Orexin-induced feeding requires NMDA receptor activation in the perifornical region of the lateral hypothalamus

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 293, Issue 3, 2007, Pages

  Doane, Dolores F ^a   Lawson, Marcus A ^a   Meade, Jonathan R ^a   Kotz, Catherine M ^b   Beverly, J Lee ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b University of Minnesota   (United States)

Author keywords

Food intake regulation; Hypocretin; Microdialysis

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; OREXIN A;

ANIMAL EXPERIMENT; ARTICLE; CANNULA; CEREBROSPINAL FLUID; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; FOOD INTAKE; LATERAL HYPOTHALAMUS; MALE; MICRODIALYSIS; MICROINJECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT;

2-AMINO-5-PHOSPHONOVALERATE; ANIMALS; EATING; EXCITATORY AMINO ACID ANTAGONISTS; HYPOTHALAMIC AREA, LATERAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICRODIALYSIS; MICROINJECTIONS; NEUROPEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; SYMPATHOMIMETICS;

EID: 34548417078     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00282.2007     Document Type: Article

References (45)

1. Backberg M, Hervieu G, Wilson S, Meister B. Orexin receptor-1 (OX-R1) immunoreactivity in chemically identified neurons of the hypothalamus: focus on orexin targets involved in control of food and water intake. Eur J Neurosci 15: 315-328, 2002.
2. Bernardis LL, Bellinger LL. The lateral hypothalamic area revisited: ingestive behavior. Neurosci Biobehav Rev 20: 189-287, 1996.
3. Beverly JL, Beverly MF, Meguid MM. Alterations in extracellular GABA in the ventral hypothalamus of rats in response to acute glucoprivation. Am J Physiol Regul Integr Comp Physiol 269: R1174-R1178, 1995.
4. Blevins JE, Truong BG, Gietzen DW. NMDA receptor function within the anterior piriform cortex and lateral hypothalamus in rats on the control of intake of amino acid-deficient diets. Brain Res 1019: 124-133, 2004.
5. Burdakov D. Electrical signaling in central orexin/hypocretin circuits: tuning arousal and appetite to fit the environment. Neuroscientist 10: 286-291, 2004.
6. Burdakov D, Alexopoulos H. Metabolic state signalling through central hypocretin/orexin neurons. J Cell Mol Med 9: 795-803, 2005.
7. Date Y, Ueta Y, Yamashita H, Yamaguchi H, Matsukura S, Kangawa K, Sakurai T, Yanagisawa M, Nakazato M. Orexins, orexigenic hypothalamic peptides, interact with autonomic, neuroendocrine and neuroregulatory systems. Proc Natl Acad Sci USA 96: 748-753, 1999.
8. Dube MG, Kalra SP, Kalra PS. Food intake elicited by central administration of orexins/hypocretins: identification of hypothalamic sites of action. Brain Res 842: 473-477, 1999.
9. Duva MA, Tomkins EM, Moranda LM, Kaplan R, Sukhaseum A, Jimenez A, Stanley BG. Reverse microdialysis of N-methyl-D-aspartic acid into the lateral hypothalamus of rats: effects on feeding and other behaviors. Brain Res 921: 122-132, 2001.
10. Duva MA, Tomkins EM, Moranda LM, Kaplan R, Sukhaseum A, Stanley BG. Origins of lateral hypothalamic afferents associated with N-methyl-D-aspartic acid-elicited eating studied using reverse microdialysis of NMDA and Fluorogold. Neurosci Res 52: 95-106, 2005.
11. Gao XB, van den Pol AN. Melanin concentrating hormone depresses synaptic activity of glutamate and GABA neurons from rat lateral hypothalamus. J Physiol 533: 237-252, 2001.
