Orexins in the midline thalamus are involved in the expression of conditioned place aversion to morphine withdrawal

Physiology and Behavior

Volumn 102, Issue 1, 2011, Pages 42-50

  Li, Yonghui ^a,b   Wang, Huiying ^a   Qi, Keke ^a   Chen, Xiaoyu ^b   Li, Sa ^b   Sui, Nan ^a   Kirouac, Gilbert J ^b,c  

^a INSTITUTE OF PSYCHOLOGY   (China)

^b UNIVERSITY OF MANITOBA   (Canada)

^c UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Conditioned place aversion; Extended amygdala; Hypocretin; Morphine withdrawal; Orexin; Thalamus

Indexed keywords

1 (2 METHYL 6 BENZOXAZOLYL) 3 (1,5 NAPHTHYRIDIN 4 YL)UREA; MORPHINE; NALOXONE; OREXIN 1 RECEPTOR; OREXIN 2 RECEPTOR; PROTEIN INHIBITOR; TCSOX229; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVERSIVE BEHAVIOR; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; INNERVATION; MALE; NERVE FIBER; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; RAT; THALAMUS MIDLINE NUCLEUS; WITHDRAWAL SYNDROME;

ANIMALS; AVOIDANCE LEARNING; BENZOXAZOLES; CONDITIONING, CLASSICAL; DISEASE MODELS, ANIMAL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICROINJECTIONS; MIDLINE THALAMIC NUCLEI; MORPHINE; NALOXONE; NEUROPEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NEUROPEPTIDE; SUBSTANCE WITHDRAWAL SYNDROME; UREA;

EID: 78149241646     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2010.10.006     Document Type: Article

References (65)

