A role for hypocretin (orexin) in male sexual behavior

Journal of Neuroscience

Volumn 27, Issue 11, 2007, Pages 2837-2845

  Muschamp, John W ^a,d   Dominguez, Juan M ^a,e   Sato, Satoru M ^b,d   Shen, Roh Yu ^c   Hull, Elaine M ^a,d  

^a FLORIDA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c RESEARCH INSTITUTE ON ADDICTIONS   (United States)

^d UNIVERSITY AT BUFFALO   (United States)

^e AMERICAN UNIVERSITY   (United States)

Author keywords

Dopamine; Electrophysiology; Hypocretin orexin; Male rats; Sexual behavior; Ventral tegmental area

Indexed keywords

ANDROGEN RECEPTOR; ESTRADIOL; ESTROGEN RECEPTOR; OREXIN; PROTEIN ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY LABELING; ARTICLE; BRAIN NERVE CELL; CASTRATION; CELL COUNT; CELL POPULATION; CONTROLLED STUDY; COPULATION; DOPAMINERGIC NERVE CELL; FEMALE; IMMUNOREACTIVITY; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; SEXUAL BEHAVIOR; VENTRAL TEGMENTUM;

ANIMALS; FEMALE; GONADAL STEROID HORMONES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; NEURONS; NEUROPEPTIDES; ORCHIECTOMY; RATS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY; SEXUAL BEHAVIOR, ANIMAL; VENTRAL TEGMENTAL AREA;

EID: 33947326579     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4121-06.2007     Document Type: Article

References (67)