12. Hagan JJ, Leslie RA, Patel S, Evans ML, Wattam TA, Holmes S, Benham CD, Taylor SG, Routledge C, Hemmati P, Munton RP, Ashmeade TE, Shah AS, Hatcher JP, Hatcher PD, Jones DN, Smith MI, Piper DC, Hunter AJ, Porter RA, Upton N. Orexin A activates locus coeruleus cell firing and increases arousal in the rat. Proc Natl Acad Sci USA 96: 10911-10916, 1999.
13. Harris GC, Aston-Jones G. Arousal and reward: a dichotomy in orexin function. Trends Neurosci 29: 571-577, 2006.
14. Haynes AC, Jackson B, Chapman H, Tadayyon M, Johns A, Porter RA, Arch JR. A selective orexin-1 receptor antagonist reduces food consumption in male and female rats. Regul Pept 96: 45-51, 2000.
15. Horvath TL, Diano S, van den Pol AN. Synaptic interaction between hypocretin (orexin) and neuropeptide Y cells in the rodent and primate hypothalamus: a novel circuit implicated in metabolic and endocrine regulations. J Neurosci 19: 1072-1087, 1999.
16. John J, Wu MF, Kodama T, Siegel JM. Intravenously administered hypocretin-1 alters brain amino acid release: an in vivo microdialysis study in rats. J Physiol 548: 557-562, 2003.
17. Kageyama H, Kita T, Toshinai K, Guan JL, Date Y, Takenoya F, Kato S, Matsumoto H, Ohtaki T, Nakazato M, Shioda S. Galanin-like peptide promotes feeding behaviour via activation of orexinergic neurones in the rat lateral hypothalamus. J Neuroendocrinol 18: 33-41, 2006.
18. Kodama T, Kimura M. Arousal effects of orexin-A correlate with GLU release from the locus coeruleus in rats. Peptides 23: 1673-1681, 2002.
19. Lee SW, Stanley BG. NMDA receptors mediate feeding elicited by neuropeptide Y in the lateral and perifornical hypothalamus. Brain Res 1063: 1-8, 2005.
20. Li Y, Gao XB, Sakurai T, van den Pol AN. Hypocretin/Orexin excites hypocretin neurons via a local glutamate neuron-A potential mechanism for orchestrating the hypothalamic arousal system. Neuron 36: 1169-1181, 2002.
21. Marcus JN, Aschkenasi CJ, Lee CE, Chemelli RM, Saper CB, Yanagisawa M, Elmquist JK. Differential expression of orexin receptors 1 and 2 in the rat brain. J Comp Neurol 435: 6-25, 2001.
22. Mieda M, Williams SC, Sinton CM, Richardson JA, Sakurai T, Yanagisawa M. Orexin neurons function in an efferent pathway of a food-entrainable circadian oscillator in eliciting food-anticipatory activity and wakefulness. J Neurosci 24: 10493-10501, 2004.
23. Mistlberger RE, Antle MC, Kilduff TS, Jones M. Food- and light-entrained circadian rhythms in rats with hypocretin-2-saporin ablations of the lateral hypothalamus. Brain Res 980: 161-168, 2003.
24. 2+ signaling in a reciprocal manner to leptin: orexigenic neuronal pathways in the mediobasal hypothalamus. Eur J Neurosci 19: 1524-1534, 2004.
25. Niimi M, Sato M, Taminato T. Neuropeptide Y in central control of feeding and interactions with orexin and leptin. Endocrine 14: 269-273, 2001.
26. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. Orlando, FL: Academic, 1986.
27. Rada P, Tucci S, Murzi E, Hernandez L. Extracellular glutamate increases in the lateral hypothalamus and decreases in the nucleus accumbens during feeding. Brain Res 768: 338-340, 1997.
28. Rosin DL, Weston MC, Sevigny CP, Stornetta RL, Guyenet PG. Hypothalamic orexin (hypocretin) neurons express vesicular glutamate transporters VGLUT1 or VGLUT2. J Comp Neurol 465: 593-603, 2003.
29. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, Williams SC, Richardson JA, Kozlowski GP, Wilson S, Arch JR, Buckingham RE, Haynes AC, Carr SA, Annan RS, McNulty DE, Liu WS, Terrett JA, Elshourbagy NA, Bergsma DJ, Yanagisawa M. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92: 573-585, 1998.
30. Shiraishi T, Oomura Y, Sasaki K, Wayner MJ. Effects of leptin and orexin-A on food intake and feeding related hypothalamic neurons. Physiol Behav 71: 251-261, 2000.
31. Song CH, Chen XW, Xia JX, Yu ZP, Hu ZA. Modulatory effects of hypocretin-1/orexin-A with glutamate and γ-aminobutyric acid on freshly isolated pyramidal neurons from the rat prefrontal cortex. Neurosci Lett 399: 101-105, 2006.
32. Stanley BG, Ha LH, Spears LC, Dee MG 2nd. Lateral hypothalamic injections of glutamate, kainic acid, D,L-α-amino-3-hydroxy-5- methylisoxazole propionic acid or N-methyl-D-aspartic acid rapidly elicit intense transient eating in rats. Brain Res 613: 88-95, 1993.
33. Stanley BG, Willett VL 3rd, Donias HW, Dee MG 2nd, Duva MA. Lateral hypothalamic NMDA receptors and glutamate as physiological mediators of eating and weight control. Am J Physiol Regul Integr Comp Physiol 270: R443-R449, 1996.
34. Stanley BG, Willett VL, 3rd Donias HW, Ha LH, Spears LC. The lateral hypothalamus: a primary site mediating excitatory amino acid-elicited eating. Brain Res 630: 41-49, 1993.
35. Sutcliffe JG, de Lecea L. The hypocretins: excitatory neuromodulatory peptides for multiple homeostatic systems, including sleep and feeding. J Neurosci Res 62: 161-168, 2000.
36. Sweet DC, Levine AS, Billington CJ, Kotz CM. Feeding response to central orexins. Brain Res 821: 535-538, 1999.
37. Sweet DC, Levine AS, Kotz CM. Functional opioid pathways are necessary for hypocretin-1 (orexin-A)-induced feeding. Peptides 25: 307-314, 2004.
38. Thorpe AJ, Doane DF, Sweet DC, Beverly JL, Kotz CM. Orexin A in the rostrolateral hypothalamic area induces feeding by modulating GABAergic transmission. Brain Res 1125: 60-66, 2006.
39. Thorpe AJ, Mullett MA, Wang C, Kotz CM. Peptides that regulate food intake: regional, metabolic, and circadian specificity of lateral hypothalamic orexin A feeding stimulation. Am J Physiol Regul Integr Comp Physiol 284: R1409-R1417, 2003.
40. Thorpe AJ, Teske JA, Kotz CM. Orexin A-induced feeding is augmented by caloric challenge. Am J Physiol Regul Integr Comp Physiol 289: R367-R372, 2005.
41. Torrealba F, Yanagisawa M, Saper CB. Colocalization of orexin a and glutamate immunoreactivity in axon terminals in the tuberomammillary nucleus in rats. Neuroscience 119: 1033-1044, 2003.
42. Toshinai K, Date Y, Murakami N, Shimada M, Mondal MS, Shimbara T, Guan JL, Wang QP, Funahashi H, Sakurai T, Shioda S, Matsukura S, Kangawa K, Nakazato M. Ghrelin-induced food intake is mediated via the orexin pathway. Endocrinology 144: 1506-1512, 2003.
43. Van den Pol AN, Gao XB, Obrietan K, Kilduff TS, Belousov AB. Presynaptic and postsynaptic actions and modulation of neuroendocrine neurons by a new hypothalamic peptide, hypocretin/orexin. J Neurosci 18: 7962-7971, 1998.
44. Van den Top M, Lee K, Whyment AD, Blanks AM, Spanswick D. Orexigen-sensitive NPY/AgRP pacemaker neurons in the hypothalamic arcuate nucleus. Nat Neurosci 7: 493-494, 2004.
45. Yamanaka A, Beuckmann CT, Willie JT, Hara J, Tsujino N, Mieda M, Tominaga M, Yagami K, Sugiyama F, Goto K, Yanagisawa M, Sakurai T. Hypothalamic orexin neurons regulate arousal according to energy balance in mice. Neuron 38: 701-713, 2003.