Effects of insulin and leptin in the ventral tegmental area and arcuate hypothalamic nucleus on food intake and brain reward function in female rats

Behavioural Brain Research

Volumn 219, Issue 2, 2011, Pages 254-264

  Bruijnzeel, Adrie W ^a   Corrie, Lu W ^a   Rogers, Jessica A ^a   Yamada, Hidetaka ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

Arcuate nucleus; Food; Insulin; Leptin; Reward; Ventral tegmental area

Indexed keywords

INSULIN; LEPTIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; FEMALE; FOOD INTAKE; HORMONE ACTION; NONHUMAN; PRIORITY JOURNAL; RAT; REWARD; SELF STIMULATION; VENTRAL TEGMENTUM; WEIGHT REDUCTION;

ANIMALS; ARCUATE NUCLEUS; BRAIN; CONDITIONING, OPERANT; EATING; ELECTRODES, IMPLANTED; FEMALE; HYPOGLYCEMIC AGENTS; INSULIN; LEPTIN; MICROINJECTIONS; RATS; RATS, SPRAGUE-DAWLEY; REWARD; SELF STIMULATION; VENTRAL TEGMENTAL AREA;

EID: 79952706915     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2011.01.020     Document Type: Article

References (68)

1. Popkin B.M., Doak C.M. The obesity epidemic is a worldwide phenomenon. Nutr Rev 1998, 56(4 (Pt 1)):106-114.
2. Flegal K.M., Carroll M.D., Ogden C.L., Curtin L.R. Prevalence and trends in obesity among US adults, 1999-2008. JAMA 2010, 303(3):235-241.
3. Woods S.C., Seeley R.J., Porte D., Schwartz M.W. Signals that regulate food intake and energy homeostasis. Science 1998, 280(5368):1378-1383.
4. Woods S.C., Schwartz M.W., Baskin D.G., Seeley R.J. Food intake and the regulation of body weight. Annu Rev Psychol 2000, 51:255-277.
5. Shioda S., Funahashi H., Nakajo S., Yada T., Maruta O., Nakai Y. Immunohistochemical localization of leptin receptor in the rat brain. Neurosci Lett 1998, 243(1-3):41-44.
6. Elmquist J.K., Bjorbaek C., Ahima R.S., Flier J.S., Saper C.B. Distributions of leptin receptor mRNA isoforms in the rat brain. J. Comp Neurol 1998, 395(4):535-547.
7. Figlewicz D.P., Evans S.B., Murphy J., Hoen M., Baskin D.G. Expression of receptors for insulin and leptin in the ventral tegmental area/substantia nigra (VTA/SN) of the rat. Brain Res 2003, 964(1):107-115.
8. Havrankova J., Roth J., Brownstein M. Insulin receptors are widely distributed in the central nervous system of the rat. Nature 1978, 272(5656):827-829.
9. Werther G.A., Hogg A., Oldfield B.J., McKinley M.J., Figdor R., Allen A.M., et al. Localization and characterization of insulin receptors in rat brain and pituitary gland using in vitro autoradiography and computerized densitometry. Endocrinology 1987, 121(4):1562-1570.
10. Air E.L., Benoit S.C., Blake Smith K.A., Clegg D.J., Woods S.C. Acute third ventricular administration of insulin decreases food intake in two paradigms. Pharmacol Biochem Behav 2002, 72(1-2):423-429.
11. Woods S.C., Lotter E.C., McKay L.D., Porte D. Chronic intracerebroventricular infusion of insulin reduces food intake and body weight of baboons. Nature 1979, 282(5738):503-505.
12. Schwartz M.W., Woods S.C., Porte D., Seeley R.J., Baskin D.G. Central nervous system control of food intake. Nature 2000, 404(6778):661-671.
13. Zhang Y., Proenca R., Maffei M., Barone M., Leopold L., Friedman J.M. Positional cloning of the mouse obese gene and its human homologue. Nature 1994, 372(6505):425-432.
14. Chua S.C., Chung W.K., Wu-Peng X.S., Zhang Y., Liu S.M., Tartaglia L., et al. Phenotypes of mouse diabetes and rat fatty due to mutations in the OB (leptin) receptor. Science 1996, 271(5251):994-996.
15. Schwartz M.W., Seeley R.J., Campfield L.A., Burn P., Baskin D.G. Identification of targets of leptin action in rat hypothalamus. J Clin Invest 1996, 98(5):1101-1106.
16. Seeley R.J., van D.G., Campfield L.A., Smith F.J., Burn P., Nelligan J.A., et al. Intraventricular leptin reduces food intake and body weight of lean rats but not obese Zucker rats. Horm Metab Res 1996, 28(12):664-668.
17. Schwartz M.W., Sipols A.J., Marks J.L., Sanacora G., White J.D., Scheurink A., et al. Inhibition of hypothalamic neuropeptide Y gene expression by insulin. Endocrinology 1992, 130(6):3608-3616.
