Selective Fos induction in hypothalamic orexin/hypocretin, but not melanin-concentrating hormone neurons, by a learned food-cue that stimulates feeding in sated rats

Neuroscience

Volumn 224, Issue , 2012, Pages 70-80

  Petrovich, G D ^a   Hobin, M P ^a   Reppucci, C J ^a  

^a BOSTON COLLEGE   (United States)

Author keywords

Appetite; Conditioning; Motivation; Non homeostatic feeding; Obesity; Orexin

Indexed keywords

MELANIN CONCENTRATING HORMONE; OREXIN; PROTEIN FOS;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASSOCIATION; BRAIN TISSUE; CONDITIONING; CONTROLLED STUDY; DIET RESTRICTION; FEEDING BEHAVIOR; FLUORESCENCE; FOOD INTAKE; HISTOLOGY; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN INDUCTION; RAT;

ANIMALS; CONDITIONING, CLASSICAL; CUES; FEEDING BEHAVIOR; HYPOTHALAMIC HORMONES; HYPOTHALAMUS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LEARNING; MALE; MELANINS; NEURONS; NEUROPEPTIDES; PITUITARY HORMONES; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, LONG-EVANS;

EID: 84866284871     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.08.036     Document Type: Article

References (94)

1. Ammar A.A., Sederholm F., Saito T.R., Scheurink A.J.W., Johnson A.E., Södersten P. NPY-leptin: opposing effects on appetitive and consummatory ingestive behavior and sexual behavior. Am J Physiol Regul Integr Comp Physiol 2000, 278:R1627-R1633.
2. Baldo B.A. Activation of a subpopulation of orexin/hypocretin-containing hypothalamic neurons by GABAa receptor-mediated inhibition of the nucleus accumbens shell, but not exposure to a novel environment. Eur J Neurosci 2004, 19:376-386.
3. Baldo B.A., Daniel R.A., Berridge C.W., Kelley A.E. Overlaping distribution of orexin/hypocretin- and dopamine-β-hydroxylase immunoreactive fibers in rat brain regions mediating arousal, motivation, and stress. J Comp Neurol 2003, 464:220-237.
4. Berridge C.W., España R.A., Vittoz N.M. Hypocretin/orexin in arousal and stress. Brain Res 2010, 1314:91-102.
5. Berridge K.C. Motivation concepts in behavioral neuroscience. Physiol Behav 2004, 81:179-209.
6. Berthoud H.R. Metabolic and hedonic drives in the neural control of appetite: who is the boss?. Curr Opin Neurobiol 2011, 21:888-896.
7. Birch L.L., McPhee L., Sullivan S., Johnson S. Conditioned meal initiation in young children. Appetite 1989, 13:105-113.
8. Blundell J.E., Herberg L.J. Relative effects of nutritional deficit and deprivation period on rate of electrical self-stimulation of lateral hypothalamus. Nat Neurosci 1968, 219:627-628.
9. Boggiano M.M., Dorsey J.R., Thomas J.M., Murdaugh D.L. The Pavlovian power of palatable food: lessons for weight-loss adherence from a new rodent model of cue-induced overeating. Int J Obes 2009, 33:693-701.
10. Borgland S.L., Chang S.J., Bowers M.S., Thompson J.L., Vittoz N., Floresco S.B., et al. Orexin A/hypocretin-1 selectively promotes motivation for positive reinforcers. J Neurosci 2009, 29:11215-11225.
11. Bouton M.E. Learning and the persistence of appetite: extinction and the motivation to eat and overeat. Physiol Behav 2011, 103:51-58.
12. Boutrel B., Cannella N., de Lecea L. The role of hypocretin in driving arousal and goal-oriented behaviors. Brain Res 2010, 1314:103-111.