1. O'Brien C.P. Review. Evidence-based treatments of addiction. Philos Trans R Soc Lond B Biol Sci 2008, 363:3277-3286.
2. Koob G.F. Dynamics of neuronal circuits in addiction: reward, antireward, and emotional memory. Pharmacopsychiatry 2009, 42(Suppl 1):S32-S41.
3. Boutrel B., de Lecea L. Addiction and arousal: the hypocretin connection. Physiol Behav 2008, 93:947-951.
4. Aston-Jones G., Smith R.J., Moorman D.E., Richardson K.A. Role of lateral hypothalamic orexin neurons in reward processing and addiction. Neuropharmacology 2009, 56(Suppl 1):112-121.
5. Zhou Y., Bendor J., Hofmann L., Randesi M., Ho A., Kreek M.J. Mu opioid receptor and orexin/hypocretin mRNA levels in the lateral hypothalamus and striatum are enhanced by morphine withdrawal. J Endocrinol 2006, 191:137-145.
6. Sharf R., Sarhan M., Dileone R.J. Orexin mediates the expression of precipitated morphine withdrawal and concurrent activation of the nucleus accumbens shell. Biol Psychiatry 2008, 64:175-183.
7. 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.
8. Kirouac G.J., Parsons M.P., Li S. Orexin (hypocretin) innervation of the paraventricular nucleus of the thalamus. Brain Res 2005, 1059:179-188.
9. Parsons M.P., Li S., Kirouac G.J. The paraventricular nucleus of the thalamus as an interface between the orexin and CART peptides and the shell of the nucleus accumbens. Synapse 2006, 59:480-490.
10. Li S., Kirouac G.J. Projections from the paraventricular nucleus of the thalamus to the forebrain, with special emphasis on the extended amygdala. J Comp Neurol 2008, 506:263-287.
11. Vertes R.P., Hoover W.B. Projections of the paraventricular and paratenial nuclei of the dorsal midline thalamus in the rat. J Comp Neurol 2008, 508:212-237.
12. Hsu D.T., Price J.L. Paraventricular thalamic nucleus: subcortical connections and innervation by serotonin, orexin, and corticotropin-releasing hormone in macaque monkeys. J Comp Neurol 2009, 512:825-848.
13. Parsons M.P., Li S., Kirouac G.J. Functional and anatomical connection between the paraventricular nucleus of the thalamus and dopamine fibers of the nucleus accumbens. J Comp Neurol 2007, 500:1050-1063.
14. Alheid G.F. Extended amygdala and basal forebrain. Ann NY Acad Sci 2003, 985:185-205.
15. de Olmos J.S., Beltramino C.A., Alheid G.F. Amygdala and extended amygdala of the rat: a cytoarchitectonical, fibroarchitectonical, and chemoarchitectonical survey. The rat nervous system 2004, 509-603. Academic Press, New York. Third edition. G. Paxinos (Ed.).
16. Alheid G.F., Heimer L. New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 1988, 27:1-39.
17. Alheid G.F., de Olmos J.S., Beltramino C.A. Amygdala and extended amygdala. The rat nervous system 1995, 495-578. Academic, San Diego. 2nd ed. G. Paxinos (Ed.).
18. Frenois F., Cador M., Caille S., Stinus L., Le Moine C. Neural correlates of the motivational and somatic components of naloxone-precipitated morphine withdrawal. Eur J Neurosci 2002, 16:1377-1389.
19. Gracy K.N., Dankiewicz L.A., Koob G.F. Opiate withdrawal-induced fos immunoreactivity in the rat extended amygdala parallels the development of conditioned place aversion. Neuropsychopharmacology 2001, 24:152-160.
20. Veinante P., Stoeckel M.E., Lasbennes F., Freund-Mercier M.J. c-Fos and peptide immunoreactivities in the central extended amygdala of morphine-dependent rats after naloxone-precipitated withdrawal. Eur J Neurosci 2003, 18:1295-1305.
21. Jin C., Araki H., Nagata M., Shimosaka R., Shibata K., Suemaru K., et al. Expression of c-Fos in the rat central amygdala accompanies the acquisition but not expression of conditioned place aversion induced by withdrawal from acute morphine dependence. Behav Brain Res 2005, 161:107-112.
22. Faure A., Richard J.M., Berridge K.C. Desire and dread from the nucleus accumbens: cortical glutamate and subcortical GABA differentially generate motivation and hedonic impact in the rat. PLoS ONE 2010, 5:e11223.
23. Lang P.J., Davis M. Emotion, motivation, and the brain: reflex foundations in animal and human research. Prog Brain Res 2006, 156:3-29.
24. Davis M., Walker D.L., Miles L., Grillon C. Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology 2009, 35:105-135.
25. Harris G.C., Aston-Jones G. Enhanced morphine preference following prolonged abstinence: association with increased Fos expression in the extended amygdala. Neuropsychopharmacology 2003, 28:292-299.
26. Frenois F., Stinus L., Di Blasi F., Cador M., Le Moine C. A specific limbic circuit underlies opiate withdrawal memories. J Neurosci 2005, 25:1366-1374.
27. Baldo B.A., Daniel R.A., Berridge C.W., Kelley A.E. Overlapping distributions of orexin/hypocretin- and dopamine-beta-hydroxylase immunoreactive fibers in rat brain regions mediating arousal, motivation, and stress. J Comp Neurol 2003, 464:220-237.
28. Stinus L., Le Moal M., Koob G.F. Nucleus accumbens and amygdala are possible substrates for the aversive stimulus effects of opiate withdrawal. Neuroscience 1990, 37:767-773.
29. Akbari E., Motamedi F., Naghdi N., Noorbakhshnia M. The effect of antagonization of orexin 1 receptors in CA1 and dentate gyrus regions on memory processing in passive avoidance task. Behav Brain Res 2008, 187:172-177.
30. Akbari E., Naghdi N., Motamedi F. Functional inactivation of orexin 1 receptors in CA1 region impairs acquisition, consolidation and retrieval in Morris water maze task. Behav Brain Res 2006, 173:47-52.
31. Akbari E., Naghdi N., Motamedi F. The selective orexin 1 receptor antagonist SB-334867-A impairs acquisition and consolidation but not retrieval of spatial memory in Morris water maze. Peptides 2007, 28:650-656.
32. Naghdi N., Asadollahi A. Genomic and nongenomic effects of intrahippocampal microinjection of testosterone on long-term memory in male adult rats. Behav Brain Res 2004, 153:1-6.
33. Pinelli A., Trivulzio S. Quantitative evaluation of opioid withdrawal signs in rats repeatedly treated with morphine and injected with naloxone, in the absence or presence of the antiabstinence agent clonidine. J Pharmacol Toxicol Meth 1997, 38:117-131.