1. Berridge KC, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28:309-369.
2. Bielajew C, Shizgal P (1986) Evidence implicating descending fibers in self-stimulation of the medial forebrain bundle. J Neurosci 6:919-929.
3. Borgland SL, Taha SA, Sarti F, Fields HL, Bonci A (2006) Orexin A in the VTA is critical for the induction of synaptic plasticity and behavioral sensitization to cocaine. Neuron 49:589-601.
4. Boutrel B, Kenny PJ, Specio SE, Martin-Fardon R, Markou A, Koob GF, de Lecea L (2005) Role for hypocretin in mediating stress-induced reinstatement of cocaine-seeking behavior. Proc Natl Acad Sci USA 102:19168-19173.
5. + channels mediate inhibition of orexin neurons by glucose. Neuron 50:711-722.
6. Caggiula AR, Hoebel BG (1966) "Copulation-reward site" in the posterior hypothalamus. Science 153:1284-1285.
7. Cai XJ, Widdowson PS, Harrold J, Wilson S, Buckingham RE, Arch JR, Tadayyon M, Clapham JC, Wilding J, Williams G (1999) Hypothalamic orexin expression: modulation by blood glucose and feeding. Diabetes 48:2132-2137.
8. Cleveland DW, Fischer SG, Kirschner MW, Laemmli UK (1977) Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem 252:1102-1106.
9. de Lecea L, Kilduff TS, Peyron C, Gao X, Foye PE, Danielson PE, Fukuhara C, Battenberg EL, Gautvik VT, Bartlett II FS, Frankel WN, van den Pol AN, Bloom FE, Gautvik KM, Sutcliffe JG (1998) The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci USA 95:322-327.
10. DiLeone RJ, Georgescu D, Nestler EJ (2003) Lateral hypothalamic neuropeptides in reward and drug addiction. Life Sci 73:759-768.
11. Enyeart JJ, Sheu SS, Hinkle PM (1987) Dihydropyridine modulators of voltage-sensitive Ca2+ channels specifically regulate prolactin production by GH4C1 pituitary tumor cells. J Biol Chem 262:3154-3159.
12. Espana RA, Valentino RJ, Berridge CW (2003) Fos immunoreactivity in hypocretin-synthesizing and hypocretin-1 receptor-expressing neurons: effects of diurnal and nocturnal spontaneous waking, stress and hypocretin-1 administration. Neuroscience 121:201-217.
13. Fadel J, Deutch AY (2002) Anatomical substrates of orexin-dopamine interactions: lateral hypothalamic projections to the ventral tegmental area. Neuroscience 111:379-387.
14. Fulop T, Radabaugh S, Smith C (2005) Activity-dependent differential transmitter release in mouse adrenal chromaffin cells. J Neurosci 25:7324-7332.
15. Fulton S, Woodside B, Shizgal P (2000) Modulation of brain reward circuitry by leptin. Science 287:125-128.
16. Georges F, Aston-Jones G (2002) Activation of ventral tegmental area cells by the bed nucleus of the stria terminalis: a novel excitatory amino acid input to midbrain dopamine neurons. J Neurosci 22:5173-5187.
17. Grace AA, Bunney BS (1983) Intracellular and extracellular electrophysiology of nigral dopaminergic neurons. 1. Identification and characterization. Neuroscience 10:301-315.
18. Grace AA, Bunney BS, Moore H, Todd CL (1997) Dopamine-cell depolarization block as a model for the therapeutic actions of antipsychotic drugs. Trends Neurosci 20:31-37.
19. Griffond B, Risold PY, Jacquemard C, Colard C, Fellmann D (1999) Insulin-induced hypoglycemia increases preprohypocretin (orexin) mRNA in the rat lateral hypothalamic area. Neurosci Lett 262:77-80.
20. Gulia KK, Mallick HN, Kumar VM (2003) Orexin A (hypocretin-1) application at the medial preoptic area potentiates male sexual behavior in rats. Neuroscience 116:921-923.
21. Harris GC, Aston-Jones G (2006) Arousal and reward: a dichotomy in orexin function. Trends Neurosci 29:571-577.
22. Harris GC, Wimmer M, Aston-Jones G (2005) A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437:556-559.
23. Henny P, Jones BE (2006) Innervation of orexin/hypocretin neurons by GABAergic, glutamatergic or cholinergic basal forebrain terminals evidenced by immunostaining for presynaptic vesicular transporter and postsynaptic scaffolding proteins. J Comp Neurol 499:645-661.
24. Hernandez L, Hoebel BG (1988) Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. Life Sci 42:1705-1712.
25. Hoebel BG (1969) Feeding and self-stimulation. Ann NY Acad Sci 157:758-778.
26. Hull EM, Wood RI, McKenna KE (2006) Neurobiology of male sexual behavior. In: Knobil and Neill's physiology of reproduction, Ed 3 (Neill JD, ed), pp 1729-1824. New York: Elsevier.
27. Ikemoto S, Panksepp J (1999) The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking. Brain Res Brain Res Rev 31:6-41.
28. Kanenishi K, Ueno M, Momose S, Kuwabara H, Tanaka H, Sato C, Kobayashi T, Hino O, Sakamoto H, Hata T (2004) Prepro-orexin mRNA expression in the rat brain is increased during pregnancy. Neurosci Lett 368:73-77.
29. Korotkova TM, Sergeeva OA, Eriksson KS, Haas HL, Brown RE (2003) Excitation of ventral tegmental area dopaminergic and nondopaminergic neurons by orexins/hypocretins. J Neurosci 23:7-11.
30. Kotz CM (2006) Integration of feeding and spontaneous physical activity: role for orexin. Physiol Behav 88:294-301.
31. Li Y, Gao XB, Sakurai T, van den Pol AN (2002) Hypocretin/orexin excites hypocretin neurons via a local glutamate neuron-A potential mechanism for orchestrating the hypothalamic arousal system. Neuron 36:1169-1181.
32. Lorrain DS, Matuszewich L, Friedman RD, Hull EM (1997) Extracellular serotonin in the lateral hypothalamic area is increased during the postejaculatory interval and impairs copulation in male rats. J Neurosci 17:9361-9366.
33. Lorrain DS, Riolo JV, Matuszewich L, Hull EM (1999) Lateral hypothalamic serotonin inhibits nucleus accumbens dopamine: implications for sexual satiety. J Neurosci 19:7648-7652.