13. Broberger C., de Lecea L., Sutcliffe J.G., Hökfelt T. Hypocretin/Orexin- and melanin-concentrating hormone-expressing cells form distinct populations in the rodent lateral hypothalamus: relationship to the neuropeptide Y and agouti gene-related protein systems. J Comp Neurol 1998, 402:460-474.
14. Campbell R.E., Smith M.S., Allen S.E., Grayson B.E., Ffrench-Mullen J.M.H., Grove K.L. Orexin neurons express a functional pancreatic polypeptide Y4 receptor. J Neurosci 2003, 23:1487-1497.
15. Carr K.D., Wolinsky T.D. Chronic food restriction and weight loss produce opioid facilitation of perifornical hypothalamic self-stimulation. Brain Res 1993, 607:141-148.
16. Cason A.M., Smith R.J., Tahsili-Fahadan P., Moorman D.E., Sartor G.C., Aston-Jones G. Role of orexin/hypocretin in reward-seeking and addiction: implications for obesity. Physiol Behav 2010, 100:419-428.
17. Chemelli R.M., Willie J.T., Sinton C.M., Elmquist J.K., Scammell T., Lee G., et al. Narcolepsy in orexin knockout mice: molecular genetics of sleep regulation. Cell 1999, 98:437-451.
18. Choi D.L., Davis J.F., Fitzerald 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.
19. Clegg D.J., Air E.L., Woods S.C., Seeley R.J. Eating elicited by orexin-a, but not melanin-concentrating hormone, is opioid mediated. Endocrinology 2002, 143:2995-3000.
20. de Lecea L., Kilduff T.S., Peyron C., Gao X., Foye P.E., Danielson P.E., et al. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci U S A 1998, 95:322-327.
21. Dube M.G., Horvath T.L., Kalra P.S., Kalra S.P. Evidence of NPY receptor involvement in food intake elicited by orexin A in sated rats. Peptides 2000, 21:1557-1560.
22. Elias C.F., Saper C.B., Maratos-Flier E., Tritos N.A., Lee C., Kelly J., et al. Chemically defined projections linking the mediobasal hypothalamus and the lateral hypothalamic area. J Comp Neurol 1998, 402:442-459.
23. Estabrooke I.V., McCarthy M.T., Ko E., Chou T.C., Chemelli R.M., Yanagisawa M., et al. Fos expression in orexin neurons varies with behavioral state. J Neurosci 2001, 21:1656-1662.
24. Flood J.F., Morley J.E. Increased food intake by neuropeptide Y is due to an increased motivation to eat. Peptides 1991, 12:1329-1332.
25. Floyd N.S., Price J.L., Ferry A.T., Keay K.A., Bandler R. Orbitomedial prefrontal cortical projections to hypothalamus in the rat. J Comp Neurol 2001, 432:307-328.
26. Friedman J.M., Halaas J.L. Leptin and the regulation of body weight in mammals. Nat Neurosci 1998, 395:763-770.
27. Fulton S., Woodside B., Shizgal P. Modulation of brain reward circuitry by leptin. Science 2000, 287:125-128.
28. Georgescu D., Zachariou V., Barrot M., Mieda M., Willie J.T., Eisch A.J., et al. Involvement of the lateral hypothalamic peptide orexin in morphine dependence and withdrawal. J Neurosci 2003, 23:3106-3111.
29. Gillard E.R., Khan A.M., Grewal R.S., Mouradi B., Wolfsohn S.D., Stanley B.G. The second messenger cAMP elicits eating by an anatomically specific action in the perifornical hypothalamus. J Neurosci 1998, 18:2646-2652.
30. Geerling J.C., Mettenleiter T.C., Loewy A.D. Orexin neurons project to diverse sympathetic outflow systems. Neuroscience 2003, 122:541-550.
31. Grill H.J., Kaplan J.M. The neuroanatomical axis for control of energy balance. Front Neuroendocrinol 2002, 23:2-40.
32. Hahn J.D. Comparison of melanin-concentrating hormone and hypocretin-orexin peptide expression patterns in a current parceling scheme of the lateral hypothalamic zone. Neurosci Lett 2010, 468:12-17.
