Orexin a in the VTA is critical for the induction of synaptic plasticity and behavioral sensitization to cocaine

Neuron

Volumn 49, Issue 4, 2006, Pages 589-601

  Borgland, Stephanie L ^a   Taha, Sharif A ^a   Sarti, Federica ^a   Fields, Howard L ^a,b   Bonci, Antonello ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN FRANCISCO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COCAINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; OREXIN 1 RECEPTOR; OREXIN A; PHOSPHOLIPASE C; PROTEIN KINASE C; RECEPTOR BLOCKING AGENT;

ADDICTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SYNAPSE; VENTRAL TEGMENTUM;

ANALYSIS OF VARIANCE; ANESTHETICS, LOCAL; ANIMALS; ANIMALS, NEWBORN; BEHAVIOR, ANIMAL; BENZOXAZOLES; CALCIUM CHANNEL BLOCKERS; COCAINE; CYCLIC AMP; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ELECTRIC STIMULATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYSINE; MALE; MOTOR ACTIVITY; N-METHYLASPARTATE; NEURONAL PLASTICITY; NEURONS; NEUROPEPTIDES; PATCH-CLAMP TECHNIQUES; PROTEIN KINASE C; QUINOXALINES; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; THIONUCLEOTIDES; TIME FACTORS; TYROSINE 3-MONOOXYGENASE; UREA; VENTRAL TEGMENTAL AREA;

EID: 32344446144     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2006.01.016     Document Type: Article

References (67)