34. Mileykovskiy BY, Kiyashchenko LI, Siegel JM (2005) Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 46:787-798.
35. Mochizuki T, Crocker A, McCormack S, Yanagisawa M, Sakurai T, Scammell TE (2004) Behavioral state instability in orexin knock-out mice. J Neurosci 24:6291-6300.
36. Morgan JI, Curran T (1991) Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu Rev Neurosci 14:421-451.
37. Nakamura T, Uramura K, Nambu T, Yada T, Goto K, Yanagisawa M, Sakurai T (2000) Orexin-induced hyperlocomotion and stereotypy are mediated by the dopaminergic system. Brain Res 873:181-187.
38. Nambu T, Sakurai T, Mizukami K, Hosoya Y, Yanagisawa M, Goto K (1999) Distribution of orexin neurons in the adult rat brain. Brain Res 827:243-260.
39. Narita M, Nagumo Y, Hashimoto S, Khotib J, Miyatake M, Sakurai T, Yanagisawa M, Nakamachi T, Shioda S, Suzuki T (2006) Direct involvement of orexinergic systems in the activation of the mesolimbic dopamine pathway and related behaviors induced by morphine. J Neurosci 26:398-405.
40. Olszewski PK, Li D, Grace MK, Billington CJ, Kotz CM, Levine AS (2003) Neural basis of orexigenic effects of ghrelin acting within lateral hypothalamus. Peptides 24:597-602.
41. Orsini JC, Jourdan F, Cooper HM, Monmaur P (1985) Influence of female odors on lateral hypothalamus in the male rat. Semiquantitative deoxyglucose analysis. Physiol Behav 35:509-516.
42. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, Ed 4. New York: Academic.
43. Peyron C, Tighe DK, van den Pol AN, de Lecea L, Heller HC, Sutcliffe JG, Kilduff TS (1998) Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neurosci 18:9996-10015.
44. Pfaus JG, Damsma G, Nomikos GG, Wenkstern DG, Blaha CD, Phillips AG, Fibiger HC (1990) Sexual behavior enhances central dopamine transmission in the male rat. Brain Res 530:345-348.
45. Putnam SK, Sato S, Riolo JV, Hull EM (2005) Effects of testosterone metabolites on copulation, medial preoptic dopamine, and NOS-immunoreactivity in castrated male rats. Horm Behav 47:513-522.
46. Rada P, Avena NM, Hoebel BG (2005) Daily bingeing on sugar repeatedly releases dopamine in the accumbens shell. Neuroscience 134:737-744.
47. Rolls ET, Burton MJ, Mora F (1980) Neurophysiological analysis of brain-stimulation reward in the monkey. Brain Res 194:339-357.
48. 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, et al. (1998) Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92:573-585.
49. Sakurai T, Nagata R, Yamanaka A, Kawamura H, Tsujino N, Muraki Y, Kageyama H, Kunita S, Takahashi S, Goto K, Koyama Y, Shioda S, Yanagisawa M (2005) Input of orexin/hypocretin neurons revealed by a genetically encoded tracer in mice. Neuron 46:297-308.
50. Saper CB, Scammell TE, Lu J (2005) Hypothalamic regulation of sleep and circadian rhythms. Nature 437:1257-1263.
51. Sato S, Braham CS, Putnam SK, Hull EM (2005) Neuronal nitric oxide synthase and gonadal steroid interaction in the MPOA of male rats: colocalization and testosterone-induced restoration of copulation and nNOS-immunoreactivity. Brain Res 1043:205-213.
52. Shakiryanova D, Tully A, Hewes RS, Deitcher DL, Levitan ES (2005) Activity-dependent liberation of synaptic neuropeptide vesicles. Nat Neurosci 8:173-178.
53. Shen RY, Choong KC (2006) Different adaptations in ventral tegmental area dopamine neurons in control and ethanol exposed rats after methylphenidate treatment. Biol Psychiatry 59:635-642.
54. Shizgal P (1989) Toward a cellular analysis of intracranial self-stimulation: contributions of collision studies. Neurosci Biobehav Rev 13:81-90.
55. Siegel JM (2004) Hypocretin (orexin): role in normal behavior and neuropathology. Annu Rev Psychol 55:125-148.
56. Simerly RB, Chang C, Muramatsu M, Swanson LW (1990) Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 294:76-95.
57. Smith MD, Jones LS, Wilson MA (2002) Sex differences in hippocampal slice excitability: role of testosterone. Neuroscience 109:517-530.
58. Sutcliffe JG, de Lecea L (2002) The hypocretins: setting the arousal threshold. Nat Rev Neurosci 3:339-349.
59. Swanson LW (2004) Brain maps III: structure of the rat brain, Ed 3. New York: Elsevier.
60. Swanson LW, Sanchez-Watts G, Watts AG (2005) Comparison of melanin-concentrating hormone and hypocretin/orexin mRNA expression patterns in a new parceling scheme of the lateral hypothalamic zone. Neurosci Lett 387:80-84.
61. Taheri S, Sunter D, Dakin C, Moyes S, Seal L, Gardiner J, Rossi M, Ghatei M, Bloom S (2000) Diurnal variation in orexin A immunoreactivity and prepro-orexin mRNA in the rat central nervous system. Neurosci Lett 279:109-112.
62. Thorpe AJ, Cleary JP, Levine AS, Kotz CM (2005) Centrally administered orexin A increases motivation for sweet pellets in rats. Psychopharmacology (Berl) 182:75-83.
63. Vaughan E, Fisher AE (1962) Male sexual behavior induced by intracranial electrical stimulation. Science 137:758-760.
64. Wenkstern D, Pfaus JG, Fibiger HC (1993) Dopamine transmission increases in the nucleus accumbens of male rats during their first exposure to sexually receptive female rats. Brain Res 618:41-46.
65. Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483-494.
66. Yoshida K, McCormack S, Espana RA, Crocker A, Scammell TE (2006) Afferents to the orexin neurons of the rat brain. J Comp Neurol 494:845-861.
67. You ZB, Chen YQ, Wise RA (2001) Dopamine and glutamate release in the nucleus accumbens and ventral tegmental area of rat following lateral hypothalamic self-stimulation. Neuroscience 107:629-639.