Insulin receptor activation in the nucleus accumbens reflects nutritive value of a recently ingested meal

Physiology and Behavior

Volumn 159, Issue , 2016, Pages 52-63

  Woods, C A ^a   Guttman, Z R ^a   Huang, D ^b   Kolaric, R A ^b   Rabinowitsch, A I ^b   Jones, K T ^b   Cabeza de Vaca, S ^b   Sclafani, A ^c   Carr, K D ^a,b  

^a Center for Neural Science   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Flavor preference; Glucose; Insulin; Insulin receptor; Nucleus accumbens; Nutrient

Indexed keywords

GLUCOSE; INSULIN; INSULIN RECEPTOR; WATER;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET INDUCED OBESITY; DIET RESTRICTION; FLAVOR; FOOD PREFERENCE; GENE ACTIVATION; GLUCOSE INTAKE; LEARNING; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RAT; ANIMAL; DRINKING; EATING; METABOLISM; NUTRITIONAL VALUE; PHYSIOLOGY; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; DRINKING; EATING; GLUCOSE; MALE; NUCLEUS ACCUMBENS; NUTRITIVE VALUE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, INSULIN;

EID: 84961206034     PISSN: 00319384     EISSN: 1873507X     Source Type: Journal    
DOI: 10.1016/j.physbeh.2016.03.013     Document Type: Article

References (61)

1. Abizaid A., Liu Z.-W., Andrews Z.B., Shanabrough M., Borok E., Elsworth J.D., Tschöp M.H. Ghrelin modulates the activity and synaptic input organization of midbrain dopamine neurons while promoting appetite. J. Clin. Investig. 2006, 116(12):3229.
2. Ackroff K., Sclafani A. Flavor change and food deprivation are not critical for post-oral glucose appetition in mice. Physiol. Behav. 2015, 140:23-31.
3. Ackroff K., Sclafani A., Axen K.V. Diabetic rats prefer glucose-paired flavors over fructose-paired flavors. Appetite 1997, 28(1):73-83. 10.1006/appe.1996.0058.
4. Ackroff K., Yiin Y.M., Sclafani A. Post-oral infusion sites that support glucose-conditioned flavor preferences in rats. Physiol. Behav. 2010, 99(3):402-411. 10.1016/j.physbeh.2009.12.012.
5. Anthony K., Reed L.J., Dunn J.T., Bingham E., Hopkins D., Marsden P.K., Amiel S.A. Attenuation of insulin-evoked responses in brain networks controlling appetite and reward in insulin resistance: the cerebral basis for impaired control of food intake in metabolic syndrome?. Diabetes 2006, 55(11):2986-2992. 10.2337/db06-0376.
6. Banke T., Bowie D., Lee H.-K., Huganir R., Schousboe A., Traynelis S. Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase. J. Neurosci. 2000, 20(1):89-102.
7. Banks W.A., Jaspan J.B., Huang W., Kastin A.J. Transport of insulin across the blood-brain barrier: saturability at euglycemic doses of insulin. Peptides 1997, 18(9):1423-1429. 10.1016/S0196-9781(97)00231-3.
8. Banks W.A., Jaspan J.B., Kastin A.J. Effect of diabetes mellitus on the permeability of the blood-brain barrier to insulin. Peptides 1997, 18(10):1577-1584.
9. Banks W.A., Kastin A.J. Differential permeability of the blood-brain barrier to two pancreatic peptides: insulin and amylin. Peptides 1998, 19(5):883-889. 10.1016/S0196-9781(98)00018-7.
10. Banks W.A., Owen J.B., E rickson M.A. Insulin in the brain: there and back again. Pharmacol. Ther. 2012, 136(1):82-93. 10.1016/j.pharmthera.2012.07.006.
11. Baskin D.G., Stein L.J., Ikeda H., Woods S.C., Figlewicz D.P., Porte D., Dorsa D.M. Genetically obese Zucker rats have abnormally low brain insulin content. Life Sci. 1985, 36(7):627-633.
12. Bernal S.Y., Dostova I., Kest A., Abayev Y., Kandova E., Touzani K., Bodnar R.J. Role of dopamine D1 and D2 receptors in the nucleus accumbens shell on the acquisition and expression of fructose-conditioned flavor-flavor preferences in rats. Behav. Brain Res. 2008, 190(1):59-66. 10.1016/j.bbr.2008.02.003.
13. Capaldi E.D., Owens J., Palmer K.A. Effects of food deprivation on learning and expression of flavor preferences conditioned by saccharin or sucrose. Anim. Learn. Behav. 1994, 22(2):173-180.
14. Caravaggio F., Borlido C., Hahn M., Feng Z., Fervaha G., Gerretsen P., Graff-Guerrero A. Reduced insulin sensitivity is related to less endogenous dopamine at D2/3 receptors in the ventral striatum of healthy nonobese humans. Int. J. Neuropsychopharmacol. 2015, 18(7):pyv014. 10.1093/ijnp/pyv014.
15. Carr K.D. Food scarcity, neuroadaptations, and the pathogenic potential of dieting in an unnatural ecology: binge eating and drug abuse. Physiol. Behav. 2011, 104(1):162-167. 10.1016/j.physbeh.2011.04.023.
16. Carr K.D., Chau L.S., Cabeza de Vaca S., Gustafson K., Stouffer M., Tukey D.S., Ziff E.B. AMPA receptor subunit GluR1 downstream of D-1 dopamine receptor stimulation in nucleus accumbens shell mediates increased drug reward magnitude in food-restricted rats. Neuroscience 2010, 165(4):1074-1086. 10.1016/j.neuroscience.2009.11.015.
17. Davis J.F., Choi D.L., Schurdak J.D., Fitzgerald M.F., Clegg D.J., Lipton J.W., Benoit S.C. Leptin regulates energy balance and motivation through action at distinct neural circuits. Biol. Psychiatry 2011, 69(7):668-674.
18. Davis J.F., Tracy A.L., Schurdak J.D., Tschop M.H., Lipton J.W., Clegg D.J., Benoit S.C. Exposure to elevated levels of dietary fat attenuates psychostimulant reward and mesolimbic dopamine turnover in the rat. Behav. Neurosci. 2008, 122(6):1257-1263. 10.1037/a0013111.
19. de Araujo I.E., Ferreira J.G., Tellez L.A., Ren X., Yeckel C.W. The gut-brain dopamine axis: a regulatory system for caloric intake. Physiol. Behav. 2012, 106(3):394-399. 10.1016/j.physbeh.2012.02.026.
20. 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(14):4812-4820.
21. Duca F.A., Swartz T.D., Covasa M. Effect of diet on preference and intake of sucrose in obese prone and resistant rats. PLoS One 2014, 9(10). 10.1371/journal.pone.0111232.
22. Dunn J.P., Kessler R.M., Feurer I.D., Volkow N.D., Patterson B.W., Ansari M.S., Abumrad N.N. Relationship of dopamine type 2 receptor binding potential with fasting neuroendocrine hormones and insulin sensitivity in human obesity. Diabetes Care 2012, 35(5):1105-1111.
23. Fedorchak P.M., Bolles R.C. Hunger enhances the expression of calorie- but not taste-mediated conditioned flavor preferences. J Exp Psychol Anim Behav Process 1987, 13(1):73-79.
24. Fernandes M.F., Sharma S., Hryhorczuk C., Auguste S., Fulton S. Nutritional controls of food reward. Canadian Journal of Diabetes 2013, 37(4):260-268.
25. Fernstrom J.D., Munger S.D., Sclafani A., de Araujo I.E., Roberts A., Molinary S. Mechanisms for sweetness. J. Nutr. 2012, 142(6):1134S-1141S.
26. Figlewicz D.P., Bennett J., Evans S.B., Kaiyala K., Sipols A.J., Benoit S.C. Intraventricular insulin and leptin reverse place preference conditioned with high-fat diet in rats. Behav. Neurosci. 2004, 118(3):479-487. 10.1037/0735-7044.118.3.479.
27. Figlewicz D.P., Bennett J.L., Aliakbari S., Zavosh A., Sipols A.J. Insulin acts at different CNS sites to decrease acute sucrose intake and sucrose self-administration in rats. Am. J. Phys. Regul. Integr. Comp. Phys. 2008, 295(2):R388-R394. 10.1152/ajpregu.90334.2008.
28. 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. 10.1016/j.neuroscience.2009.02.007.
29. Hajnal A., Acharya N.K., Grigson P.S., Covasa M., Twining R.C. Obese OLETF rats exhibit increased operant performance for palatable sucrose solutions and differential sensitivity to D2 receptor antagonism. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 293(5):R1846-R1854.
30. Jones D.M., Arters J., Berger-Sweeney J. Carbon dioxide-induced anesthesia has no effect on brain biogenic amine concentrations in mice. Comparative Medicine 1999, 49(3):316-318.
31. Kaiyala K.J., Prigeon R.L., Kahn S.E., Woods S.C., Schwartz M.W. Obesity induced by a high-fat diet is associated with reduced brain insulin transport in dogs. Diabetes 2000, 49(9):1525-1533.
32. Kenny P.J. Reward mechanisms in obesity: new insights and future directions. Neuron 2011, 69(4):664-679.
33. Kessels H.W., Malinow R. Synaptic AMPA receptor plasticity and behavior. Neuron 2009, 61(3):340-350.
34. Krügel U., Schraft T., Kittner H., Kiess W., Illes P. Basal and feeding-evoked dopamine release in the rat nucleus accumbens is depressed by leptin. Eur. J. Pharmacol. 2003, 482(1):185-187.
35. 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.
36. McCaleb M., Myers R. Striatal dopamine release is altered by glucose and insulin during push-pull perfusion of the rat's caudate nucleus. Brain Res. Bull. 1979, 4(5):651-656.
37. McNay E.C., Ong C.T., McCrimmon R.J., Cresswell J., Bogan J.S., Sherwin R.S. Hippocampal memory processes are modulated by insulin and high-fat-induced insulin resistance. Neurobiol. Learn. Mem. 2010, 93(4):546-553.
38. Narayanaswami V., Thompson A., Cassis L., Bardo M., Dwoskin L. Diet-induced obesity: dopamine transporter function, impulsivity and motivation. Int. J. Obes. 2013, 37(8):1095-1103.
39. Owens W.A., Sevak R.J., Galici R., Chang X., Javors M.A., Galli A., Daws L.C. Deficits in dopamine clearance and locomotion in hypoinsulinemic rats unmask novel modulation of dopamine transporters by amphetamine. J. Neurochem. 2005, 94(5):1402-1410. 10.1111/j.1471-4159.2005.03289.x.
40. Paranjape S.A., Chan O., Zhu W., Horblitt A.M., McNay E.C., Cresswell J.A., Sherwin R.S. Influence of insulin in the ventromedial hypothalamus on pancreatic glucagon secretion in vivo. Diabetes 2010, 59(6):1521-1527. 10.2337/db10-0014.
41. Richard J.E., Anderberg R.H., Göteson A., Gribble F.M., Reimann F., Skibicka K.P. Activation of the GLP-1 Receptors in the Nucleus of the Solitary Tract Reduces Food Reward Behavior and Targets the Mesolimbic System 2015.
42. Robinson M.J., Burghardt P.R., Patterson C.M., Nobile C.W., Akil H., Watson S.J., Ferrario C.R. Individual differences in cue-induced motivation and striatal systems in rats susceptible to diet-induced obesity. Neuropsychopharmacology 2015, 40(9):2113-2123. 10.1038/npp.2015.71.
43. Roche K.W., O'Brien R.J., Mammen A.L., Bernhardt J., Huganir R.L. Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron 1996, 16(6):1179-1188.
44. Schulingkamp R.J., Pagano T.C., Hung D., Raffa R.B. Insulin receptors and insulin action in the brain: review and clinical implications. Neurosci. Biobehav. Rev. 2000, 24(8):855-872. 10.1016/S0149-7634(00)00040-3.
45. 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. Phys. Regul. Integr. Comp. Phys. 2011, 301(5):R1267-R1280. 10.1152/ajpregu.00314.2011.
46. Snyder G.L., Allen P.B., Fienberg A.A., Valle C.G., Huganir R.L., Nairn A.C., Greengard P. Regulation of phosphorylation of the GluR1 AMPA receptor in the neostriatum by dopamine and psychostimulants in vivo. J. Neurosci. 2000, 20(12):4480-4488.
47. Stice E., Figlewicz D.P., Gosnell B.A., Levine A.S., Pratt W.E. The contribution of brain reward circuits to the obesity epidemic. Neurosci. Biobehav. Rev. 2013, 37(9 Pt A):2047-2058. 10.1016/j.neubiorev.2012.12.001.
48. Stice E., Yokum S., Blum K., Bohon C. Weight gain is associated with reduced striatal response to palatable food. J. Neurosci. 2010, 30(39):13105-13109. 10.1523/jneurosci.2105-10.2010.
49. Stouffer, M. A., Woods, C. A., Patel, J. C., Lee, C. R., Witkovsky, P., Bao, L., . . . Rice, M. E. (2015). Insulin enhances striatal dopamine release by activating cholinergic interneurons and thereby signals reward. Nat Commun, 6. doi:10.1038/ncomms9543.
50. Strubbe J.H., Mein C.G. Increased feeding in response to bilateral injection of insulin antibodies in the VMH. Physiol. Behav. 1977, 19(2):309-313.
51. Tellez L.A., Ren X., Han W., Medina S., Ferreira J.G., Yeckel C.W., de Araujo I.E. Glucose utilization rates regulate intake levels of artificial sweeteners. J. Physiol. 2013, 591(Pt 22):5727-5744. 10.1113/jphysiol.2013.263103.
52. Touzani K., Bodnar R., Sclafani A. Activation of dopamine D1-like receptors in nucleus accumbens is critical for the acquisition, but not the expression, of nutrient-conditioned flavor preferences in rats. Eur. J. Neurosci. 2008, 27(6):1525-1533. 10.1111/j.1460-9568.2008.06127.x.
53. Urayama A., Banks W.A. Starvation and triglycerides reverse the obesity-induced impairment of insulin transport at the blood-brain barrier. Endocrinology 2008, 149(7):3592-3597. 10.1210/en.2008-0008.
54. Volkow N.D., Wang G.J., Maynard L., Jayne M., Fowler J.S., Zhu W., Pappas N. Brain dopamine is associated with eating behaviors in humans. Int J Eat Disord 2003, 33(2):136-142. 10.1002/eat.10118.
55. Wald H.S., Myers K.P. Enhanced flavor-nutrient conditioning in obese rats on a high-fat, high-carbohydrate choice diet. Physiol. Behav. 2015, 151:102-110. 10.1016/j.physbeh.2015.07.002.
56. Wang G.J., Tomasi D., Convit A., Logan J., Wong C.T., Shumay E., Volkow N.D. BMI modulates calorie-dependent dopamine changes in accumbens from glucose intake. PLoS One 2014, 9(7). 10.1371/journal.pone.0101585.
57. Warwick Z.S., Weingarten H.P. Dissociation of palatability and calorie effects in learned flavor preferences. Physiol. Behav. 1994, 55(3):501-504.
58. Williams J.M., Owens W.A., Turner G.H., Saunders C., Dipace C., Blakely R.D., Galli A. Hypoinsulinemia regulates amphetamine-induced reverse transport of dopamine. PLoS Biol. 2007, 5(10). 10.1371/journal.pbio.0050274.
59. Yiin Y.M., Ackroff K., Sclafani A. Flavor preferences conditioned by intragastric nutrient infusions in food restricted and free-feeding rats. Physiol. Behav. 2005, 84(2):217-231. 10.1016/j.physbeh.2004.11.008.
60. Yiin Y.M., Ackroff K., Sclafani A. Food deprivation enhances the expression but not acquisition of flavor acceptance conditioning in rats. Appetite 2005, 45(2):152-160. 10.1016/j.appet.2005.04.002.
61. Zhen J., Reith M.E., Carr K.D. Chronic food restriction and dopamine transporter function in rat striatum. Brain Res. 2006, 1082(1):98-101. 10.1016/j.brainres.2006.01.094.