It's MORe exciting than mu: Crosstalk between mu opioid receptors and glutamatergic transmission in the mesolimbic dopamine system

Frontiers in Pharmacology

Volumn 5 MAY, Issue , 2014, Pages

  Chartoff, Elena H ^a   Connery, Hilary S ^a  

^a MCLEAN HOSPITAL   (United States)

Author keywords

AMPA; GluR1; heroin; morphine; NMDA; opioid withdrawal syndrome; plasticity

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMPA RECEPTOR; BUPRENORPHINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DIAMORPHINE; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; GLUTAMIC ACID; GUANINE NUCLEOTIDE BINDING PROTEIN; HARKOSERIDE; LAMOTRIGINE; MEMANTINE; METHADONE; MORPHINE; MU OPIATE RECEPTOR; MU OPIATE RECEPTOR AGONIST; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NALTREXONE; TOPIRAMATE;

ANALGESIA; CLINICAL FEATURE; DRUG EFFICACY; DRUG SEEKING BEHAVIOR; EFFERENT NERVE; EMOTIONALITY; EUPHORIA; GLUTAMATERGIC TRANSMISSION; HEROIN DEPENDENCE; HUMAN; MESOLIMBIC DOPAMINERGIC SYSTEM; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; NUCLEUS ACCUMBENS; OPIATE ADDICTION; PROTEIN PROTEIN INTERACTION; PSYCHOSOCIAL CARE; REVIEW; SENSORY NERVE; SYNAPTIC TRANSMISSION; TREATMENT OUTCOME; VENTRAL TEGMENTUM; WITHDRAWAL SYNDROME;

EID: 84904684020     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2014.00116     Document Type: Review

References (252)

1. Aghajanian, G. K., Kogan, J. H., and Moghaddam, B. (1994). Opiate withdrawal increases glutamate and aspartate efflux in the locus coeruleus: an in vivo microdialysis study. Brain Res. 636, 126-130. doi: 10.1016/0006-8993(94)90186-4
2. Alderson, H. L., Parkinson, J. A., Robbins, T. W., and Everitt, B. J. (2001). The effects of excitotoxic lesions of the nucleus accumbens core or shell regions on intravenous heroin self-administration in rats. Psychopharmacology (Berl.) 153, 455-463. doi: 10.1007/s002130000634
3. Anggono, V., and Huganir, R. L. (2012). Regulation of AMPA receptor trafficking and synaptic plasticity. Curr. Opin. Neurobiol. 22, 461-469. doi: 10.1016/j.conb.2011.12.006
4. Badiani, A., Belin, D., Epstein, D., Calu, D., and Shaham, Y. (2011). Opiate versus psychostimulant addiction: the differences do matter. Nat. Rev. Neurosci. 12, 685-700. doi: 10.1038/nrn3104
5. Bailey, C. P., and Connor, M. (2005). Opioids: cellular mechanisms of tolerance and physical dependence. Curr. Opin. Pharmacol. 5, 60-68. doi: 10.1016/j.coph.2004.08.012
6. Bajo, M., Crawford, E. F., Roberto, M., Madamba, S. G., and Siggins, G. R. (2006). Chronic morphine treatment alters expression of N-methyl-D-aspartate receptor subunits in the extended amygdala. J. Neurosci. Res. 83, 532-537. doi: 10.1002/jnr.20756
7. Beattie, E. C., Carroll, R. C., Yu, X., Morishita, W., Yasuda, H., Von Zastrow, M., et al. (2000). Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat. Neurosci. 3, 1291-1300. doi: 10.1038/81823
8. Becerra, L., Breiter, H. C., Wise, R., Gonzalez, R. G., and Borsook, D. (2001). Reward circuitry activation by noxious thermal stimuli. Neuron 32, 927-946. doi: 10.1016/S0896-6273(01)00533-5
9. Beguin, C., Potter, D. N., Carlezon, W. A. Jr., Stohr, T., and Cohen, B. M. (2012). Effects of the anticonvulsant lacosamide compared to valproate and lamotrigine on cocaine-enhanced reward in rats. Brain Res. 1479, 44-51. doi: 10.1016/j.brainres.2012.08.030
10. Berendse, H. W., Galis-De Graaf, Y., and Groenewegen, H. J. (1992). Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J. Comp. Neurol. 316, 314-347. doi: 10.1002/cne.903160305
11. Berendse, H. W., and Groenewegen, H. J. (1990). Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum. J. Comp. Neurol. 299, 187-228. doi: 10.1002/cne.902990206
12. Berridge, K. C., and Robinson, T. E. (1998). What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Brain Res. Rev. 28, 309-369. doi: 10.1016/S0165-0173(98)00019-8
13. Beyreuther, B. K., Freitag, J., Heers, C., Krebsfanger, N., Scharfenecker, U., and Stohr, T. (2007). Lacosamide: a review of preclinical properties. CNS Drug Rev. 13, 21-42. doi: 10.1111/j.1527-3458.2007.00001.x
14. Bisaga, A., Comer, S. D., Ward, A. S., Popik, P., Kleber, H. D., and Fischman, M. W. (2001). The NMDA antagonist memantine attenuates the expression of opioid physical dependence in humans. Psychopharmacology (Berl.) 157, 1-10. doi: 10.1007/s002130100739
15. Bonci, A., and Williams, J. T. (1996). A common mechanism mediates long-term changes in synaptic transmission after chronic cocaine and morphine. Neuron 16, 631-639. doi: 10.1016/S0896-6273(00)80082-3
16. Bonci, A., and Williams, J. T. (1997). Increased probability of GABA release during withdrawal from morphine. J. Neurosci. 17, 796-803.