33. Hahn J.D., Swanson L.W. Distinct patterns of neuronal inputs and outputs of the juxtaparaventricular and suprafornical regions of the lateral hypothalamic area in the male rat. Brain Res Rev 2010, 64:14-103.
34. Harris G.C., Aston-Jones G. Arousal and reward: a dichotomy in orexin function. Trends Neurosci 2006, 29:571-577.
35. Harris G.C., Wimmer M., Aston-Jones G. A role for lateral hypothalamic orexin neurons in reward seeking. Nat Neurosci 2005, 437:556-559.
36. Hill J.O., Wyatt H.R., Reed G.W., Peters J.C. Obesity and the environment: where do we go from here?. Science 2003, 161:751-756.
37. Holland P.C., Petrovich G.D., Gallagher M. The effects of amygdala lesions on conditioned stimulus-potentiated eating in rats. Psychol Behav 2002, 76:117-129.
38. Horvath T.L., Diano S., van den Pol A.N. Synaptic intercation between hypocretin (orexin) and neuropeptide Y cells in the rodent and primate hypothalamus: a novel circuit implicated in metabolic and endocrine regulations. J Neurosci 1999, 19:1072-1087.
39. Jain M.R., Horvath T.L., Kalra P.S., Kalra S.P. Evidence that NPY Y1 receptors are involved in stimulation of feeding by orexins (hypocretins) in sated rats. Regil Pept 2000, 87:19-24.
40. Johnson AW, Sherwood A, Adamantidis A, Millan M, Gallagher M, Holland PC. Melanin concentrating hormone influences cue driven food intake under conditions of satiety. Society for Neuroscience Abstracts; 2011.
41. Khan A.M., Cheung H.H., Gillard E.R., Palarca J.A., Welsbie D.S., Gurd J.W., et al. Lateral hypothalamic signaling mechanisms underlying feeding stimulation: differential contributions of Src family tyrosine kinases to feeding triggered either by NMDA injection or by food deprivation. J Neurosci 2004, 24:10603-10615.
42. Le Merrer J., Stephens D.N. Food-induced behavioral sensitization, its cross-sensitization to cocaine and morphine, pharmacological blockade, and effect on food intake. J Neurosci 2006, 26:7163-7171.
43. Lee S.W., Stanley B.G. NMDA receptors mediate feeding elicited by neuropeptide Y in the lateral and perifornical hypothalamus. Brain Res 2005, 1063:1-18.
44. Leibowitz S.F. Specificity of hypothalamic peptides in the control of behavioral and physiological procesesses. Ann N Y Acad Sci 1994, 739:12-35.
45. Ludwig D.S., Tritos N.A., Mastaistis J.W., Kulkarni R., Kokkotoy E., Elmquist J., et al. Melanin-concentrating hormone overexpression in transgenic mice leads to obesity and insulin resistance. J Clin Invest 2001, 107:379-386.
46. 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.
47. Martins P.J.F., Marques M.S., Tufik S., D'Almeida V. Orexin activation precedes increased NPY expression, hyperphagia, and metabolic changes in response to sleep deprivation. Am J Physiol Endocrinol Metab 2010, 298:E726-E734.
48. Mena J.D., Sadeghian K., Baldo B.A. Induction of hyperphagia and carbohydrate intake by μ-opioid receptor stimulation in circumscribed region of frontal cortex. J Neurosci 2011, 31:3249-3260.
49. Mieda M., Willie J.T., Hara J., Sinton C.M., Sakurai T., Yanagisawa M. Orexin peptides prevent cataplexy and improve wakefulness in an orexin neuron-ablated model of narcolepsy in mice. Proc Natl Acad Sci U S A 2004, 101:4649-4654.
50. 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. Nat Neurosci 2006, 443:289-295.
