Inhibition of VTA neurons activates the centrally projecting Edinger-Westphal nucleus: Evidence of a stress-reward link?

Journal of Chemical Neuroanatomy

Volumn 54, Issue , 2013, Pages 57-61

  Ryabinin, Andrey E ^a   Cocking, Davelle L ^a   Kaur, Simranjit ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Dopamine; Edinger Westphal nucleus; Stress; Tonic inhibition; Urocortin

Indexed keywords

ALCOHOL; MUSCIMOL; PROTEIN FOS; QUINPIROLE;

ANIMAL EXPERIMENT; ARTICLE; AVOIDANCE BEHAVIOR; DOPAMINERGIC NERVE CELL; EDINGER WESTPHAL NUCLEUS; IMMUNOREACTIVITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; REGULATORY MECHANISM; REWARD; STRESS; VENTRAL TEGMENTUM;

DOPAMINE; EDINGER-WESTPHAL NUCLEUS; STRESS; TONIC INHIBITION; UROCORTIN;

ANIMALS; MALE; MESENCEPHALON; MICE; MICE, INBRED C57BL; NEURAL PATHWAYS; NEURONS; REWARD; STRESS, PHYSIOLOGICAL; VENTRAL TEGMENTAL AREA;

EID: 84888431565     PISSN: 08910618     EISSN: 18736300     Source Type: Journal    
DOI: 10.1016/j.jchemneu.2013.05.004     Document Type: Article

References (51)