18. Schwartz M.W., Marks J.L., Sipols A.J., Baskin D.G., Woods S.C., Kahn S.E., et al. Central insulin administration reduces neuropeptide Y mRNA expression in the arcuate nucleus of food-deprived lean (Fa/Fa) but not obese (fa/fa) Zucker rats. Endocrinology 1991, 128(5):2645-2647.
19. Kalra S.P., Dube M.G., Sahu A., Phelps C.P., Kalra P.S. Neuropeptide Y secretion increases in the paraventricular nucleus in association with increased appetite for food. Proc Natl Acad Sci USA 1991, 88(23):10931-10935.
20. Sahu A., Kalra S.P. Neuropeptidergic regulation of feeding behavior neuropeptide Y. Trends Endocrinol Metab 1993, 4(7):217-224.
21. Obici S., Feng Z., Karkanias G., Baskin D.G., Rossetti L. Decreasing hypothalamic insulin receptors causes hyperphagia and insulin resistance in rats. Nat Neurosci 2002, 5(6):566-572.
22. 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 Physiol Regul Integr Comp Physiol 2008, 295(2):R388-R394.
23. Satoh N., Ogawa Y., Katsuura G., Hayase M., Tsuji T., Imagawa K., et al. The arcuate nucleus as a primary site of satiety effect of leptin in rats. Neurosci Lett 1997, 224(3):149-152.
24. 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.
25. 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 2010.
26. Lutter M., Nestler E.J. Homeostatic and hedonic signals interact in the regulation of food intake. J Nutr 2009, 139(3):629-632.
27. Ludwig D.S., Majzoub J.A., Al-Zahrani A., Dallal G.E., Blanco I., Roberts S.B. High glycemic index foods, overeating, and obesity. Pediatrics 1999, 103(3):E26.
28. Lissner L., Heitmann B.L. Dietary fat and obesity: evidence from epidemiology. Eur J Clin Nutr 1995, 49(2):79-90.
29. Koob G.F. Drugs of abuse: anatomy, pharmacology and function of reward pathways. Trends Pharmacol Sci 1992, 13(5):177-184.
30. Wise R.A., Rompre P.P. Brain dopamine and reward. Annu Rev Psychol 1989, 40:191-225.
31. 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.
32. Figlewicz D.P., Bennett J.L., Naleid A.M., Davis C., Grimm J.W. Intraventricular insulin and leptin decrease sucrose self-administration in rats. Physiol Behav 2006, 89(4):611-616.
33. Carr K.D., Kim G., Cabezad V. Hypoinsulinemia may mediate the lowering of self-stimulation thresholds by food restriction and streptozotocin-induced diabetes. Brain Res 2000, 863(1-2):160-168.
34. Fulton S., Woodside B., Shizgal P. Modulation of brain reward circuitry by leptin. Science 2000, 287:125-128.
35. Licinio J., Negrao A.B., Mantzoros C., Kaklamani V., Wong M.L., Bongiorno P.B., et al. Sex differences in circulating human leptin pulse amplitude: clinical implications. J Clin Endocrinol Metab 1998, 83(11):4140-4147.
36. Clegg D.J., Riedy C.A., Smith K.A., Benoit S.C., Woods S.C. Differential sensitivity to central leptin and insulin in male and female rats. Diabetes 2003, 52(3):682-687.
37. Koob G.F., Le Moal M. Drug abuse: hedonic homeostatic dysregulation. Science 1997, 278:52-58.
38. Bruijnzeel A.W., Lewis B., Bajpai L.K., Morey T.E., Dennis D.M., Gold M. Severe deficit in brain reward function associated with fentanyl withdrawal in rats. Biol Psychiatry 2006, 59(5):477-480.
39. Bruijnzeel A.W., Zislis G., Wilson C., Gold M.S. Antagonism of CRF receptors prevents the deficit in brain reward function associated with precipitated nicotine withdrawal in rats. Neuropsychopharmacology 2007, 32(4):955-963.
40. Kornetsky C., Esposito R.U. Euphorigenic drugs: effects on the reward pathways of the brain. Fed Proc 1979, 38(11):2473-2476.
41. Markou A., Koob G.F. Construct validity of a self-stimulation threshold paradigm: effects of reward and performance manipulations. Physiol Behav 1992, 51(1):111-119.
42. Markou A., Koob G.F. Postcocaine anhedonia. An animal model of cocaine withdrawal. Neuropsychopharmacology 1991, 4(1):17-26.
43. Bruijnzeel A.W., Markou A. Adaptations in cholinergic transmission in the ventral tegmental area associated with the affective signs of nicotine withdrawal in rats. Neuropharmacology 2004, 47(4):572-579.
44. Marcinkiewcz C.A., Prado M.M., Isaac S.K., Marshall A., Rylkova D., Bruijnzeel A.W. Corticotropin-releasing factor within the central nucleus of the amygdala and the nucleus accumbens shell mediates the negative affective state of nicotine withdrawal in rats. Neuropsychopharmacology 2009, 34(7):1743-1752.
