Stress and VTA synapses: Implications for addiction and depression

European Journal of Neuroscience

Volumn 39, Issue 7, 2014, Pages 1179-1188

  Polter, Abigail M ^a   Kauer, Julie A ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Depression; Dopamine; Reward; Synaptic plasticity; Ventral tegmental area

Indexed keywords

ADDICTION; ANXIETY DISORDER; ARTICLE; COMORBIDITY; DEPRESSION; HEALTH STATUS; HUMAN; LIFE STRESS; MENTAL DISEASE; MOOD DISORDER; NONHUMAN; PRIORITY JOURNAL; RISK ASSESSMENT; SUBSTANCE ABUSE; SYNAPSE; VENTRAL TEGMENTUM; ANIMAL; CYTOLOGY; MENTAL STRESS; METABOLISM; NERVE CELL PLASTICITY; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; DEPRESSIVE DISORDER; HUMANS; NEURONAL PLASTICITY; STRESS, PSYCHOLOGICAL; SUBSTANCE-RELATED DISORDERS; SYNAPSES; VENTRAL TEGMENTAL AREA;

EID: 84898742123     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12490     Document Type: Article

References (160)

1. Ambroggi, F., Turiault, M., Milet, A., Deroche-Gamonet, V., Parnaudeau, S., Balado, E., Barik, J., van der Veen, R., Maroteaux, G., Lemberger, T., Schutz, G., Lazar, M., Marinelli, M., Piazza, P.V. & Tronche, F. (2009) Stress and addiction: glucocorticoid receptor in dopaminoceptive neurons facilitates cocaine seeking. Nat. Neurosci., 12, 247-249.
2. Anstrom, K.K. & Woodward, D.J. (2005) Restraint increases dopaminergic burst firing in awake rats. Neuropsychopharmacology, 30, 1832-1840.
3. Argilli, E., Sibley, D.R., Malenka, R.C., England, P.M. & Bonci, A. (2008) Mechanism and time course of cocaine-induced long-term potentiation in the ventral tegmental area. J. Neurosci., 28, 9092-9100.
4. Arvidsson, U., Riedl, M., Chakrabarti, S., Vulchanova, L., Lee, J.H., Nakano, A.H., Lin, X., Loh, H.H., Law, P.Y., Wessendorf, M.W. & Elde, R. (1995) The kappa-opioid receptor is primarily postsynaptic: combined immunohistochemical localization of the receptor and endogenous opioids. Proc. Natl. Acad. Sci. USA, 92, 5062-5066.
5. Autry, A.E., Adachi, M., Nosyreva, E., Na, E.S., Los, M.F., Cheng, P.F., Kavalali, E.T. & Monteggia, L.M. (2011) NMDA receptor blockade at rest triggers rapid behavioural antidepressant responses. Nature, 475, 91-95.
6. Bale, T.L. & Vale, W.W. (2004) CRF and CRF receptors: role in stress responsivity and other behaviors. Annu. Rev. Pharmacol., 44, 525-557.
7. Bals-Kubik, R., Ableitner, A., Herz, A. & Shippenberg, T.S. (1993) Neuroanatomical sites mediating the motivational effects of opioids as mapped by the conditioned place preference paradigm in rats. J. Pharmacol. Exp. Ther., 264, 489-495.
8. Beardsley, P.M., Howard, J.L., Shelton, K.L. & Carroll, F.I. (2005) Differential effects of the novel kappa opioid receptor antagonist, JDTic, on reinstatement of cocaine-seeking induced by footshock stressors vs cocaine primes and its antidepressant-like effects in rats. Psychopharmacology, 183, 118-126.
9. Beardsley, P.M., Pollard, G.T., Howard, J.L. & Carroll, F.I. (2010) Effectiveness of analogs of the kappa opioid receptor antagonist (3R)-7-hydroxy-N-((1S)-1-{[(3R, 4R)-4-(3-hydroxyphenyl)-3, 4-dimethyl-1-piperidinyl]methyl}-2-methylpropyl)-1, 2, 3, 4-tetrahydro-3-isoquinolinecarboxamide (JDTic) to reduce U50, 488-induced diuresis and stress-induced cocaine reinstatement in rats. Psychopharmacology, 210, 189-198.
10. Becker, H.C., Lopez, M.F. & Doremus-Fitzwater, T.L. (2011) Effects of stress on alcohol drinking: a review of animal studies. Psychopharmacology, 218, 131-156.
11. Bellone, C. & Luscher, C. (2006) Cocaine triggered AMPA receptor redistribution is reversed in vivo by mGluR-dependent long-term depression. Nat. Neurosci., 9, 636-641.
12. Berton, O., McClung, C.A., Dileone, R.J., Krishnan, V., Renthal, W., Russo, S.J., Graham, D., Tsankova, N.M., Bolanos, C.A., Rios, M., Monteggia, L.M., Self, D.W. & Nestler, E.J. (2006) Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science, 311, 864-868.
13. Bocklisch, C., Pascoli, V., Wong, J.C., House, D.R., Yvon, C., de Roo, M., Tan, K.R. & Luscher, C. (2013) Cocaine disinhibits dopamine neurons by potentiation of GABA transmission in the ventral tegmental area. Science, 341, 1521-1525.