51. Nahon J.L., Presse F., Bittencourt J.C., Sawchenko P.E., Vale W. The rat melanin-concentrating hormone messenger ribonucleic acid encodes multiple putative neuropeptides coexpressed in the dorsolateral hypothalamus. Endocrinology 1989, 125:2056-2065.
52. Nair S.G., Golden S.A., Shaham Y. Differential effects of the hypocretin 1 receptor antagonist SB 334867 on high-fat food self-administration and reinstatement of food seeking in rats. Br J Pharmacol 2008, 154:406-416.
53. Niimi M., Sato M., Taminato T. Neuropeptide Y in central control of feeding and interactions with Orexin and Leptin. Endocrine 2001, 14:269-273.
54. Olds J., Milner P. Positive reinforcement produced by electrical stimulation of septal area and other regions of rat brain. J Comp Physiol Psychol 1954, 47:419-427.
55. Pavlov I.P. Conditioned reflexes 1927, Oxford University Press, London.
56. Petrovich G.D. Learning and the motivation to eat: forebrain circuitry. Physiol Behav 2011, 104:582-589.
57. Petrovich G.D., Canteras N.S., Swanson L.W. Combinatorial amygdalar inputs to hippocampal domains and hypothalamic behavior systems. Brain Res Rev 2001, 38:247-289.
58. Petrovich G.D., Holland P.C., Gallagher M. Amygdalar and prefrontal pathways to the lateral hypothalamus are activated by a learned cue that stimulates eating. J Neurosci 2005, 25:8295-8302.
59. Petrovich G.D., Ross C.A., Gallagher M., Holland P.C. Learned contextual cue potentiates eating in rats. Physiol Behav 2007, 90:362-367.
60. Petrovich G.D., Ross C.A., Holland P.C., Gallagher M. Medial prefrontal cortex is necessary for an appetitive contextual conditioned stimulus to promote eating in sated rats. J Neurosci 2007, 27:6436-6441.
61. Petrovich G.D., Setlow B., Holland P.C., Gallagher M. Amygdalo-hypothalamic circuit allows learned cues to override satiety and promote eating. J Neurosci 2002, 22:8748-8753.
62. 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.
63. Qu D., Ludwig D.S., Gammeltoft S., Piper M., Pelleymounter M.A., Cullen M.J., et al. A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nat Neurosci 1996, 380:243-247.
64. Reppucci CJ, Petrovich GD (2011) Characterization of the basolateral amygdala pathways to the medial prefrontal cortex and lateral hypothalamus in rats. Society for Neuroscience Abstracts.
65. Reppucci C.J., Petrovich G.D. Learned food-cue stimulates persistent feeding in sated rats. Appetite 2012, 59:437-447.
66. Reppucci CJ, Petrovich GD (2012b) Neuroanatomical evidence for a topographically organized forebrain network composed of the amygdala, medial prefrontal cortex, and lateral hypothalamus in rats. Society for Neuroscience Abstracts.
67. Rodgers R.J. Dose-response effects of orexin-A on food intake and the behavioural satiety sequence in rats. Regul Pept 2000, 96:71-84.
68. 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, 92:573-585.
69. Saper C.B. Staying awake for dinner: hypothalamic integration of sleep, feeding, and circadian rhythms. Prog Brain Res 2006, 153:243-252.
70. 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.
71. Sharf R., Sarhan M., DiLeone R.J. Role of orexin/hypocretin in dependence and addiction. Brain Res 2010, 1314:130-138.
72. Shimada M., Tritos N.A., Lowell B.B., Flier J.S., Maratos-Flier E. Mice lacking melanin-concentrating hormone are hypophagic and lean. Nat Neurosci 1998, 396:670-674.
73. Simmons DM, Swanson LW (1993) The Nissl stain. In: FG, Wouterlood (Ed.), Neuroscience Protocols. (pp. 93-050-12-01-93-050-12-07). Amsterdam, New York: Elsevier.