45. Yamada H., Bruijnzeel A.W. Stimulation of alpha2-adrenergic receptors in the central nucleus of the amygdala attenuates stress-induced reinstatement of nicotine seeking in rats. Neuropharmacology 2011, 60(2-3):303-311.
46. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, San Diego.
47. Clifton P.G., Barnfield A.M., Philcox L. A behavioural profile of fluoxetine-induced anorexia. Psychopharmacology (Berl) 1989, 97(1):89-95.
48. Epping-Jordan M.P., Watkins S.S., Koob G.F., Markou A. Dramatic decreases in brain reward function during nicotine withdrawal. Nature 1998, 393(6680):76-79.
49. Figlewicz D.P., Benoit S.C. Insulin, leptin, and food reward: update 2008. Am J Physiol Regul Integr Comp Physiol 2009, 296(1):R9-R19.
50. Mistry A.M., Swick A.G., Romsos D.R. Leptin rapidly lowers food intake and elevates metabolic rates in lean and ob/ob mice. J Nutr 1997, 127(10):2065-2072.
51. Schwartz G.J., Moran T.H. Leptin and neuropeptide y have opposing modulatory effects on nucleus of the solitary tract neurophysiological responses to gastric loads: implications for the control of food intake. Endocrinology 2002, 143(10):3779-3784.
52. Kobashi M., Ichikawa H., Sugimoto T., Adachi A. Response of neurons in the solitary tract nucleus, area postrema and lateral parabrachial nucleus to gastric load of hypertonic saline. Neurosci Lett 1993, 158(1):47-50.
53. Phillips R.J., Powley T.L. Gastric volume rather than nutrient content inhibits food intake. Am J Physiol 1996, 271(3 (Pt 2)):R766-R769.
54. Phillips R.J., Powley T.L. Gastric volume detection after selective vagotomies in rats. Am J Physiol 1998, 274(6 (Pt 2)):R1626-R1638.
55. Morton G.J., Blevins J.E., Kim F., Matsen M., Figlewicz D.P. The action of leptin in the ventral tegmental area to decrease food intake is dependent on Jak-2 signaling. Am J Physiol Endocrinol Metab 2009, 297(1):E202-E210.
56. Ikeda H., West D.B., Pustek J.J., Figlewicz D.P., Greenwood M.R., Porte D., et al. Intraventricular insulin reduces food intake and body weight of lean but not obese Zucker rats. Appetite 1986, 7(4):381-386.
57. McGowan M.K., Andrews K.M., Kelly J., Grossman S.P. Effects of chronic intrahypothalamic infusion of insulin on food intake and diurnal meal patterning in the rat. Behav Neurosci 1990, 104(2):373-385.
58. Katz A.I., Rubenstein A.H. Metabolism of proinsulin, insulin, and C-peptide in the rat. J Clin Invest 1973, 52(5):1113-1121.
59. Krugel 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(1-3):185-187.
60. Diana M., Pistis M., Muntoni A., Gessa G. Profound decrease of mesolimbic dopaminergic neuronal activity in morphine withdrawn rats. J Pharmacol Exp Ther 1995, 272(2):781-785.
61. Diana M., Pistis M., Carboni S., Gessa G.L., Rossetti Z.L. Profound decrement of mesolimbic dopaminergic neuronal activity during ethanol withdrawal syndrome in rats: electrophysiological and biochemical evidence. Proc Natl Acad Sci USA 1993, 90(17):7966-7969.
62. Weiss F., Markou A., Lorang M.T., Koob G.F. Basal extracellular dopamine levels in the nucleus accumbens are decreased during cocaine withdrawal after unlimited-access self-administration. Brain Res 1992, 593(2):314-318.
63. Wise R.A. Addictive drugs and brain stimulation reward. Annu Rev Neurosci 1996, 19:319-340.
64. Klein S., Coppack S.W., Mohamed-Ali V., Landt M. Adipose tissue leptin production and plasma leptin kinetics in humans. Diabetes 1996, 45(7):984-987.
65. Burt R.L., Davidson I.W. Insulin half-life and utilization in normal pregnancy. Obstet Gynecol 1974, 43(2):161-170.
66. Pinto S., Roseberry A.G., Liu H., Diano S., Shanabrough M., Cai X., et al. Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 2004, 304(5667):110-115.
67. Arnow B., Kenardy J., Agras W.S. The Emotional Eating Scale: the development of a measure to assess coping with negative affect by eating. Int J Eat Disord 1995, 18(1):79-90.
68. Chua J.L., Touyz S., Hill A.J. Negative mood-induced overeating in obese binge eaters: an experimental study. Int J Obes Relat Metab Disord 2004, 28(4):606-610.