1. Alcaro A., Panksepp J. The SEEKING mind: primal neuro-affective substrates for appetitive incentive states and their pathological dynamics in addictions and depression. Neuroscience & Biobehavioral Reviews 2011, 35:1805-1820.
2. Allen Institute for Brain Science Allen Brain Atlas 2004, S Allen Institute for Brain Science. http://www.brain-map.org/.
3. Bachtell R.K., Tsivkovskaia N.O., Ryabinin A.E. Alcohol-induced c-Fos expression in the Edinger-Westphal nucleus: pharmacological and signal transduction mechanisms. Journal of Pharmacology and Experimental Therapeutics 2002, 302:516-524.
4. Bachtell R.K., Tsivkovskaia N.O., Ryabinin A.E. Strain differences in urocortin expression in the Edinger-Westphal nucleus and its relation to alcohol-induced hypothermia. Neuroscience 2002, 113:421-434.
5. Bachtell R.K., Wang Y.M., Freeman P., Risinger F.O., Ryabinin A.E. Alcohol drinking produces brain region-selective changes in expression of inducible transcription factors. Brain Research 1999, 847:157-165.
6. Bachtell R.K., Weitemier A.Z., Galvan-Rosas A., Tsivkovskaia N.O., Risinger F.O., Phillips T.J., Grahame N.J., Ryabinin A.E. The Edinger-Westphal-lateral septum urocortin pathway and its relationship to alcohol consumption. The Journal of Neuroscience 2003, 23:2477-2487.
7. Bale T.L., Vale W.W. CRF and CRF receptors: role in stress responsivity and other behaviors. The Annual Review of Pharmacology and Toxicology 2004, 44:525-557.
8. Bittencourt J.C., Vaughan J., Arias C., Rissman R.A., Vale W.W., Sawchenko P.E. Urocortin expression in rat brain: evidence against a pervasive relationship of urocortin-containing projections with targets bearing type 2 CRF receptors. The Journal of Comparative Neurology 1999, 415:285-312.
9. Chang S.L., Patel N.A., Romero A.A. Activation and desensitization of Fos immunoreactivity in the rat brain following ethanol administration. Brain Research 1995, 679:89-98.
10. Congar P., Bergevin A., Trudeau L.E. D2 receptors inhibit the secretory process downstream from calcium influx in dopaminergic neurons: implication of K+ channels. Journal of Neurophysiology 2002, 87:1046-1056.
11. Dreher J.C., Burnod Y. An integrative theory of the phasic and tonic modes of dopamine modulation in the prefrontal cortex. Neural Networks 2002, 15:583-602.
12. Fonareva I., Spangler E., Cannella N., Sabino V., Cottone P., Ciccocioppo R., Zorrilla E.P., Ryabinin A.E. Increased perioculomotor urocortin 1 immunoreactivity in genetically selected alcohol preferring rats. Alcoholism, Clinical and Experimental Research 2009, 33:1956-1965.
13. Gaszner B., Csernus V., Kozicz T. Urocortinergic neurons respond in a differentiated manner to various acute stressors in the Edinger-Westphal nucleus in the rat. The Journal of Comparative Neurology 2004, 480:170-179.
14. Gaszner B., Korosi A., Palkovits M., Roubos E.W., Kozicz T. Neuropeptide Y activates urocortin 1 neurons in the nonpreganglionic Edinger-Westphal nucleus. The Journal of Comparative Neurology 2007, 500:708-719.
15. Gaszner B., Kozicz T. Interaction between catecholaminergic terminals and urocortinergic neurons in the Edinger-Westphal nucleus in the rat. Brain Research 2003, 989:117-121.
16. Giardino W.J., Cote D.M., Li J., Ryabinin A.E. Characterization of genetic differences within the centrally projecting Edinger-Westphal nucleus of C57BL/6J and DBA/2J mice by expression profiling. Frontiers in Neuroanatomy 2012, 6:5.
17. Giardino W.J., Pastor R., Anacker A.M., Spangler E., Cote D.M., Li J., Stenzel-Poore M.P., Phillips T.J., Ryabinin A.E. Dissection of corticotropin-releasing factor system involvement in locomotor sensitivity to methamphetamine. Genes, Brain and Behavior 2011, 10:78-89.
18. Gong S., Zheng C., Doughty M.L., Losos K., Didkovsky N., Schambra U.B., Nowak N.J., Joyner A., Leblanc G., Hatten M.E., Heintz N. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 2003, 425:917-925.
19. Grace A.A. Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 1991, 41:1-24.
20. Grace A.A. The tonic/phasic model of dopamine system regulation and its implications for understanding alcohol and psychostimulant craving. Addiction 2000, 95(Suppl. 2):S119-S128.
21. Jeziorski M., White F.J. Dopamine agonists at repeated autoreceptor-selective doses: effects upon the sensitivity of A10 dopamine autoreceptors. Synapse 1989, 4:267-280.
22. Kalivas P.W., Duffy P., Latimer L.G. Neurochemical and behavioral effects of corticotropin-releasing factor in the ventral tegmental area of the rat. Journal of Pharmacology and Experimental Therapeutics 1987, 242:757-763.
23. Kaur S., Ryabinin A.E. Ghrelin receptor antagonism decreases alcohol consumption and activation of perioculomotor urocortin-containing neurons. Alcoholism, Clinical and Experimental Research 2010, 34:1525-1534.
24. Korotkova T.M., Brown R.E., Sergeeva O.A., Ponomarenko A.A., Haas H.L. Effects of arousal- and feeding-related neuropeptides on dopaminergic and GABAergic neurons in the ventral tegmental area of the rat. European Journal of Neuroscience 2006, 23:2677-2685.
25. Korte S.M., Koolhaas J.M., Wingfield J.C., McEwen B.S. The Darwinian concept of stress: benefits of allostasis and costs of allostatic load and the trade-offs in health and disease. Neuroscience & Biobehavioral Reviews 2005, 29:3-38.
26. Kozicz T. Neurons colocalizing urocortin and cocaine and amphetamine-regulated transcript immunoreactivities are induced by acute lipopolysaccharide stress in the Edinger-Westphal nucleus in the rat. Neuroscience 2003, 116:315-320.