1. B.A. Baldo, R.A. Daniel, C.W. Berridge, and A.E. Kelley Overlapping distributions of orexin/hypocretin- and dopamine-β-hydroxylase immunoreactivity fibers in rat brain regions mediating arousal, motivation, and stress J. Comp. Neurol. 464 2003 220 237
2. T.A. Benke, A. Luthi, J.T. Isaac, and G.L. Collingridge Modulation of AMPA receptor unitary conductions by synaptic activity Nature 393 1998 793 797
3. S. Berberich, P. Punnakkal, V. Jensen, V. Pawlak, P.H. Seeburg, O. Hvalby, and G. Kohr Lack of NMDA receptor subtype selectivity for hippocampal long-term potentiation J. Neurosci. 25 2005 6907 6910
4. L.L. Bernardis, and L.L. Bellinger The lateral hypothalamic area revisited: ingestive behavior Neurosci. Biobehav. Rev. 20 1996 189 287
5. A. Bonci, and R.C. Malenka Properties and plasticity of excitatory synapses on dopaminergic and GABAergic cells in the ventral tegmental area J. Neurosci. 19 1999 3723 3730
6. S.L. Borgland, R. Malenka, and A. Bonci Acute and chronic cocaine-induced potentiation of synaptic strength in the VTA: electrophysiological and behavioral correlates in individual rats J. Neurosci. 24 2004 7482 7490
7. D.L. Cameron, M.W. Wessendorf, and J.T. Williams A subset of ventral tegmental area neurons is inhibited by dopamine, 5-hydroxytryptamine and opioids Neuroscience 77 1997 155 166
8. W.A. Carlezon, and E.J. Nestler Elevated levels of GluR1 in the midbrain: a trigger for sensitization to drugs of abuse? Trends Neurosci. 25 2002 610 615
9. S. Cull-Candy, S. Brickley, and M. Farrant NMDA receptor subunits: diversity, development and disease Curr. Opin. Neurobiol. 11 2001 327 335
10. L. DeLecea, T.S. Kilduff, C. Peyron, X.-B. Gao, P.E. Foye, P.E. Danielson, C. Fukuhara, E.L. Battenberg, V.T. Gautvik, and F.S. Bartless The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity Proc. Natl. Acad. Sci. USA 95 1998 322 327
11. V. Derkach, A. Barria, and T.R. Soderling Ca2+/calmodulin-kinase II enhances channel conductance of alpha-amino-3-hydroxy-5-methyl-4- isoxazolepropionate type glutamate receptors Proc. Natl. Acad. Sci. USA 96 1999 3269 3274
12. R.J. DiLeone, D. Georgescu, and E.J. Nestler Lateral hypothalamic neuropeptides in reward and drug addiction Life Sci. 73 2003 759 768
13. A.W. Dunah, R.P. Yasuda, Y.-H. Wang, J. Luo, M.I. Davila-Garcia, M. Gbadegesin, S. Vicini, and B.B. Wolfe Regional and ontogenic expression of the NMDA receptor subunit NR2D protein in rat using a subunit-specific antibody J. Neurochem. 67 1996 2335 2345
14. K. Erreger, S.M. Dravid, T.G. Banke, D.J. Wyllie, and S.F. Traynelis Subunit-specific gating controls rat NR1/NR2A and NR1/NR2B NMDA channel kinetics and synaptic signaling profiles J. Physiol. 563 2005 345 358
15. J. Fadel, and A.Y. Deutch Anatomical substrates of orexin-dopamine interactions: lateral hypothalamic projections to the ventral tegmental area Neuroscience 111 2002 379 387
16. B. Feng, H.W. Tse, D.A. Skifter, R. Morley, D.E. Jane, and D.T. Monaghan Structure-activity analysis of a novel NR2C/NR2D-preferring NMDA receptor antagonist: 1-(phenantrene-2carbonyl) piperazine-2,3-dicarboxylic acid Br. J. Pharmacol. 141 2004 508 516
17. L.W. Fitzgerald, J. Ortiz, A.G. Hamedani, and E.J. Nestler Drugs of abuse and stress increase the expression of GluR1 and NMDAR1 glutamate receptor subunits in the rat ventral tegmental area: common adaptations among cross-sensitizing agents J. Neurosci. 16 1996 274 282
18. D.K. Fong, A. Rao, F.T. Crump, and A.M. Craig Rapid synaptic modeling by protein kinase C: reciprocal translocation of NMDA receptors and calcium/calmodulin dependent kinase II J. Neurosci. 22 2002 2153 2164
19. P.A. Garris, M. Kilpatrick, M.A. Bunin, D. Michael, Q.D. Walker, and R.M. Wightman Dissociation of dopamine release in the nucleus accumbens from intracranial self-stimulation Nature 398 1999 67 69
20. D. Georgescu, V. Zachariou, M. Barrot, M. Mieda, J.T. Willie, A.J. Eisch, M. Yanagisawa, E.J. Nestler, and R.J. DiLeone Involvement of lateral hypothalamic peptide orexin in morphine dependence and withdrawal J. Neurosci. 23 2003 3106 3111