14. Borgland, S.L., Malenka, R.C. & Bonci, A. (2004) Acute and chronic cocaine-induced potentiation of synaptic strength in the ventral tegmental area: electrophysiological and behavioral correlates in individual rats. J. Neurosci., 24, 7482-7490.
15. Boyce-Rustay, J.M., Cameron, H.A. & Holmes, A. (2007) Chronic swim stress alters sensitivity to acute behavioral effects of ethanol in mice. Physiol. Behav., 91, 77-86.
16. Briand, L.A., Vassoler, F.M., Pierce, R.C., Valentino, R.J. & Blendy, J.A. (2010) Ventral tegmental afferents in stress-induced reinstatement: the role of cAMP response element-binding protein. J. Neurosci., 30, 16149-16159.
17. Brischoux, F., Chakraborty, S., Brierley, D.I. & Ungless, M.A. (2009) Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proc. Natl. Acad. Sci. USA, 106, 4894-4899.
18. Brown, M.T., Tan, K.R., O'Connor, E.C., Nikonenko, I., Muller, D. & Luscher, C. (2012) Ventral tegmental area GABA projections pause accumbal cholinergic interneurons to enhance associative learning. Nature, 492, 452-456.
19. Bruchas, M.R., Land, B.B. & Chavkin, C. (2010) The dynorphin/kappa opioid system as a modulator of stress-induced and pro-addictive behaviors. Brain Res., 1314, 44-55.
20. Butts, K.A. & Phillips, A.G. (2013) Glucocorticoid receptors in the prefrontal cortex regulate dopamine efflux to stress via descending glutamatergic feedback to the ventral tegmental area. Int. J. Neuropsychoph., 16, 1799-1807.
21. Cao, J.L., Covington, H.E. 3rd., Friedman, A.K., Wilkinson, M.B., Walsh, J.J., Cooper, D.C., Nestler, E.J. & Han, M.H. (2010) Mesolimbic dopamine neurons in the brain reward circuit mediate susceptibility to social defeat and antidepressant action. J. Neurosci., 30, 16453-16458.
22. Carey, A.N., Borozny, K., Aldrich, J.V. & McLaughlin, J.P. (2007) Reinstatement of cocaine place-conditioning prevented by the peptide kappa-opioid receptor antagonist arodyn. Eur. J. Pharmacol., 569, 84-89.
23. Chartoff, E.H., Papadopoulou, M., MacDonald, M.L., Parsegian, A., Potter, D., Konradi, C. & Carlezon, W.A. Jr. (2009) Desipramine reduces stress-activated dynorphin expression and CREB phosphorylation in NAc tissue. Mol. Pharmacol., 75, 704-712.
24. Chaudhury, D., Walsh, J.J., Friedman, A.K., Juarez, B., Ku, S.M., Koo, J.W., Ferguson, D., Tsai, H.C., Pomeranz, L., Christoffel, D.J., Nectow, A.R., Ekstrand, M., Domingos, A., Mazei-Robison, M.S., Mouzon, E., Lobo, M.K., Neve, R.L., Friedman, J.M., Russo, S.J., Deisseroth, K., Nestler, E.J. & Han, M.H. (2013) Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature, 493, 532-536.
25. Chen, B.T., Bowers, M.S., Martin, M., Hopf, F.W., Guillory, A.M., Carelli, R.M., Chou, J.K. & Bonci, A. (2008) Cocaine but not natural reward self-administration nor passive cocaine infusion produces persistent LTP in the VTA. Neuron, 59, 288-297.
26. Conrad, K.L., Tseng, K.Y., Uejima, J.L., Reimers, J.M., Heng, L.J., Shaham, Y., Marinelli, M. & Wolf, M.E. (2008) Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature, 454, 118-121.
27. Conrad, K.L., McCutcheon, J.E., Cotterly, L.M., Ford, K.A., Beales, M. & Marinelli, M. (2010) Persistent increases in cocaine-seeking behavior after acute exposure to cold swim stress. Biol. Psychiat., 68, 303-305.
28. Covington, H.E. 3rd. & Miczek, K.A. (2001) Repeated social-defeat stress, cocaine or morphine. Effects on behavioral sensitization and intravenous cocaine self-administration "binges". Psychopharmacology, 158, 388-398.
29. Covington, H.E. 3rd. & Miczek, K.A. (2005) Intense cocaine self-administration after episodic social defeat stress, but not after aggressive behavior: dissociation from corticosterone activation. Psychopharmacology, 183, 331-340.
30. Covington, H.E. 3rd., Tropea, T.F., Rajadhyaksha, A.M., Kosofsky, B.E. & Miczek, K.A. (2008) NMDA receptors in the rat VTA: a critical site for social stress to intensify cocaine taking. Psychopharmacology, 197, 203-216.
31. Croft, A.P., Brooks, S.P., Cole, J. & Little, H.J. (2005) Social defeat increases alcohol preference of C57BL/10 strain mice; effect prevented by a CCKB antagonist. Psychopharmacology, 183, 163-170.
32. Daftary, S.S., Panksepp, J., Dong, Y. & Saal, D.B. (2009) Stress-induced, glucocorticoid-dependent strengthening of glutamatergic synaptic transmission in midbrain dopamine neurons. Neurosci. Lett., 452, 273-276.