27. Kozicz T., Bittencourt J.C., May P.J., Reiner A., Gamlin P.D., Palkovits M., Horn A.K., Toledo C.A., Ryabinin A.E. The Edinger-Westphal nucleus: a historical, structural, and functional perspective on a dichotomous terminology. The Journal of Comparative Neurology 2011, 519:1413-1434.
28. Kozicz T., Li M., Arimura A. The activation of urocortin immunoreactive neurons in the Einger-Westphal nucleus following stress in rats. Stress 2001, 4:85-90.
29. Kozicz T., Yanaihara H., Arimura A. Distribution of urocortin-like immunoreactivity in the central nervous system of the rat. The Journal of Comparative Neurology 1998, 391:1-10.
30. Lewis K., Li C., Perrin M.H., Blount A., Kunitake K., Donaldson C., Vaughan J., Reyes T.M., Gulyas J., Fischer W., Bilezikjian L., Rivier J., Sawchenko P.E., Vale W.W. Identification of urocortin III, an additional member of the corticotropin-releasing factor (CRF) family with high affinity for the CRF2 receptor. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:7570-7575.
31. Linden A.M., Greene S.J., Bergeron M., Schoepp D.D. Anxiolytic activity of the MGLU2/3 receptor agonist LY354740 on the elevated plus maze is associated with the suppression of stress-induced c-Fos in the hippocampus and increases in c-Fos induction in several other stress-sensitive brain regions. Neuropsychopharmacology 2004, 29:502-513.
32. Neufeld-Cohen A., Tsoory M.M., Evans A.K., Getselter D., Gil S., Lowry C.A., Vale W.W., Chen A. A triple urocortin knockout mouse model reveals an essential role for urocortins in stress recovery. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:19020-19025.
33. Noain D., Avale M.E., Wedemeyer C., Calvo D., Peper M., Rubinstein M. Identification of brain neurons expressing the dopamine D4 receptor gene using BAC transgenic mice. European Journal of Neurosciences 2006, 24:2429-2438.
34. Reyes T.M., Lewis K., Perrin M.H., Kunitake K.S., Vaughan J., Arias C.A., Hogenesch J.B., Gulyas J., Rivier J., Vale W.W., Sawchenko P.E. Urocortin II: a member of the corticotropin-releasing factor (CRF) neuropeptide family that is selectively bound by type 2 CRF receptors. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:2843-2848.
35. Rodaros D., Caruana D.A., Amir S., Stewart J. Corticotropin-releasing factor projections from limbic forebrain and paraventricular nucleus of the hypothalamus to the region of the ventral tegmental area. Neuroscience 2007, 150:8-13.
36. Ryabinin A.E., Criado J.R., Henriksen S.J., Bloom F.E., Wilson M.C. Differential sensitivity of c-Fos expression in hippocampus and other brain regions to moderate and low doses of alcohol. Molecular Psychiatry 1997, 2:32-43.
37. Ryabinin A.E., Galvan-Rosas A., Bachtell R.K., Risinger F.O. High alcohol/sucrose consumption during dark circadian phase in C57BL/6J mice: involvement of hippocampus, lateral septum and urocortin-positive cells of the Edinger-Westphal nucleus. Psychopharmacology (Berl) 2003, 165:296-305.
38. Ryabinin A.E., Tsoory M.M., Kozicz T., Thiele T.E., Neufeld-Cohen A., Chen A., Lowery-Gionta E.G., Giardino W.J., Kaur S. Urocortins: CRF's siblings and their potential role in anxiety, depression and alcohol drinking behavior. Alcohol 2012, 46:349-357.
39. Ryabinin A.E., Yoneyama N., Tanchuck M.A., Mark G.P., Finn D.A. Urocortin 1 microinjection into the mouse lateral septum regulates the acquisition and expression of alcohol consumption. Neuroscience 2008, 151:780-790.
40. Schank J.R., Ryabinin A.E., Giardino W.J., Ciccocioppo R., Heilig M. Stress-related neuropeptides and addictive behaviors: beyond the usual suspects. Neuron 2012, 76:192-208.
41. Spangler E., Cote D.M., Anacker A.M., Mark G.P., Ryabinin A.E. Differential sensitivity of the perioculomotor urocortin-containing neurons to ethanol, psychostimulants and stress in mice and rats. Neuroscience 2009, 160:115-125.
42. Topple A.N., Hunt G.E., McGregor I.S. Possible neural substrates of beer-craving in rats. Neuroscience Letters 1998, 252:99-102.
43. Trinh J.V., Nehrenberg D.L., Jacobsen J.P., Caron M.G., Wetsel W.C. Differential psychostimulant-induced activation of neural circuits in dopamine transporter knockout and wild type mice. Neuroscience 2003, 118:297-310.
44. Turek V.F., Ryabinin A.E. Expression of c-Fos in the mouse Edinger-Westphal nucleus following ethanol administration is not secondary to hypothermia or stress. Brain Research 2005, 1063:132-139.
45. Ungless M.A., Singh V., Crowder T.L., Yaka R., Ron D., Bonci A. Corticotropin-releasing factor requires CRF binding protein to potentiate NMDA receptors via CRF receptor 2 in dopamine neurons. Neuron 2003, 39:401-407.
46. Vale W., Spiess J., Rivier C., Rivier J. Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 1981, 213:1394-1397.
47. Vaughan J., Donaldson C., Bittencourt J., Perrin M.H., Lewis K., Sutton S., Chan R., Turnbull A.V., Lovejoy D., Rivier C., et al. Urocortin, a mammalian neuropeptide related to fish urotensin I and to corticotropin-releasing factor. Nature 1995, 378:287-292.
48. Wang B., Shaham Y., Zitzman D., Azari S., Wise R.A., You Z.B. Cocaine experience establishes control of midbrain glutamate and dopamine by corticotropin-releasing factor: a role in stress-induced relapse to drug seeking. The Journal of Neuroscience 2005, 25:5389-5396.
49. Weitemier A.Z., Ryabinin A.E. Lesions of the Edinger-Westphal nucleus alter food and water consumption. Behavioral Neuroscience 2005, 119:1235-1243.
50. Weitemier A.Z., Ryabinin A.E. Urocortin 1 in the dorsal raphe regulates food and fluid consumption, but not ethanol preference in C57BL/6J mice. Neuroscience 2006, 137:1439-1445.
51. Weitemier A.Z., Tsivkovskaia N.O., Ryabinin A.E. Urocortin 1 distribution in mouse brain is strain-dependent. Neuroscience 2005, 132:729-740.