21. F.G. Gonon Non-linear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry Neuroscience 24 1988 19 28
22. D.R. Grosshans, D.A. Clayton, S.J. Coultrap, and M.D. Browning LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1 Nat. Neurosci. 5 2001 27 33
23. G.C. Harris, W. Wimmer, and G. Aston Jones A role for lateral hypothalamic orexin neurons in reward seeking Nature 437 2005 556 559
24. S.W. Johnson, and R.A. North Two types of neurone in the rat ventral tegmental area and their synaptic inputs J. Physiol. 450 1992 455 468
25. S.W. Johnson, V. Seutin, and R.A. North Burst firing in dopamine neurons induced by N-methyl-D-aspartate: role of electrogenic sodium pump Science 258 1992 665 667
26. S. Jones, and A.J. Gibb Functional NR2B- and NR2D- containing NMDA receptor channels in rat substantia nigra dopamine neurones J. Physiol. 569 2005 209 221
27. J.A. Kauer Learning mechanisms in addiction: synaptic plasticity in the ventral tegmental area as a result of exposure to drugs of abuse Annu. Rev. Physiol. 66 2004 447 475
28. J.A. Kim, K.A. Pollak, G.O. Hjelmstad, and H.L. Fields A single cocaine exposure enhances both opioid reward and aversion through a ventral tegmental area-dependent mechanism Proc. Natl. Acad. Sci. USA 101 2004 5664 5669
29. A.O. Komendantov, O.G. Komendantova, S.W. Johnson, and C. Canavier A modeling study suggests complementary roles for GABAA and NMDA receptors and the SK channel in regulating the firing pattern in midbrain dopamine neurons J. Neurophysiol. 91 2004 346 357
30. T.M. Korotkova, O.A. Sergeeva, K.S. Eriksson, H.L. Haas, and R.E. Brown Excitation of ventral tegmental area dopaminergic and nondopaminergic neurons by orexin/hypocretins J. Neurosci. 23 2003 7 11
31. M.G. Lacey, N.B. Mercuri, and R.A. North Actions of cocaine on rat dopaminergic neurons in vitro Br. J. Pharmacol. 99 1990 731 735
32. J.-Y. Lan, V.A. Skeberdis, T. Jover, S.Y. Grooms, Y. Lin, R.C. Araneda, X. Zhen, M.V.L. Bennett, and R.S. Zukin Protein kinase C modulates NMDA receptor trafficking and gating Nat. Neurosci. 4 2001 382 390
33. D.R. Levitt, and P. Teitelbaum Somnolence, akinesia, and sensory activation of motivated behavior in the lateral hypothalamic syndrome Proc. Natl. Acad. Sci. USA 72 1975 2819 2823
34. L. Liu, T.P. Wong, M.F. Pozza, K. Ligenhoehl, Y. Wang, M. Sheng, Y.P. Auberson, and Y.T. Wang Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity Science 304 2004 1021 1024
35. W. Lu, H. Man, W. Ju, W.S. Trimble, J.S. Macdonald, and Y.T. Wang Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons Neuron 29 2001 243 254
36. R. Malinow, H. Schulman, and R.W. Tsien Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP Science 245 1989 862 866
37. R. Malinow, Z.F. Mainen, and Y. Hiyashi LTP mechanisms: from silence to four lane traffic Curr. Opin. Neurobiol. 10 2000 352 357
38. E.B. Margolis, G.O. Hjelmstad, A. Bonci, and H.L. Fields k-Opioid agonists directly inhibit midbrain dopaminergic neurons J. Neurosci. 23 2003 9981 9986
39. H. Monyer, N. Burnashev, D.J. Laurie, B. Sakmann, and P.H. Seeburg Developmental and regional expression in the rat brain and functional properties of four NMDA receptors Neuron 12 1994 529 540
40. T. Nakamura, K. Uramura, T. Nambu, T. Yada, K. Goto, M. Yanagisawa, and T. Sakurai Orexin-induced hyperlocomotion and stereotypy are mediated by the dopaminergic system Brain Res. 873 2000 181 187
41. A. Nayak, D.J. Zastrow, R. Lickteig, N.R. Zahniser, and M.D. Browning Maintenance of late-phase LTP is accompanied by PKA-dependent increase in AMPA receptor synthesis Nature 394 1998 680 683
42. E.J. Nestler Molecular basis of long-term plasticity underlying addiction Nat. Rev. Neurosci. 2 2001 119 128
43. P.G. Overton, and D. Clark Iontophoretically administered drugs acting at the N-methyl-D-aspartate receptor modulate burst firing in A9 dopamine neurons in the rat Synapse 10 1992 131 140