17. Bossert, J. M., Gray, S. M., Lu, L., and Shaham, Y. (2006). Activation of group II metabotropic glutamate receptors in the nucleus accumbens shell attenuates context-induced relapse to heroin seeking. Neuropsychopharmacology 31, 2197-2209. doi: 10.1038/sj.npp.1300977
18. Bossert, J. M., Liu, S. Y., Lu, L., and Shaham, Y. (2004). A role of ventral tegmental area glutamate in contextual cue-induced relapse to heroin seeking. J. Neurosci. 24, 10726-10730. doi: 10.1523/JNEUROSCI.3207-04.2004
19. Bossert, J. M., Stern, A. L., Theberge, F. R., Cifani, C., Koya, E., Hope, B. T., et al. (2011). Ventral medial prefrontal cortex neuronal ensembles mediate context-induced relapse to heroin. Nat. Neurosci. 14, 420-422. doi: 10.1038/nn.2758
20. Bossert, J. M., Stern, A. L., Theberge, F. R., Marchant, N. J., Wang, H. L., Morales, M., et al. (2012). Role of projections from ventral medial prefrontal cortex to nucleus accumbens shell in context-induced reinstatement of heroin seeking. J. Neurosci. 32, 4982-4991. doi: 10.1523/JNEUROSCI.0005-12.2012
21. Botreau, F., Paolone, G., and Stewart, J. (2006). d-Cycloserine facilitates extinction of a cocaine-induced conditioned place preference. Behav. Brain Res. 172, 173-178. doi: 10.1016/j.bbr.2006.05.012
22. Bourdy, R., and Barrot, M. (2012). A new control center for dopaminergic systems: pulling the VTA by the tail. Trends Neurosci. 35, 681-690. doi: 10.1016/j.tins.2012.06.007
23. Bozarth, M. A. (1987). Neuroanatomical boundaries of the reward-relevant opiate-receptor field in the ventral tegmental area as mapped by the conditioned place preference method in rats. Brain Res. 414, 77-84. doi: 10.1016/0006-8993(87)91327-8
24. Bozarth, M. A., and Wise, R. A. (1981). Heroin reward is dependent on a dopaminergic substrate. Life Sci. 29, 1881-1886. doi: 10.1016/0024-3205(81)90519-1
25. Bozarth, M. A., and Wise, R. A. (1983). Neural substrates of opiate reinforcement. Prog. Neuropsychopharmacol. Biol. Psychiatry 7, 569-575. doi: 10.1016/0278-5846(83)90027-1
26. Brebner, K., Wong, T. P., Liu, L., Liu, Y., Campsall, P., Gray, S., et al. (2005). Nucleus accumbens long-term depression and the expression of behavioral sensitization. Science 310, 1340-1343. doi: 10.1126/science.1116894
27. Britt, M. D., and Wise, R. A. (1983). Ventral tegmental site of opiate reward: antagonism by a hydrophilic opiate receptor blocker. Brain Res. 258, 105-108. doi: 10.1016/0006-8993(83)91232-5
28. Broekkamp, C. L., Van Den Bogaard, J. H., Heijnen, H. J., Rops, R. H., Cools, A. R., and Van Rossum, J. M. (1976). Separation of inhibiting and stimulating effects of morphine on self-stimulation behaviour by intracerebral microinjections. Eur. J. Pharmacol. 36, 443-446. doi: 10.1016/0014-2999(76)90099-6
29. Brog, J. S., Salyapongse, A., Deutch, A. Y., and Zahm, D. S. (1993). The patterns of afferent innervation of the core and shell in the "accumbens" part of the rat ventral striatum: immunohistochemical detection of retrogradely transported fluoro-gold. J. Comp. Neurol. 338, 255-278. doi: 10.1002/cne.903380209
30. Brown, M. T., Bellone, C., Mameli, M., Labouebe, G., Bocklisch, C., Balland, B., et al. (2010). Drug-driven AMPA receptor redistribution mimicked by selective dopamine neuron stimulation. PLoS ONE 5:e15870. doi: 10.1371/journal.pone.0015870
31. Burnashev, N., Monyer, H., Seeburg, P. H., and Sakmann, B. (1992). Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 8, 189-198. doi: 10.1016/0896-6273(92)90120-3
32. Carelli, R. M. (2002). The nucleus accumbens and reward: neurophysiological investigations in behaving animals. Behav. Cogn. Neurosci. Rev. 1, 281-296. doi: 10.1177/1534582302238338
33. Carlezon, W. A. Jr., Boundy, V. A., Haile, C. N., Lane, S. B., Kalb, R. G., Neve, R. L., et al. (1997). Sensitization to morphine induced by viral-mediated gene transfer. Science 277, 812-814. doi: 10.1126/science.277.5327.812
34. Carlezon, W. A. Jr., Haile, C. N., Coppersmith, R., Hayashi, Y., Malinow, R., Neve, R. L., et al. (2000). Distinct sites of opiate reward and aversion within the midbrain identified using a herpes simplex virus vector expressing GluR1. J. Neurosci. 20, RC62.
35. Carlezon, W. A. Jr., and Nestler, E. J. (2002). Elevated levels of GluR1 in the midbrain: a trigger for sensitization to drugs of abuse? Trends Neurosci. 25, 610-615. doi: 10.1016/S0166-2236(02)02289-0
36. Carlezon, W. A. Jr., and Thomas, M. J. (2009). Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuropharmacology 56(Suppl. 1), 122-132. doi: 10.1016/j.neuropharm.2008.06.075
37. Carlezon, W. A. Jr., and Wise, R. A. (1996a). Microinjections of phencyclidine (PCP) and related drugs into nucleus accumbens shell potentiate medial forebrain bundle brain stimulation reward. Psychopharmacologia 128, 413-420. doi: 10.1007/s002130050151
38. Carlezon, W. A. Jr., and Wise, R. A. (1996b). Rewarding actions of phencyclidine and related drugs in nucleus accumbens shell and frontal cortex. J. Neurosci. 16, 3112-3122.
39. Carr, D. B., and Sesack, S. R. (2000). Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J. Neurosci. 20, 3864-3873.
40. Chartoff, E. H., Barhight, M. F., Mague, S. D., Sawyer, A. M., and Carlezon, W. A. Jr. (2009). Anatomically dissociable effects of dopamine D1 receptor agonists on reward and relief of withdrawal in morphine-dependent rats. Psychopharmacology (Berl.) 204, 227-239. doi: 10.1007/s00213-008-1454-7
41. Chartoff, E. H., Mague, S. D., Barhight, M. F., Smith, A. M., and Carlezon, W. A. Jr. (2006). Behavioral and molecular effects of dopamine D1 receptor stimulation during naloxone-precipitated morphine withdrawal. J. Neurosci. 26, 6450-6457. doi: 10.1523/JNEUROSCI.0491-06.2006
42. Chartoff, E. H., Papadopoulou, M., Konradi, C., and Carlezon, W. A. Jr. (2003a). Dopamine-dependent increases in phosphorylation of cAMP response element binding protein (CREB) during precipitated morphine withdrawal in primary cultures of rat striatum. J. Neurochem. 87, 107-118. doi: 10.1046/j.1471-4159.2003.01992.x
43. Chartoff, E. H., Papadopoulou, M., Konradi, C., and Carlezon, W. A. Jr. (2003b). Effects of naloxone-precipitated morphine withdrawal on glutamate-mediated signaling in striatal neurons in vitro. Ann. N. Y. Acad. Sci. 1003, 368-371. doi: 10.1196/annals.1300.028
44. Chen, Q., and Reiner, A. (1996). Cellular distribution of the NMDA receptor NR2A/2B subunits in the rat striatum. Brain Res. 743, 346-352. doi: 10.1016/S0006-8993(96)01098-0
45. Chen, Y., Mestek, A., Liu, J., and Yu, L. (1993). Molecular cloning of a rat kappa opioid receptor reveals sequence similarities to the mu and delta opioid receptors. Biochem. J. 295(Pt 3), 625-628.
46. Cherubini, E., Herrling, P. L., Lanfumey, L., and Stanzione, P. (1988). Excitatory amino acids in synaptic excitation of rat striatal neurones in vitro. J. Physiol. 400, 677-690.
47. Chieng, B., and Williams, J. T. (1998). Increased opioid inhibition of GABA release in nucleus accumbens during morphine withdrawal. J. Neurosci. 18, 7033-7039.
48. Childers, S. R. (1991). Opioid receptor-coupled second messenger systems. Life Sci. 48, 1991-2003. doi: 10.1016/0024-3205(91)90154-4
49. Citri, A., and Malenka, R. C. (2008). Synaptic plasticity: multiple forms, functions, and mechanisms. Neuropsychopharmacology 33, 18-41. doi: 10.1038/sj.npp.1301559
50. Clem, R. L., and Barth, A. (2006). Pathway-specific trafficking of native AMPARs by in vivo experience. Neuron 49, 663-670. doi: 10.1016/j.neuron.2006.01.019
51. Contarino, A., and Papaleo, F. (2005). The corticotropin-releasing factor receptor-1 pathway mediates the negative affective states of opiate withdrawal. Proc. Natl. Acad. Sci. U.S.A. 102, 18649-18654. doi: 10.1073/pnas.0506999102
52. David, V., and Cazala, P. (2000). Anatomical and pharmacological specificity of the rewarding effect elicited by microinjections of morphine into the nucleus accumbens of mice. Psychopharmacology (Berl.) 150, 24-34. doi: 10.1007/s002130000425
53. Denier, N., Gerber, H., Vogel, M., Klarhofer, M., Riecher-Rossler, A., Wiesbeck, G. A., et al. (2013). Reduction in cerebral perfusion after heroin administration: a resting state arterial spin labeling study. PLoS ONE 8:e71461. doi: 10.1371/journal.pone.0071461
54. Desole, M. S., Esposito, G., Fresu, L., Migheli, R., Enrico, P., Mura, M. A., et al. (1996). Effects of morphine treatment and withdrawal on striatal and limbic monoaminergic activity and ascorbic acid oxidation in the rat. Brain Res. 723, 154-161. doi: 10.1016/0006-8993(96)00235-1
55. Devine, D. P., and Wise, R. A. (1994). Self-administration of morphine, DAMGO, and DPDPE into the ventral tegmental area of rats. J. Neurosci. 14, 1978-1984.
56. Diana, M., Pistis, M., Muntoni, A., and Gessa, G. (1995). Profound decrease of mesolimbic dopaminergic neuronal activity in morphine withdrawn rats. J. Pharmacol. Exp. Ther. 272, 781-785.
57. Di Chiara, G., and Imperato, A. (1988a). Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc. Natl. Acad. Sci. U.S.A. 85, 5274-5278. doi: 10.1073/pnas.85.14.5274
58. Di Chiara, G., and Imperato, A. (1988b). Opposite effects of mu and kappa opiate agonists on dopamine release in the nucleus accumbens and in the dorsal caudate of freely moving rats. J. Pharmacol. Exp. Ther. 244, 1067-1080.
59. Dingledine, R., Borges, K., Bowie, D., and Traynelis, S. F. (1999). The glutamate receptor ion channels. Pharmacol. Rev. 51, 7-61.
60. Dole, V. P., Nyswander, M. E., and Kreek, M. J. (1966). Narcotic blockade. Arch. Intern. Med. 118, 304-309. doi: 10.1001/archinte.1966.00290160004002
61. Duman, R. S., Tallman, J. F., and Nestler, E. J. (1988). Acute and chronic opiate-regulation of adenylate cyclase in brain: specific effects in locus coeruleus. J. Pharmacol. Exp. Ther. 246, 1033-1039.
62. Dunah, A. W., Yasuda, R. P., Luo, J., Wang, Y., Prybylowski, K. L., and Wolfe, B. B. (1999). Biochemical studies of the structure and function of the N-methyl-D-aspartate subtype of glutamate receptors. Mol. Neurobiol. 19, 151-179. doi: 10.1007/BF02743658
63. Dworkin, S. I., Guerin, G. F., Goeders, N. E., and Smith, J. E. (1988). Kainic acid lesions of the nucleus accumbens selectively attenuate morphine self-administration. Pharmacol. Biochem. Behav. 29, 175-181. doi: 10.1016/0091-3057(88)90292-4
64. Enrico, P., Mura, M. A., Esposito, G., Serra, P., Migheli, R., De Natale, G., et al. (1998). Effect of naloxone on morphine-induced changes in striatal dopamine metabolism and glutamate, ascorbic acid and uric acid release in freely moving rats. Brain Res. 797, 94-102. doi: 10.1016/S0006-8993(98)00371-0
65. Epstein, D. H., Preston, K. L., Stewart, J., and Shaham, Y. (2006). Toward a model of drug relapse: an assessment of the validity of the reinstatement procedure. Psychopharmacology (Berl.) 189, 1-16. doi: 10.1007/s00213-006-0529-6
66. Esteban, J. A., Shi, S. H., Wilson, C., Nuriya, M., Huganir, R. L., and Malinow, R. (2003). PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat. Neurosci. 6, 136-143. doi: 10.1038/nn997
67. Fields, H. L., Hjelmstad, G. O., Margolis, E. B., and Nicola, S. M. (2007). Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu. Rev. Neurosci. 30, 289-316. doi: 10.1146/annurev.neuro.30.051606.094341
68. Fitzgerald, L. W., Ortiz, J., Hamedani, A. G., and 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.
69. Floresco, S. B., West, A. R., Ash, B., Moore, H., and Grace, A. A. (2003). Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat. Neurosci. 6, 968-973. doi: 10.1038/nn1103
70. Fudala, P. J., Bridge, T. P., Herbert, S., Williford, W. O., Chiang, C. N., Jones, K., et al. (2003). Office-based treatment of opiate addiction with a sublingual-tablet formulation of buprenorphine and naloxone. N. Engl. J. Med. 349, 949-958. doi: 10.1056/NEJMoa022164
71. Garzon, M., and Pickel, V. M. (2001). Plasmalemmal mu-opioid receptor distribution mainly in nondopaminergic neurons in the rat ventral tegmental area. Synapse 41, 311-328. doi: 10.1002/syn.1088
72. Georges, F., Le Moine, C., and Aston-Jones, G. (2006). No effect of morphine on ventral tegmental dopamine neurons during withdrawal. J. Neurosci. 26, 5720-5726. doi: 10.1523/JNEUROSCI.5032-05.2006
73. Georges, F., Stinus, L., Bloch, B., and Le Moine, C. (1999). Chronic morphine exposure and spontaneous withdrawal are associated with modifications of dopamine receptor and neuropeptide gene expression in the rat striatum. Eur. J. Neurosci. 11, 481-490. doi: 10.1046/j.1460-9568.1999.00462.x
74. Gerfen, C. R. (1992). The neostriatal mosaic: multiple levels of compartmental organization. Trends Neurosci. 15, 133-139. doi: 10.1016/0166-2236(92)90355-C
75. Gerfen, C. R., Engber, T. M., Mahan, L. C., Susel, Z., Chase, T. N., Monsma, F. J., et al. (1990). D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250, 1429-1432. doi: 10.1126/science.2147780
76. Gerrits, M. A., and Van Ree, J. M. (1996). Effect of nucleus accumbens dopamine depletion on motivational aspects involved in initiation of cocaine and heroin self-administration in rats. Brain Res. 713, 114-124. doi: 10.1016/0006-8993(95)01491-8
77. Giacchino, J. L., and Henriksen, S. J. (1996). Systemic morphine and local opioid effects on neuronal activity in the medial prefrontal cortex. Neuroscience 70, 941-949. doi: 10.1016/0306-4522(95)00409-2
78. Glass, M. J., Lane, D. A., Colago, E. E., Chan, J., Schlussman, S. D., Zhou, Y., et al. (2008). Chronic administration of morphine is associated with a decrease in surface AMPA GluR1 receptor subunit in dopamine D1 receptor expressing neurons in the shell and non-D1 receptor expressing neurons in the core of the rat nucleus accumbens. Exp. Neurol. 210, 750-761. doi: 10.1016/j.expneurol.2008.01.012
79. Glass, M. J., Vanyo, L., Quimson, L., and Pickel, V. M. (2009). Ultrastructural relationship between N-methyl-D-aspartate-NR1 receptor subunit and mu-opioid receptor in the mouse central nucleus of the amygdala. Neuroscience 163, 857-867. doi: 10.1016/j.neuroscience.2009.07.020
80. Goeders, N. E., Lane, J. D., and Smith, J. E. (1984). Self-administration of methionine enkephalin into the nucleus accumbens. Pharmacol. Biochem. Behav. 20, 451-455. doi: 10.1016/0091-3057(84)90284-3
81. Gonzalez, P., Cabello, P., Germany, A., Norris, B., and Contreras, E. (1997). Decrease of tolerance to, and physical dependence on morphine by, glutamate receptor antagonists. Eur. J. Pharmacol. 332, 257-262. doi: 10.1016/S0014-2999(97)01099-6
82. Grace, A. A., Floresco, S. B., Goto, Y., and Lodge, D. J. (2007). Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci. 30, 220-227. doi: 10.1016/j.tins.2007.03.003
83. Gracy, K. N., Svingos, A. L., and Pickel, V. M. (1997). Dual ultrastructural localization of mu-opioid receptors and NMDA-type glutamate receptors in the shell of the rat nucleus accumbens. J. Neurosci. 17, 4839-4848.
84. Groenewegen, H. J., Vermeulen-Van Der Zee, E., Te Kortschot, A., and Witter, M. P. (1987). Organization of the projections from the subiculum to the ventral striatum in the rat. A study using anterograde transport of Phaseolus vulgaris leucoagglutinin. Neuroscience 23, 103-120. doi: 10.1016/0306-4522(87)90275-2
85. Gysling, K., and Wang, R. Y. (1983). Morphine-induced activation of A10 dopamine neurons in the rat. Brain Res. 277, 119-127. doi: 10.1016/0006-8993(83)90913-7
86. Haber, S. N., Fudge, J. L., and Mcfarland, N. R. (2000). Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J. Neurosci. 20, 2369-2382.
87. Haber, S. N., and Knutson, B. (2010). The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 4-26. doi: 10.1038/npp.2009.129
88. Haber, S. N., Lynd, E., Klein, C., and Groenewegen, H. J. (1990). Topographic organization of the ventral striatal efferent projections in the rhesus monkey: an anterograde tracing study. J. Comp. Neurol. 293, 282-298. doi: 10.1002/cne.902930210
89. Harris, G. C., and Aston-Jones, G. (1994). Involvement of D2 dopamine receptors in the nucleus accumbens in the opiate withdrawal syndrome. Nature 371, 155-157. doi: 10.1038/371155a0
90. Harris, G. C., Wimmer, M., Byrne, R., and Aston-Jones, G. (2004). Glutamate-associated plasticity in the ventral tegmental area is necessary for conditioning environmental stimuli with morphine. Neuroscience 129, 841-847. doi: 10.1016/j.neuroscience.2004.09.018
91. Heather, N., Stallard, A., and Tebbutt, J. (1991). Importance of substance cues in relapse among heroin users: comparison of two methods of investigation. Addict. Behav. 16, 41-49. doi: 10.1016/0306-4603(91)90038-J
92. Heine, M., Groc, L., Frischknecht, R., Beique, J. C., Lounis, B., Rumbaugh, G., et al. (2008). Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science 320, 201-205. doi: 10.1126/science.1152089
93. Herrold, A. A., Persons, A. L., and Napier, T. C. (2013). Cellular distribution of AMPA receptor subunits and mGlu5 following acute and repeated administration of morphine or methamphetamine. J. Neurochem. 126, 503-517. doi: 10.1111/jnc.12323
94. Hokfelt, T., Broberger, C., Xu, Z. Q., Sergeyev, V., Ubink, R., and Diez, M. (2000). Neuropeptides - an overview. Neuropharmacology 39, 1337-1356. doi: 10.1016/S0028-3908(00)00010-1
95. Hollmann, M., Hartley, M., and Heinemann, S. (1991). Ca2+ permeability of KA-AMPA - gated glutamate receptor channels depends on subunit composition. Science 252, 851-853. doi: 10.1126/science.1709304
96. Hollmann, M., and Heinemann, S. (1994). Cloned glutamate receptors. Annu. Rev. Neurosci. 17, 31-108. doi: 10.1146/annurev.ne.17.030194.000335
97. Hu, X. T., and White, F. J. (1996). Glutamate receptor regulation of rat nucleus accumbens neurons in vivo. Synapse 23, 208-218. doi: 10.1002/(SICI)1098-2396(199607)23:3<208::AID-SYN10>3.0.CO;2-V
98. Hyman, S. E., Malenka, R. C., and Nestler, E. J. (2006). Neural mechanisms of addiction: the role of reward-related learning and memory. Annu. Rev. Neurosci. 29, 565-598. doi: 10.1146/annurev.neuro.29.051605.113009
99. Ikemoto, S. (2007). Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res. Rev. 56, 27-78. doi: 10.1016/j.brainresrev.2007.05.004
100. Ikemoto, S., and 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. doi: 10.1016/S0165-0173(99)00023-5
101. Inoue, M., Mishina, M., and Ueda, H. (2003). Locus-specific rescue of GluRepsilon1 NMDA receptors in mutant mice identifies the brain regions important for morphine tolerance and dependence. J. Neurosci. 23, 6529-6536.
102. Jacobs, E. H., Wardeh, G., Smit, A. B., and Schoffelmeer, A. N. (2005). Morphine causes a delayed increase in glutamate receptor functioning in the nucleus accumbens core. Eur. J. Pharmacol. 511, 27-30. doi: 10.1016/j.ejphar.2005.02.009
103. Jalabert, M., Bourdy, R., Courtin, J., Veinante, P., Manzoni, O. J., Barrot, M., et al. (2011). Neuronal circuits underlying acute morphine action on dopamine neurons. Proc. Natl. Acad. Sci. U.S.A. 108, 16446-16450. doi: 10.1073/pnas.1105418108
104. Jensen, J., Mcintosh, A. R., Crawley, A. P., Mikulis, D. J., Remington, G., and Kapur, S. (2003). Direct activation of the ventral striatum in anticipation of aversive stimuli. Neuron 40, 1251-1257. doi: 10.1016/S0896-6273(03)00724-4
105. Jhou, T. C., Geisler, S., Marinelli, M., Degarmo, B. A., and Zahm, D. S. (2009). The mesopontine rostromedial tegmental nucleus: a structure targeted by the lateral habenula that projects to the ventral tegmental area of Tsai and substantia nigra compacta. J. Comp. Neurol. 513, 566-596. doi: 10.1002/cne.21891
106. Johnson, S. W., and North, R. A. (1992). Opioids excite dopamine neurons by hyperpolarization of local interneurons. J. Neurosci. 12, 483-488.
107. Johnston, L. D., O'Malley, P. M., Miech, R. A., Bachman, J. G., and Schulenberg, J. E. (2014). Monitoring the Future National Survey Results on Drug Use: 2013 Overview, Key Findings on Adolescent Drug Use. Ann Arbor: University of Michigan.
108. Ju, W., Morishita, W., Tsui, J., Gaietta, G., Deerinck, T. J., Adams, S. R., et al. (2004). Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors. Nat. Neurosci. 7, 244-253. doi: 10.1038/nn1189
109. Kalivas, P. W. (2009). The glutamate homeostasis hypothesis of addiction. Nat. Rev. Neurosci. 10, 561-572. doi: 10.1038/nrn2515
110. Kalivas, P. W., Lalumiere, R. T., Knackstedt, L., and Shen, H. (2009). Glutamate transmission in addiction. Neuropharmacology 56(Suppl. 1), 169-173. doi: 10.1016/j.neuropharm.2008.07.011
111. Kauer, J. A., and Malenka, R. C. (2007). Synaptic plasticity and addiction. Nat. Rev. Neurosci. 8, 844-858. doi: 10.1038/nrn2234
112. Kawaguchi, Y., Wilson, C. J., Augood, S. J., and Emson, P. C. (1995). Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci. 18, 527-535. doi: 10.1016/0166-2236(95)98374-8
113. Kelley, A. E., and Domesick, V. B. (1982). The distribution of the projection from the hippocampal formation to the nucleus accumbens in the rat: an anterograde- and retrograde-horseradish peroxidase study. Neuroscience 7, 2321-2335. doi: 10.1016/0306-4522(82)90198-1
114. Kelley, A. E., Domesick, V. B., and Nauta, W. J. (1982). The amygdalostriatal projection in the rat - an anatomical study by anterograde and retrograde tracing methods. Neuroscience 7, 615-630. doi: 10.1016/0306-4522(82)90067-7
115. Kerchner, G. A., and Nicoll, R. A. (2008). Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat. Rev. Neurosci. 9, 813-825. doi: 10.1038/nrn2501
116. Kessels, H. W., and Malinow, R. (2009). Synaptic AMPA receptor plasticity and behavior. Neuron 61, 340-350. doi: 10.1016/j.neuron.2009.01.015
117. Khan, Z. U., Gutierrez, A., Martin, R., Penafiel, A., Rivera, A., and De La Calle, A. (2000). Dopamine D5 receptors of rat and human brain. Neuroscience 100, 689-699. doi: 10.1016/S0306-4522(00)00274-8
118. Konradi, C., Cole, R. L., Heckers, S., and Hyman, S. E. (1994). Amphetamine regulates gene expression in rat striatum via transcription factor CREB. J. Neurosci. 14, 5623-5634.
119. Konradi, C., Leveque, J. C., and Hyman, S. E. (1996). Amphetamine and dopamine-induced immediate early gene expression in striatal neurons depends on postsynaptic NMDA receptors and calcium. J. Neurosci. 16, 4231-4239.
120. Koob, G. F. (1992). Drugs of abuse: anatomy, pharmacology and function of reward pathways. Trends Pharmacol. Sci. 13, 177-184. doi: 10.1016/0165-6147(92)90060-J
121. Koob, G. F. (2009). Neurobiological substrates for the dark side of compulsivity in addiction. Neuropharmacology 56(Suppl. 1), 18-31. doi: 10.1016/j.neuropharm.2008.07.043
122. Koob, G. F., Maldonado, R., and Stinus, L. (1992). Neural substrates of opiate withdrawal. Trends Neurosci. 15, 186-191. doi: 10.1016/0166-2236(92)90171-4
123. Kosel, M., Noss, R. S., Hammig, R., Wielepp, P., Bundeli, P., Heidbreder, R., et al. (2008). Cerebral blood flow effects of acute intravenous heroin administration. Eur. Neuropsychopharmacol. 18, 278-285. doi: 10.1016/j.euroneuro.2007.11.007
124. Kreek, M. J., and Koob, G. F. (1998). Drug dependence: stress and dysregulation of brain reward pathways. Drug Alcohol Depend. 51, 23-47. doi: 10.1016/S0376-8716(98)00064-7
125. Kuppenbender, K. D., Standaert, D. G., Feuerstein, T. J., Penney, J. B. Jr., Young, A. B., and Landwehrmeyer, G. B. (2000). Expression of NMDA receptor subunit mRNAs in neurochemically identified projection and interneurons in the human striatum. J. Comp. Neurol. 419, 407-421. doi: 10.1002/(SICI)1096-9861(20000417)419:4<407::AID-CNE1>3.0.CO;2-I
126. LaLumiere, R. T., and Kalivas, P. W. (2008). Glutamate release in the nucleus accumbens core is necessary for heroin seeking. J. Neurosci. 28, 3170-3177. doi: 10.1523/JNEUROSCI.5129-07.2008
127. Lane, D. A., Lessard, A. A., Chan, J., Colago, E. E., Zhou, Y., Schlussman, S. D., et al. (2008). Region-specific changes in the subcellular distribution of AMPA receptor GluR1 subunit in the rat ventral tegmental area after acute or chronic morphine administration. J. Neurosci. 28, 9670-9681. doi: 10.1523/JNEUROSCI.2151-08.2008
128. Law, P. Y., Wong, Y. H., and Loh, H. H. (2000). Molecular mechanisms and regulation of opioid receptor signaling. Annu. Rev. Pharmacol. Toxicol. 40, 389-430. doi: 10.1146/annurev.pharmtox.40.1.389
129. Le Merrer, J., Becker, J. A., Befort, K., and Kieffer, B. L. (2009). Reward processing by the opioid system in the brain. Physiol. Rev. 89, 1379-1412. doi: 10.1152/physrev.00005.2009
130. Leri, F., Flores, J., Rajabi, H., and Stewart, J. (2003). Effects of cocaine in rats exposed to heroin. Neuropsychopharmacology 28, 2102-2116. doi: 10.1038/sj.npp.1300284
131. Li, S. X., Shi, J., Epstein, D. H., Wang, X., Zhang, X. L., Bao, Y. P., et al. (2009). Circadian alteration in neurobiology during 30 days of abstinence in heroin users. Biol. Psychiatry 65, 905-912. doi:10.1016/j.biopsych.2008.11.025
132. Liu, S. Q., and Cull-Candy, S. G. (2000). Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 405, 454-458. doi: 10.1038/35013064
133. Lobo, M. K. (2009). Molecular profiling of striatonigral and striatopallidal medium spiny neurons past, present, and future. Int. Rev. Neurobiol. 89, 1-35. doi: 10.1016/S0074-7742(09)89001-6
134. Lodge, D. J., and Grace, A. A. (2006). The laterodorsal tegmentum is essential for burst firing of ventral tegmental area dopamine neurons. Proc. Natl. Acad. Sci. U.S.A. 103, 5167-5172. doi: 10.1073/pnas.0510715103
135. London, E. D., Broussolle, E. P., Links, J. M., Wong, D. F., Cascella, N. G., Dannals, R. F., et al. (1990). Morphine-induced metabolic changes in human brain. Studies with positron emission tomography and [fluorine 18]fluorodeoxyglucose. Arch. Gen. Psychiatry 47, 73-81. doi: 10.1001/archpsyc.1990.01810130075010
136. Lu, X. Y., Ghasemzadeh, M. B., and Kalivas, P. W. (1998). Expression of D1 receptor, D2 receptor, substance P and enkephalin messenger RNAs in the neurons projecting from the nucleus accumbens. Neuroscience 82, 767-780. doi: 10.1016/S0306-4522(97)00327-8
137. Luscher, C. (2013). Cocaine-evoked synaptic plasticity of excitatory transmission in the ventral tegmental area. Cold Spring Harb. Perspect. Med. 3, a012013. doi: 10.1101/cshperspect.a012013
138. Magura, S., and Rosenblum, A. (2001). Leaving methadone treatment: lessons learned, lessons forgotten, lessons ignored. Mt. Sinai J. Med. 68, 62-74.
139. Mahler, S. V., Smith, R. J., