S.L., Shirazi R.H., Hansson C., Bergquist F., Nissbrandt H., Skibicka K.P. The glucagon-like peptide 1 (GLP-1) analogue, exendin-4, decreases the rewarding value of food: a new role for mesolimbic GLP-1 receptors. J Neurosci 2012, 32:4812-4820.
47. 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.
48. 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.
49. Mietlicki-Baase E.G., Ortinski P.I., Rupprecht L.E., Olivos D.R., Alhadeff A.L., Pierce R.C., et al. The food intake-suppressive effects of glucagon-like peptide-1 receptor signaling in the ventral tegmental area are mediated by AMPA/kainate receptors. Am J Physiol Endocrinol Metab 2013, 305:E1367-E1374.
50. Sakurai T., Amemiya A., Ishii M., Matsuzaki I., Chemelli R.M., Tanaka H., et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 1998, 92. [1 page following 696].
51. Ammoun S., Holmqvist T., Shariatmadari R., Oonk H.B., Detheux M., Parmentier M., et al. Distinct recognition of OX1 and OX2 receptors by orexin peptides. J Pharmacol Exp Ther 2003, 305:507-514.
52. Haynes A.C., Jackson B., Overend P., Buckingham R.E., Wilson S., Tadayyon M., et al. Effects of single and chronic intracerebroventricular administration of the orexins on feeding in the rat. Peptides 1999, 20:1099-1105.
53. Ishii Y., Blundell J.E., Halford J.C., Upton N., Porter R., Johns A., et al. Differential effects of the selective orexin-1 receptor antagonist SB-334867 and lithium chloride on the behavioural satiety sequence in rats. Physiol Behav 2004, 81:129-140.
54. Peyron C., Tighe D.K., van den Pol A.N., de Lecea L., Heller H.C., Sutcliffe J.G., et al. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 1998, 18:9996-10015.
55. Hervieu G.J., Cluderay J.E., Harrison D.C., Roberts J.C., Leslie R.A. Gene expression and protein distribution of the orexin-1 receptor in the rat brain and spinal cord. Neuroscience 2001, 103:777-797.
56. Marcus J.N., Aschkenasi C.J., Lee C.E., Chemelli R.M., Saper C.B., Yanagisawa M., et al. Differential expression of orexin receptors 1 and 2 in the rat brain. J Comp Neurol 2001, 435:6-25.
57. Choi D.L., Davis J.F., Fitzgerald M.E., Benoit S.C. The role of orexin-A in food motivation, reward-based feeding behavior and food-induced neuronal activation in rats. Neuroscience 2010, 167:11-20.
58. Sharf R., Sarhan M., Brayton C.E., Guarnieri D.J., Taylor J.R., DiLeone R.J. Orexin signaling via the orexin 1 receptor mediates operant responding for food reinforcement. Biol Psychiatry 2010, 67:753-760.
59. Cason A.M., Aston-Jones G. Role of orexin/hypocretin in conditioned sucrose-seeking in rats. Psychopharmacology (Berl) 2013, 226:155-165.
60. 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.
61. Choi D.L., Davis J.F., Magrisso I.J., Fitzgerald M.E., Lipton J.W., Benoit S.C. Orexin signaling in the paraventricular thalamic nucleus modulates mesolimbic dopamine and hedonic feeding in the rat. Neuroscience 2012, 210:243-248.
62. Zheng H., Patterson L.M., Berthoud H.R. Orexin-A projections to the caudal medulla and orexin-induced c-fos expression, food intake, and autonomic function. J Comp Neurol 2005, 485:127-142.
63. Baird J.P., Choe A., Loveland J.L., Beck J., Mahoney C.E., Lord J.S., et al. Orexin-A hyperphagia: hindbrain participation in consummatory feeding responses. Endocrinology 2009, 150:1202-1216.
64. Parise E.M., Lilly N., Kay K., Dossat A.M., Seth R., Overton J.M., et al. Evidence for the role of hindbrain orexin-1 receptors in the control of meal size. Am J Physiol Regul Integr Comp Physiol 2011, 301:R1692-R1699.
65. Kay K., Parise E.M., Lilly N., Williams D.L. Hindbrain orexin 1 receptors influence palatable food intake, operant responding for food, and food-conditioned place preference in rats. Psychopharmacology (Berl) 2014, 231:419-427.
66. Kanoski S.E., Alhadeff A.L., Fortin S.M., Gilbert J.R., Grill H.J. Leptin signaling in the medial nucleus tractus solitarius reduces food seeking and willingness to work for food. Neuropsychopharmacology 2014, 39:605-613.
67. Huo L., Maeng L., Bjorbaek C., Grill H.J. Leptin and the control of food intake: neurons in the nucleus of the solitary tract are activated by both gastric distension and leptin. Endocrinology 2007, 148:2189-2197.
68. Huo L., Gamber K.M., Grill H.J., Bjorbaek C. Divergent leptin signaling in proglucagon neurons of the nucleus of the solitary tract in mice and rats. Endocrinology 2008, 149:492-497.
69. Olszewski P.K., Klockars A., Schioth H.B., Levine A.S. Oxytocin as feeding inhibitor: maintaining homeostasis in consummatory behavior. Pharmacol Biochem Behav 2010, 97:47-54.
70. Vaccari C., Lolait S.J., Ostrowski N.L. Comparative distribution of vasopressin V1b and oxytocin receptor messenger ribonucleic acids in brain. Endocrinology 1998, 139:5015-5033.
71. Sofroniew M.V. Morphology of vasopressin and oxytocin neurones and their central and vascular projections. Prog Brain Res 1983, 60:101-114.
72. Mullis K., Kay K., Williams D.L. Oxytocin action in the ventral tegmental area affects sucrose intake. Brain Res 2013, 1513:85-91.
73. Nowend K.L., Arizzi M., Carlson B.B., Salamone J.D. D1 or D2 antagonism in nucleus accumbens core or dorsomedial shell suppresses lever pressing for food but leads to compensatory increases in chow consumption. Pharmacol Biochem Behav 2001, 69:373-382.
74. Skibicka K.P., Shirazi R.H., Rabasa-Papio C., Alvarez-Crespo M., Neuber C., Vogel H., et al. Divergent circuitry underlying food reward and intake effects of ghrelin: dopaminergic VTA-accumbens projection mediates ghrelin's effect on food reward but not food intake. Neuropharmacology 2013, 73:274-283.