33. Di Chiara, G. & Imperato, A. (1988) Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc. Natl. Acad. Sci. USA, 85, 5274-5278.
34. Dong, H.W. & Swanson, L.W. (2003) Projections from the rhomboid nucleus of the bed nuclei of the stria terminalis: implications for cerebral hemisphere regulation of ingestive behaviors. J. Comp. Neurol., 463, 434-472.
35. Dong, Y., Saal, D., Thomas, M., Faust, R., Bonci, A., Robinson, T. & Malenka, R.C. (2004) Cocaine-induced potentiation of synaptic strength in dopamine neurons: behavioral correlates in GluRA(-/-) mice. Proc. Natl. Acad. Sci. USA, 101, 14282-14287.
36. Dong, L., Bilbao, A., Laucht, M., Henriksson, R., Yakovleva, T., Ridinger, M., Desrivieres, S., Clarke, T.K., Lourdusamy, A., Smolka, M.N., Cichon, S., Blomeyer, D., Treutlein, J., Perreau-Lenz, S., Witt, S., Leonardi-Essmann, F., Wodarz, N., Zill, P., Soyka, M., Albrecht, U., Rietschel, M., Lathrop, M., Bakalkin, G., Spanagel, R. & Schumann, G. (2011) Effects of the circadian rhythm gene period 1 (per1) on psychosocial stress-induced alcohol drinking. Am. J. Psychiat., 168, 1090-1098.
37. El Mestikawy, S., Wallen-Mackenzie, A., Fortin, G.M., Descarries, L. & Trudeau, L.E. (2011) From glutamate co-release to vesicular synergy: vesicular glutamate transporters. Nat. Rev. Neurosci., 12, 204-216.
38. Erb, S., Shaham, Y. & Stewart, J. (1996) Stress reinstates cocaine-seeking behavior after prolonged extinction and a drug-free period. Psychopharmacology, 128, 408-412.
39. Faleiro, L.J., Jones, S. & Kauer, J.A. (2003) Rapid AMPAR/NMDAR response to amphetamine: a detectable increase in AMPAR/NMDAR ratios in the ventral tegmental area is detectable after amphetamine injection. Ann. NY Acad. Sci., 1003, 391-394.
40. Fallon, J.H., Leslie, F.M. & Cone, R.I. (1985) Dynorphin-containing pathways in the substantia nigra and ventral tegmentum: a double labeling study using combined immunofluorescence and retrograde tracing. Neuropeptides, 5, 457-460.
41. Fields, H.L., Hjelmstad, G.O., Margolis, E.B. & Nicola, S.M. (2007) Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu. Rev. Neurosci., 30, 289-316.
42. Fitzgerald, L.W., Ortiz, J., Hamedani, A.G. & Nestler, E.J. (1996) 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, 274-282.
43. Ford, C.P., Mark, G.P. & Williams, J.T. (2006) Properties and opioid inhibition of mesolimbic dopamine neurons vary according to target location. J. Neurosci., 26, 2788-2797.
44. Ford, C.P., Beckstead, M.J. & Williams, J.T. (2007) Kappa opioid inhibition of somatodendritic dopamine inhibitory postsynaptic currents. J. Neurophysiol., 97, 883-891.
45. Gariano, R.F. & Groves, P.M. (1988) Burst firing induced in midbrain dopamine neurons by stimulation of the medial prefrontal and anterior cingulate cortices. Brain Res., 462, 194-198.
46. Goeders, N.E. & Guerin, G.F. (1994) Non-contingent electric footshock facilitates the acquisition of intravenous cocaine self-administration in rats. Psychopharmacology, 114, 63-70.
47. Goncalves, L., Sego, C. & Metzger, M. (2012) Differential projections from the lateral habenula to the rostromedial tegmental nucleus and ventral tegmental area in the rat. J. Comp. Neurol., 520, 1278-1300.
48. Graziane, N.M., Polter, A.M., Briand, L.A., Pierce, R.C. & Kauer, J.A. (2013) Kappa opioid receptors regulate stress-induced cocaine seeking and synaptic plasticity. Neuron, 77, 942-954.
49. Hadaway, P.F., Alexander, B.K., Coambs, R.B. & Beyerstein, B. (1979) The effect of housing and gender on preference for morphine-sucrose solutions in rats. Psychopharmacology, 66, 87-91.
50. Hahn, J., Hopf, F.W. & Bonci, A. (2009) Chronic cocaine enhances corticotropin-releasing factor-dependent potentiation of excitatory transmission in ventral tegmental area dopamine neurons. J. Neurosci., 29, 6535-6544.
51. Haney, M., Maccari, S., Le Moal, M., Simon, H. & Piazza, P.V. (1995) Social stress increases the acquisition of cocaine self-administration in male and female rats. Brain Res., 698, 46-52.
52. Hjelmstad, G.O., Xia, Y., Margolis, E.B. & Fields, H.L. (2013) Opioid modulation of ventral pallidal afferents to ventral tegmental area neurons. J. Neurosci., 33, 6454-6459.