74. Small D.M. Individual differences in the neurophysiology of reward and the obesity epidemic. Int J Obes 2009, 33:S44-S48.
75. Stanley B.G., Chin A.S., Leibowitz S.F. Feeding and drinking elicited by central injection of neuropeptide Y: evidence for a hypothalamic site(s) of action. Brain Res Bull 1985, 14:521-524.
76. Stanley B.G., Magdalin W., Seirafi A., Thomas W.J., Leibowitz S.F. The perifornical area: the major focus of (a) patchily distributed hypothalamic neuropeptide Y-sensitive feeding system(s). Brain Res 1993, 604:304-317.
77. Stanley B.G., Urstadt K.R., Charles J.R., Kee T. Glutamate and GABA in lateral hypothalamic mechanisms controlling food intake. Physiol Behav 2011, 104:40-46.
78. Stratford T.R., Kelley A.E. GABA in the nucleus accumbens shell participates in the central regulation of feeding behavior. J Neurosci 1997, 17:4434-4440.
79. Swanson L.W. Cerebral hemisphere regulation of motivated behavior. Brain Res 2000, 886:113-164.
80. Swanson L.W. Brain maps: structure of the rat brain. A laboratory guide with printed and electronic templates for data, models and schematics 2004, Elsevier, Amsterdam.
81. Swanson L.W., Sanchez-Watts G., Watts A.G. Comparison of melanin-concentrating hormone and hypocretin/orexin mRNA expression patterns in a new parceling scheme of the lateral hypothalamic zone. Neurosci Lett 2005, 387:80-84.
82. Thorpe A.J., Cleary J.P., Levine A.S., Kotz C.M. Centrally administered orexin A increases motivation for sweet pellets in rats. Psychopharmacology 2005, 182:75-83.
83. Tsujino N., Sakurai T. Orexin/hypocretin: a neuropeptide at the interface of sleep, energy homeostasis, and reward system. Pharmacol Rev 2009, 61:162-176.
84. Volkow N.D., Wise R.A. How can drug addiction help us understand obesity?. Nat Neurosci 2005, 8:555-560.
85. Watts A.G., Sanchez-Watts G. Rapid and preferential activation of Fos protein in hypocretin/orexin neurons following the reversal of dehydration-anorexia. J Comp Neurol 2007, 502:768-782.
86. Weingarten H.P. Conditioned cues elicit feeding in sated rats: a role for learning in meal initiation. Science 1983, 220:431-433.
87. Willie J.T., Chemelli R.M., Sinton C.M., Yanagisawa M. To eat or to sleep? Orexin in the regulation of feeding and wakefulness. Annu Rev Neurosci 2001, 24:429-458.
88. Wise R.A. Lateral hypothalamic electrical stimulation: does it make animals "hungry" ?. Brain Res 1974, 67:187-209.
89. Woods S.C. The eating paradox: how we tolerate food. Psychol Rev 1991, 98:488-505.
90. Yamanaka A., Beuckmann C.T., Willie J.T., Hara J., Tsujino N., Mieda M., et al. Hypothalamic orexin neurons regulate arousal according to energy balance in mice. Neuron 2003, 38:701-713.
91. Yamanaka A., Kunii K., Nambu T., Tsujino N., Sakai A., Matsuzaki I., et al. Orexin-induced food intake involves neuropeptide Y pathway. Brain Res 2000, 859:404-409.
92. Yoshida K., McCormack S., España R.A., Crocker A., Scammell T. Afferents to the orexin neurons of the rat brain. J Comp Neurol 2006, 494:845-861.
93. Zheng H., Corkern M., Stoyanova I., Patterson L.M., Tian R., Berthoud H.R. Peptides that regulate food intake: appetite-inducing accumbens manipulation activates hypothalamic orexin neurons and inhibits POMC neurons. Am J Physiol 2003, 284:R1436-1444.
94. 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.