44. P.G. Overton, and D. Clark Burst firing in midbrain dopaminergic neurons Brain Res. Brain Res. Rev. 25 1997 312 334
45. P.G. Overton, C.D. Richards, M.S. Berry, and D. Clark Long-term potentiation at excitatory amino acid synapses on midbrain dopamine neurons Neuroreport 10 1999 221 226
46. P. Paoletti, P. Ascher, and J. Neyton High-affinity zinc inhibition of NMDA NR1-NR2A receptors J. Neurosci. 17 1997 5711 5725
47. G. Paxinos, and C. Watson The Rat Brain in Sterotaxic Coordinates 1997 Academic Press New York
48. T.E. Robinson, and K.C. Berridge The neural basis of drug craving; an incentive-sensitization theory of addiction Brain Res. Brain Res. Rev. 18 1993 247 291
49. C. Rosemund, J.D. Clements, and G.L. Westbrook Non-uniform probability of glutamate release at a hippocampal synapse Science 262 1993 754 757
50. A. Routtenberg, and J. Lindy Effects of the availability of rewarding septal and hypothalamic stimulation on bar pressing for food under conditions of deprivation J. Comp. Physiol. Psychol. 65 1965 158 161
51. D. Saal, Y. Dong, A. Bonci, and R.C. Malenka Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons Neuron 37 2003 577 582
52. T. Sakurai, A. Amemiya, M. Ishii, I. Matsuzaki, R.M. Chemelli, H. Tanaka, S.C. Williams, J.A. Richardson, G.P. Kozlowski, and S. Wilson Orexin and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior Cell 92 1998 573 585
53. W. Schultz Getting formal with dopamine reward Neuron 36 2002 241 263
54. D.B. Scott, T.A. Blanpied, G.T. Swanson, C. Zhang, and M.D. Ehlers An NMDA receptor ER retention signal regulated by phosphorylation and alternative splicing J. Neurosci. 21 2001 3063 3072
55. T.S. Shippenberg, and C. Heidbreder Sensitization to the conditioned rewarding effects of cocaine: pharmacological and temporal characteristics J. Pharmacol. Exp. Ther. 273 1995 808 815
56. D.G. Standaert, C.M. Testa, A.B. Young, and J.B. Penney Organization of N-Methyl-D-Aspartate glutamate receptor gene expression in the basal ganglia of the rat J. Comp. Neurol. 343 1994 1 16
57. M.J. Thomas, C. Beurrier, A. Bonci, and R.C. Malenka Long-term depression in the nucleus accumbens: a neural correlate of behavioural sensitization to cocaine Nat. Neurosci. 4 2001 1217 1223
58. K.R. Tovar, and G.L. Westbrook Mobile NMDA receptors at hippocampal synapses Neuron 34 2002 255 264
59. M.A. Ungless, J.L. Whistler, R.C. Malenka, and A. Bonci A single cocaine exposure in vivo induces long-term potentiation in dopamine neurons Nature 411 2001 583 587
60. 2+ signaling in dopamine neurons of the ventral tegmental area Neuroreport 12 2001 1885 1889
61. L.J. Vanderschuren, and P.W. Kalivas Alterations in dopaminergic and glutamatergic transmission in the induction and expression of behavioral sensitization: a critical review of preclinical studies Psychopharmacology (Berl). 151 2000 99 120
62. M.J. Wayner, D.L. Armstrong, C.F. Phelix, and Y. Oomura Orexin-A (Hypocretin-1) and leptin enhance LTP in the dentate gyrus of rats in vivo Peptides 25 2004 991 996
63. C. Weitlauf, Y. Honse, Y. Auberson, M. Mishina, D. Lovinger, and D. Winder Activation of NR2A-containing NMDA receptors is not obligatory for NMDA-receptor dependent LTP J. Neurosci. 25 2005 8386 8390
64. R. Wise Addictive drugs and brain stimulation reward Annu. Rev. Neurosci. 19 1996 319 340
65. J.P. Wisor, S. Nishino, I. Sora, G.H. Uhl, E. Mignot, and D.M. Edgar Dopaminergic role in stimulant-induced wakefulness J. Neurosci. 21 2001 1787 1794
66. A. Yamanaka, C.T. Beuckmann, J.T. Willie, J. Hara, N. Tsujino, M. Mieda, M. Tomnaga, K. Yagami, F. Sugiyama, and K. Goto Hypothalamic orexin neurons regulate arousal according to energy balance in mice Neuron 38 2003 701 713
67. Y. Zhu, Y. Miwa, A. Yamanaka, T. Yada, M. Shibahara, Y. Abe, T. Sakurai, and K. Goto Orexin receptor type-1 couples exclusively to pertussis toxin-insensitive G-proteins, while orexin receptor type-2 couples to both pertussis toxin-sensitive and -insensitive G-proteins J. Pharmacol. Sci. 92 2003 259 266