53. Hnasko, T.S., Hjelmstad, G.O., Fields, H.L. & Edwards, R.H. (2012) Ventral tegmental area glutamate neurons: electrophysiological properties and projections. J. Neurosci., 32, 15076-15085.
54. Ishikawa, M., Otaka, M., Huang, Y.H., Neumann, P.A., Winters, B.D., Grace, A.A., Schluter, O.M. & Dong, Y. (2013a) Dopamine triggers heterosynaptic plasticity. J. Neurosci., 33, 6759-6765.
55. Ishikawa, M., Otaka, M., Neumann, P., Wang, Z., Cook, J., Schlueter, O., Dong, Y. & Huang, Y. (2013b) Exposure to cocaine regulates inhibitory synaptic transmission from the ventral tegmental area to nucleus accumbens. J. Physiol., 591, 4827-4841.
56. Jennings, J.H., Sparta, D.R., Stamatakis, A.M., Ung, R.L., Pleil, K.E., Kash, T.L. & Stuber, G.D. (2013) Distinct extended amygdala circuits for divergent motivational states. Nature, 496, 224-228.
57. Johnson, S.W. & North, R.A. (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J. Neurosci., 12, 483-488.
58. Johnson, S.W., Seutin, V. & North, R.A. (1992) Burst firing in dopamine neurons induced by N-methyl-D-aspartate: role of electrogenic sodium pump. Science, 258, 665-667.
59. Kalivas, P.W., Duffy, P. & Eberhardt, H. (1990) Modulation of A10 dopamine neurons by gamma-aminobutyric acid agonists. J. Pharmacol. Exp. Ther., 253, 858-866.
60. Kalivas, P.W., Churchill, L. & Klitenick, M.A. (1993) GABA and enkephalin projection from the nucleus accumbens and ventral pallidum to the ventral tegmental area. Neuroscience, 57, 1047-1060.
61. Kallupi, M., Wee, S., Edwards, S., Whitfield, T.W. Jr., Oleata, C.S., Luu, G., Schmeichel, B.E., Koob, G.F. & Roberto, M. (2013) Kappa opioid receptor-mediated dysregulation of gamma-aminobutyric acidergic transmission in the central amygdala in cocaine addiction. Biol. Psychiat., 74, 520-528.
62. Kauer, J.A. & Malenka, R.C. (2007) Synaptic plasticity and addiction. Nat. Rev. Neurosci., 8, 844-858.
63. Kelley, A.E. & Berridge, K.C. (2002) The neuroscience of natural rewards: relevance to addictive drugs. J. Neurosci., 22, 3306-3311.
64. Kempadoo, K.A., Tourino, C., Cho, S.L., Magnani, F., Leinninger, G.M., Stuber, G.D., Zhang, F., Myers, M.G., Deisseroth, K., de Lecea, L. & Bonci, A. (2013) Hypothalamic neurotensin projections promote reward by enhancing glutamate transmission in the VTA. J. Neurosci., 33, 7618-7626.
65. Klitenick, M.A., DeWitte, P. & Kalivas, P.W. (1992) Regulation of somatodendritic dopamine release in the ventral tegmental area by opioids and GABA: an in vivo microdialysis study. J. Neurosci., 12, 2623-2632.
66. Koob, G. & Kreek, M.J. (2007) Stress, dysregulation of drug reward pathways, and the transition to drug dependence. Am. J. Psychiat., 164, 1149-1159.
67. Koob, G.F. & Volkow, N.D. (2010) Neurocircuitry of addiction. Neuropsychopharmacology, 35, 217-238.
68. Kopp, C., Longordo, F. & Luthi, A. (2007) Experience-dependent changes in NMDA receptor composition at mature central synapses. Neuropharmacology, 53, 1-9.
69. Korotkova, T.M., Brown, R.E., Sergeeva, O.A., Ponomarenko, A.A. & Haas, H.L. (2006) Effects of arousal- and feeding-related neuropeptides on dopaminergic and GABAergic neurons in the ventral tegmental area of the rat. Eur. J. Neurosci., 23, 2677-2685.
70. Kosten, T.A., Miserendino, M.J. & Kehoe, P. (2000) Enhanced acquisition of cocaine self-administration in adult rats with neonatal isolation stress experience. Brain Res., 875, 44-50.
71. Krishnan, V., Han, M.H., Graham, D.L., Berton, O., Renthal, W., Russo, S.J., Laplant, Q., Graham, A., Lutter, M., Lagace, D.C., Ghose, S., Reister, R., Tannous, P., Green, T.A., Neve, R.L., Chakravarty, S., Kumar, A., Eisch, A.J., Self, D.W., Lee, F.S., Tamminga, C.A., Cooper, D.C., Gershenfeld, H.K. & Nestler, E.J. (2007) Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell, 131, 391-404.
72. Lammel, S., Hetzel, A., Hackel, O., Jones, I., Liss, B. & Roeper, J. (2008) Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron, 57, 760-773.
73. Lammel, S., Ion, D.I., Roeper, J. & Malenka, R.C. (2011) Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron, 70, 855-862.
74. Lammel, S., Lim, B.K., Ran, C., Huang, K.W., Betley, M.J., Tye, K.M., Deisseroth, K. & Malenka, R.C. (2012) Input-specific control of reward and aversion in the ventral tegmental area. Nature, 491, 212-217.
75. Lammel, S., Lim, B.K. & Malenka, R.C. (2014) Reward and aversion in a heterogeneous midbrain dopamine system. Neuropharmacology, 76, 351-359.
76. Land, B.B., Bruchas, M.R., Lemos, J.C., Xu, M., Melief, E.J. & Chavkin, C. (2008) The dysphoric component of stress is encoded by activation of the dynorphin kappa-opioid system. J. Neurosci., 28, 407-414.
77. Land, B.B., Bruchas, M.R., Schattauer, S., Giardino, W.J., Aita, M., Messinger, D., Hnasko, T.S., Palmiter, R.D. & Chavkin, C. (2009) Activation of the kappa opioid receptor in the dorsal raphe nucleus mediates the aversive effects of stress and reinstates drug seeking. Proc. Natl. Acad. Sci. USA, 106, 19168-19173.
78. Le, A.D., Quan, B., Juzytch, W., Fletcher, P.J., Joharchi, N. & Shaham, Y. (1998) Reinstatement of alcohol-seeking by priming injections of alcohol and exposure to stress in rats. Psychopharmacology, 135, 169-174.
79. Li, N., Lee, B., Liu, R.J., Banasr, M., Dwyer, J.M., Iwata, M., Li, X.Y., Aghajanian, G. & Duman, R.S. (2010) mTOR-dependent synapse formation underlies the rapid antidepressant effects of NMDA antagonists. Science, 329, 959-964.
80. Li, B., Piriz, J., Mirrione, M., Chung, C., Proulx, C.D., Schulz, D., Henn, F. & Malinow, R. (2011) Synaptic potentiation onto habenula neurons in the learned helplessness model of depression. Nature, 470, 535-539.
81. Loweth, J.A., Scheyer, A.F., Milovanovic, M., Lacrosse, A.L., Flores-Barrera, E., Werner, C.T., Li, X., Ford, K.A., Le, T., Olive, M.F., Szumlinski, K.K., Tseng, K.Y. & Wolf, M.E. (2014) Synaptic depression via mGluR1 positive allosteric modulation suppresses cue-induced cocaine craving. Nat. Neurosci., 17, 73-78.
82. Luscher, C. & Malenka, R.C. (2011) Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron, 69, 650-663.
83. Mameli, M., Balland, B., Lujan, R. & Luscher, C. (2007) Rapid synthesis and synaptic insertion of GluR2 for mGluR-LTD in the ventral tegmental area. Science, 317, 530-533.
84. Mameli, M., Bellone, C., Brown, M.T. & Luscher, C. (2011) Cocaine inverts rules for synaptic plasticity of glutamate transmission in the ventral tegmental area. Nat. Neurosci., 14, 414-416.
85. Mansour, A., Burke, S., Pavlic, R.J., Akil, H. & Watson, S.J. (1996) Immunohistochemical localization of the cloned kappa 1 receptor in the rat CNS and pituitary. Neuroscience, 71, 671-690.
86. Mansvelder, H.D. & McGehee, D.S. (2000) Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron, 27, 349-357.
87. Margolis, E.B., Hjelmstad, G.O., Bonci, A. & Fields, H.L. (2005) Both kappa and mu opioid agonists inhibit glutamatergic input to ventral tegmental area neurons. J. Neurophysiol., 93, 3086-3093.
88. Margolis, E.B., Lock, H., Chefer, V.I., Shippenberg, T.S., Hjelmstad, G.O. & Fields, H.L. (2006) Kappa opioids selectively control dopaminergic neurons projecting to the prefrontal cortex. Proc. Natl. Acad. Sci. USA, 103, 2938-2942.
89. Margolis, E.B., Mitchell, J.M., Ishikawa, J., Hjelmstad, G.O. & Fields, H.L. (2008) Midbrain dopamine neurons: projection target determines action potential duration and dopamine D(2) receptor inhibition. J. Neurosci., 28, 8908-8913.
90. Margolis, E.B., Mitchell, J.M., Hjelmstad, G.O. & Fields, H.L. (2011) A novel opioid receptor-mediated enhancement of GABAA receptor function induced by stress in ventral tegmental area neurons. J. Physiol., 589, 4229-4242.
91. Mathews, D.C. & Zarate, C.A. Jr. (2013) Current status of ketamine and related compounds for depression. J. Clin. Psychiat., 74, 516-517.
92. McFarland, K., Davidge, S.B., Lapish, C.C. & Kalivas, P.W. (2004) Limbic and motor circuitry underlying footshock-induced reinstatement of cocaine-seeking behavior. J. Neurosci., 24, 1551-1560.
93. McLaughlin, J.P., Marton-Popovici, M. & Chavkin, C. (2003) Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J. Neurosci., 23, 5674-5683.
94. McLaughlin, J.P., Land, B.B., Li, S., Pintar, J.E. & Chavkin, C. (2006) Prior activation of kappa opioid receptors by U50, 488 mimics repeated forced swim stress to potentiate cocaine place preference conditioning. Neuropsychopharmacology, 31, 787-794.
95. Meredith, G.E. (1999) The synaptic framework for chemical signaling in nucleus accumbens. Ann. NY Acad. Sci., 877, 140-156.
96. Mereu, G., Lilliu, V., Casula, A., Vargiu, P.F., Diana, M., Musa, A. & Gessa, G.L. (1997) Spontaneous bursting activity of dopaminergic neurons in midbrain slices from immature rats: role of N-methyl-D-aspartate receptors. Neuroscience, 77, 1029-1036.
97. Miczek, K.A. & Mutschler, N.H. (1996) Activational effects of social stress on IV cocaine self-administration in rats. Psychopharmacology, 128, 256-264.
98. Miczek, K.A., Yap, J.J. & Covington, H.E. 3rd. (2008) Social stress, therapeutics and drug abuse: preclinical models of escalated and depressed intake. Pharmacol. Therapeut., 120, 102-128.
99. Moffett, M.C., Vicentic, A., Kozel, M., Plotsky, P., Francis, D.D. & Kuhar, M.J. (2007) Maternal separation alters drug intake patterns in adulthood in rats. Biochem. Pharmacol., 73, 321-330.
100. Murase, S., Grenhoff, J., Chouvet, G., Gonon, F.G. & Svensson, T.H. (1993) Prefrontal cortex regulates burst firing and transmitter release in rat mesolimbic dopamine neurons studied in vivo. Neurosci. Lett., 157, 53-56.
101. Nabeshima, T., Katoh, A., Wada, M. & Kameyama, T. (1992) Stress-induced changes in brain Met-enkephalin, Leu-enkephalin and dynorphin concentrations. Life Sci., 51, 211-217.
102. Nair-Roberts, R.G., Chatelain-Badie, S.D., Benson, E., White-Cooper, H., Bolam, J.P. & Ungless, M.A. (2008) Stereological estimates of dopaminergic, GABAergic and glutamatergic neurons in the ventral tegmental area, substantia nigra and retrorubral field in the rat. Neuroscience, 152, 1024-1031.
103. Nauta, W.J., Smith, G.P., Faull, R.L. & Domesick, V.B. (1978) Efferent connections and nigral afferents of the nucleus accumbens septi in the rat. Neuroscience, 3, 385-401.
104. Nestler, E.J. & Carlezon, W.A. Jr. (2006) The mesolimbic dopamine reward circuit in depression. Biol. Psychiat., 59, 1151-1159.
105. Niehaus, J., Murali, M. & Kauer, J. (2010) Drugs of abuse and stress impair LTP at inhibitory synapses in the ventral tegmental area. Eur. J. Neurosci., 32, 108-117.
106. Nugent, F., Penick, E. & Kauer, J. (2007) Opioids block long-term potentiation of inhibitory synapses. Nature, 446, 1086-1090.
107. Nugent, F.S., Niehaus, J.L. & Kauer, J.A. (2009) PKG and PKA signaling in LTP at GABAergic synapses. Neuropsychopharmacology, 34, 1829-1842.
108. Paladini, C.A. & Tepper, J.M. (1999) GABA(A) and GABA(B) antagonists differentially affect the firing pattern of substantia nigra dopaminergic neurons in vivo. Synapse, 32, 165-176.
109. Piazza, P.V. & Le Moal, M.L. (1996) Pathophysiological basis of vulnerability to drug abuse: role of an interaction between stress, glucocorticoids, and dopaminergic neurons. Annu. Rev. Pharmacol., 36, 359-378.
110. Piazza, P.V., Deminiere, J.M., le Moal, M. & Simon, H. (1990) Stress- and pharmacologically-induced behavioral sensitization increases vulnerability to acquisition of amphetamine self-administration. Brain Res., 514, 22-26.
111. Poulin, J.F., Arbour, D., Laforest, S. & Drolet, G. (2009) Neuroanatomical characterization of endogenous opioids in the bed nucleus of the stria terminalis. Prog. Neuropsychoph., 33, 1356-1365.
112. Quinlan, E.M., Olstein, D.H. & Bear, M.F. (1999) Bidirectional, experience-dependent regulation of N-methyl-D-aspartate receptor subunit composition in the rat visual cortex during postnatal development. Proc. Natl. Acad. Sci. USA, 96, 12876-12880.
113. Ramsey, N.F. & Van Ree, J.M. (1993) Emotional but not physical stress enhances intravenous cocaine self-administration in drug-naive rats. Brain Res., 608, 216-222.
114. Razzoli, M., Andreoli, M., Michielin, F., Quarta, D. & Sokal, D.M. (2011) Increased phasic activity of VTA dopamine neurons in mice 3 weeks after repeated social defeat. Behav. Brain Res., 218, 253-257.
115. Redila, V.A. & Chavkin, C. (2008) Stress-induced reinstatement of cocaine seeking is mediated by the kappa opioid system. Psychopharmacology, 200, 59-70.
116. Robinson, T.E. & Berridge, K.C. (2000) The psychology and neurobiology of addiction: an incentive-sensitization view. Addiction, 95(Suppl 2), S91-S117.
117. Rodaros, D., Caruana, D.A., Amir, S. & Stewart, J. (2007) Corticotropin-releasing factor projections from limbic forebrain and paraventricular nucleus of the hypothalamus to the region of the ventral tegmental area. Neuroscience, 150, 8-13.
118. Russo, S.J., Murrough, J.W., Han, M.H., Charney, D.S. & Nestler, E.J. (2012) Neurobiology of resilience. Nat. Neurosci., 15, 1475-1484.
119. Saal, D., Dong, Y., Bonci, A. & Malenka, R.C. (2003) Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron, 37, 577-582.
120. Sarnyai, Z., Shaham, Y. & Heinrichs, S.C. (2001) The role of corticotropin-releasing factor in drug addiction. Pharmacol. Rev., 53, 209-243.
121. Sartorius, A., Kiening, K.L., Kirsch, P., von Gall, C.C., Haberkorn, U., Unterberg, A.W., Henn, F.A. & Meyer-Lindenberg, A. (2010) Remission of major depression under deep brain stimulation of the lateral habenula in a therapy-refractory patient. Biol. Psychiat., 67, e9-e11.
122. Sesack, S.R. & Grace, A.A. (2010) Cortico-Basal Ganglia reward network: microcircuitry. Neuropsychopharmacology, 35, 27-47.
123. Shaham, Y. & Stewart, J. (1994) Exposure to mild stress enhances the reinforcing efficacy of intravenous heroin self-administration in rats. Psychopharmacology, 114, 523-527.
124. Shaham, Y. & Stewart, J. (1995) Stress reinstates heroin-seeking in drug-free animals: an effect mimicking heroin, not withdrawal. Psychopharmacology, 119, 334-341.
125. Shaham, Y., Rodaros, D. & Stewart, J. (1994) Reinstatement of heroin-reinforced behavior following long-term extinction: implications for the treatment of relapse to drug taking. Behav. Pharmacol., 5, 360-364.
126. Shaham, Y., Shalev, U., Lu, L., De Wit, H. & Stewart, J. (2003) The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology, 168, 3-20.
127. Sinha, R. (2001) How does stress increase risk of drug abuse and relapse? Psychopharmacology, 158, 343-359.
128. Sinha, R. (2008) Chronic stress, drug use, and vulnerability to addiction. Ann. NY Acad. Sci., 1141, 105-130.
129. Speciale, S.G., Manaye, K.F., Sadeq, M. & German, D.C. (1993) Opioid receptors in midbrain dopaminergic regions of the rat. II. Kappa and delta receptor autoradiography. J. Neural Transm. Gen., 91, 53-66.
130. Sperling, R.E., Gomes, S.M., Sypek, E.I., Carey, A.N. & McLaughlin, J.P. (2010) Endogenous kappa-opioid mediation of stress-induced potentiation of ethanol-conditioned place preference and self-administration. Psychopharmacology, 210, 199-209.
131. Stamatakis, A.M. & Stuber, G.D. (2012) Activation of lateral habenula inputs to the ventral midbrain promotes behavioral avoidance. Nat. Neurosci., 15, 1105-1107.
132. Stamatakis, A.M., Jennings, J.H., Ung, R.L., Blair, G.A., Weinberg, R.J., Neve, R.L., Boyce, F., Mattis, J., Ramakrishnan, C., Deisseroth, K. & Stuber, G.D. (2013) A unique population of ventral tegmental area neurons inhibits the lateral habenula to promote reward. Neuron, 80, 1039-1053.
133. Stuber, G.D., Hnasko, T.S., Britt, J.P., Edwards, R.H. & Bonci, A. (2010) Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J. Neurosci., 30, 8229-8233.
134. Tagliaferro, P. & Morales, M. (2008) Synapses between corticotropin-releasing factor-containing axon terminals and dopaminergic neurons in the ventral tegmental area are predominantly glutamatergic. J. Comp. Neurol., 506, 616-626.
135. Tan, K.R., Yvon, C., Turiault, M., Mirzabekov, J.J., Doehner, J., Labouebe, G., Deisseroth, K., Tye, K.M. & Luscher, C. (2012) GABA neurons of the VTA drive conditioned place aversion. Neuron, 73, 1173-1183.
136. Tidey, J.W. & Miczek, K.A. (1996) Social defeat stress selectively alters mesocorticolimbic dopamine release: an in vivo microdialysis study. Brain Res., 721, 140-149.
137. Tidey, J.W. & Miczek, K.A. (1997) Acquisition of cocaine self-administration after social stress: role of accumbens dopamine. Psychopharmacology, 130, 203-212.
138. Tong, Z.Y., Overton, P.G. & Clark, D. (1996) Stimulation of the prefrontal cortex in the rat induces patterns of activity in midbrain dopaminergic neurons which resemble natural burst events. Synapse, 22, 195-208.
139. Tritsch, N.X., Ding, J.B. & Sabatini, B.L. (2012) Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. Nature, 490, 262-266.
140. Tsai, H.C., Zhang, F., Adamantidis, A., Stuber, G.D., Bonci, A., de Lecea, L. & Deisseroth, K. (2009) Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science, 324, 1080-1084.
141. Tye, K.M., Mirzabekov, J.J., Warden, M.R., Ferenczi, E.A., Tsai, H.C., Finkelstein, J., Kim, S.Y., Adhikari, A., Thompson, K.R., Andalman, A.S., Gunaydin, L.A., Witten, I.B. & Deisseroth, K. (2013) Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature, 493, 537-541.
142. Ungless, M.A., Whistler, J.L., Malenka, R.C. & Bonci, A. (2001) Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature, 411, 583-587.
143. Ungless, M.A., Singh, V., Crowder, T.L., Yaka, R., Ron, D. & Bonci, A. (2003) Corticotropin-releasing factor requires CRF binding protein to potentiate NMDA receptors via CRF receptor 2 in dopamine neurons. Neuron, 39, 401-407.
144. Ungless, M.A., Argilli, E. & Bonci, A. (2010) Effects of stress and aversion on dopamine neurons: implications for addiction. Neurosci. Biobehav. R., 35, 151-156.
145. Valdez, G.R., Platt, D.M., Rowlett, J.K., Ruedi-Bettschen, D. & Spealman, R.D. (2007) Kappa agonist-induced reinstatement of cocaine seeking in squirrel monkeys: a role for opioid and stress-related mechanisms. J. Pharmacol. Exp. Ther., 323, 525-533.
146. Van Pett, K., Viau, V., Bittencourt, J.C., Chan, R.K., Li, H.Y., Arias, C., Prins, G.S., Perrin, M., Vale, W. & Sawchenko, P.E. (2000) Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J. Comp. Neurol., 428, 191-212.
147. Van't Veer, A. & Carlezon, W.A. Jr. (2013) Role of kappa-opioid receptors in stress and anxiety-related behavior. Psychopharmacology, 229, 435-452.
148. Van't Veer, A., Bechtholt, A.J., Onvani, S., Potter, D., Wang, Y., Liu-Chen, L.Y., Schutz, G., Chartoff, E.H., Rudolph, U., Cohen, B.M. & Carlezon, W.A. Jr. (2013) Ablation of kappa-opioid receptors from brain dopamine neurons has anxiolytic-like effects and enhances cocaine-induced plasticity. Neuropsychopharmacology, 38, 1585-1597.
149. Volkow, N.D. & Li, T.K. (2004) Drug addiction: the neurobiology of behaviour gone awry. Nat. Rev. Neurosci., 5, 963-970.
150. Wanat, M.J., Hopf, F.W., Stuber, G.D., Phillips, P.E. & Bonci, A. (2008) Corticotropin-releasing factor increases mouse ventral tegmental area dopamine neuron firing through a protein kinase C-dependent enhancement of Ih. J. Physiol., 586, 2157-2170.
151. Wang, B., Shaham, Y., Zitzman, D., Azari, S., Wise, R.A. & You, Z.B. (2005) Cocaine experience establishes control of midbrain glutamate and dopamine by corticotropin-releasing factor: a role in stress-induced relapse to drug seeking. J. Neurosci., 25, 5389-5396.
152. Wang, B., You, Z.B., Rice, K.C. & Wise, R.A. (2007) Stress-induced relapse to cocaine seeking: roles for the CRF(2) receptor and CRF-binding protein in the ventral tegmental area of the rat. Psychopharmacology, 193, 283-294.
153. Wee, S., Orio, L., Ghirmai, S., Cashman, J.R. & Koob, G.F. (2009) Inhibition of kappa opioid receptors attenuated increased cocaine intake in rats with extended access to cocaine. Psychopharmacology, 205, 565-575.
154. Wise, R.A. & Morales, M. (2010) A ventral tegmental CRF-glutamate-dopamine interaction in addiction. Brain Res., 1314, 38-43.
155. Witten, I.B., Steinberg, E.E., Lee, S.Y., Davidson, T.J., Zalocusky, K.A., Brodsky, M., Yizhar, O., Cho, S.L., Gong, S., Ramakrishnan, C., Stuber, G.D., Tye, K.M., Janak, P.H. & Deisseroth, K. (2011) Recombinase-driver rat lines: tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron, 72, 721-733.
156. Xi, Z.X. & Stein, E.A. (1998) Nucleus accumbens dopamine release modulation by mesolimbic GABAA receptors-an in vivo electrochemical study. Brain Res., 798, 156-165.
157. Xia, Y., Driscoll, J.R., Wilbrecht, L., Margolis, E.B., Fields, H.L. & Hjelmstad, G.O. (2011) Nucleus accumbens medium spiny neurons target non-dopaminergic neurons in the ventral tegmental area. J. Neurosci., 31, 7811-7816.
158. Yuan, T., Mameli, M., EC, O.C., Dey, P.N., Verpelli, C., Sala, C., Perez-Otano, I., Luscher, C. & Bellone, C. (2013) Expression of cocaine-evoked synaptic plasticity by GluN3A-containing NMDA receptors. Neuron, 80, 1025-1038.
159. Zarate, C.A. Jr., Singh, J.B., Carlson, P.J., Brutsche, N.E., Ameli, R., Luckenbaugh, D.A., Charney, D.S. & Manji, H.K. (2006) A randomized trial of an N-methyl-D-aspartate antagonist in treatment-resistant major depression. Arch. Gen. Psychiat., 63, 856-864.
160. van Zessen, R., Phillips, J.L., Budygin, E.A. & Stuber, G.D. (2012) Activation of VTA GABA neurons disrupts reward consumption. Neuron, 73, 1184-1194.