34. Marchant N.J., Densmore V.S., Osborne P.B. Coexpression of prodynorphin and corticotrophin-releasing hormone in the rat central amygdala: evidence of two distinct endogenous opioid systems in the lateral division. J Comp Neurol 2007, 504:702-715.
35. Li Y., Li S., Wei C., Wang H., Sui N., Kirouac G.J. Changes in emotional behavior produced by orexin microinjections in the paraventricular nucleus of the thalamus. Pharmacol Biochem Behav 2010, 95:121-128.
36. Beck C.H., Fibiger H.C. Conditioned fear-induced changes in behavior and in the expression of the immediate early gene c-fos: with and without diazepam pretreatment. J Neurosci 1995, 15:709-720.
37. Igelstrom K.M., Herbison A.E., Hyland B.I. Enhanced c-Fos expression in superior colliculus, paraventricular thalamus and septum during learning of cue-reward association. Neuroscience 2010, 168:706-714.
38. Yasoshima Y., Scott T.R., Yamamoto T. Differential activation of anterior and midline thalamic nuclei following retrieval of aversively motivated learning tasks. Neuroscience 2007, 146:922-930.
39. Brown E.E., Robertson G.S., Fibiger H.C. Evidence for conditional neuronal activation following exposure to a cocaine-paired environment: role of forebrain limbic structures. J Neurosci 1992, 12:4112-4121.
40. Rhodes J.S., Ryabinin A.E., Crabbe J.C. Patterns of brain activation associated with contextual conditioning to methamphetamine in mice. Behav Neurosci 2005, 119:759-771.
41. Dayas C.V., McGranahan T.M., Martin-Fardon R., Weiss F. Stimuli linked to ethanol availability activate hypothalamic CART and orexin neurons in a reinstatement model of relapse. Biol Psychiatry 2008, 63:152-157.
42. Hamlin A.S., Clemens K.J., Choi E.A., McNally G.P. Paraventricular thalamus mediates context-induced reinstatement (renewal) of extinguished reward seeking. Eur J Neurosci 2009, 29:802-812.
43. 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.
44. Cluderay J.E., Harrison D.C., Hervieu G.J. Protein distribution of the orexin-2 receptor in the rat central nervous system. Regul Pept 2002, 104:131-144.
45. Li Y., Li S., Wei C., Wang H., Sui N., Kirouac G.J. Orexins in the paraventricular nucleus of the thalamus mediate anxiety-like responses in rats. Psychopharmacol (Berl) 2010, 212:251-265.
46. 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.
47. 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.
48. Boutrel B., Cannella N., de Lecea L. The role of hypocretin in driving arousal and goal-oriented behaviors. Brain Res 2010, 1314:103-111.
49. Azizi H., Mirnajafi-Zadeh J., Rohampour K., Semnanian S. Antagonism of orexin type 1 receptors in the locus coeruleus attenuates signs of naloxone-precipitated morphine withdrawal in rats. Neurosci Lett 2010, 255:255-259.
50. Kelsey J.E., Arnold S.R. Lesions of the dorsomedial amygdala, but not the nucleus accumbens, reduce the aversiveness of morphine withdrawal in rats. Behav Neurosci 1994, 108:1119-1127.
51. Watanabe T., Yamamoto R., Maeda A., Nakagawa T., Minami M., Satoh M. Effects of excitotoxic lesions of the central or basolateral nucleus of the amygdala on naloxone-precipitated withdrawal-induced conditioned place aversion in morphine-dependent rats. Brain Res 2002, 958:423-428.
52. Nakagawa T., Yamamoto R., Fujio M., Suzuki Y., Minami M., Satoh M., et al. Involvement of the bed nucleus of the stria terminalis activated by the central nucleus of the amygdala in the negative affective component of morphine withdrawal in rats. Neuroscience 2005, 134:9-19.
53. Valverde O., Tzavara E., Hanoune J., Roques B.P., Maldonado R. Protein kinases in the rat nucleus accumbens are involved in the aversive component of opiate withdrawal. Eur J Neurosci 1996, 8:2671-2678.
54. Watanabe T., Nakagawa T., Yamamoto R., Maeda A., Minami M., Satoh M. Involvement of noradrenergic system within the central nucleus of the amygdala in naloxone-precipitated morphine withdrawal-induced conditioned place aversion in rats. Psychopharmacol (Berl) 2003, 170:80-88.
55. Delfs J.M., Zhu Y., Druhan J.P., Aston-Jones G. Noradrenaline in the ventral forebrain is critical for opiate withdrawal-induced aversion. Nature 2000, 403:430-434.
56. Hou Y.Y., Lu B., Li M., Liu Y., Chen J., Chi Z.Q., et al. Involvement of actin rearrangements within the amygdala and the dorsal hippocampus in aversive memories of drug withdrawal in acute morphine-dependent rats. J Neurosci 2009, 29:12,244-12,254.
57. Carlezon W.A., Thomas M.J. Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuropharmacology 2009, 56(Suppl 1):122-132.
58. Cardinal R.N., Parkinson J.A., Hall J., Everitt B.J. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 2002, 26:321-352.
59. Li Y., Li S., Sui N., Kirouac G.J. Orexin-A acts on the paraventricular nucleus of the midline thalamus to inhibit locomotor activity in rats. Pharmacol Biochem Behav 2009, 93:506-514.
60. Trivedi P., Yu H., MacNeil D.J., Van der Ploeg L.H., Guan X.M. Distribution of orexin receptor mRNA in the rat brain. FEBS Lett 1998, 438:71-75.
61. Hervieu G.J., Cluderay J.E., Harrison D.C., Roberts J.C., Leslie R.A. Gene expression and protein distribution of the orexin-1 receptor in the rat brain and spinal cord. Neuroscience 2001, 103:777-797.
62. Bayer L., Eggermann E., Saint-Mleux B., Machard D., Jones B.E., Muhlethaler M., et al. Selective action of orexin (hypocretin) on nonspecific thalamocortical projection neurons. J Neurosci 2002, 22:7835-7839.
63. Huang H., Ghosh P., van den Pol A.N. Prefrontal cortex-projecting glutamatergic thalamic paraventricular nucleus-excited by hypocretin: a feedforward circuit that may enhance cognitive arousal. J Neurophysiol 2006, 95:1656-1668.
64. Kolaj M., Doroshenko P., Yan Cao X., Coderre E., Renaud L.P. Orexin-induced modulation of state-dependent intrinsic properties in thalamic paraventricular nucleus neurons attenuates action potential patterning and frequency. Neuroscience 2007, 147:1066-1075.
65. Sharf R., Sarhan M., Dileone R.J. Role of orexin/hypocretin in dependence and addiction. Brain Res 2010, 1314:130-138.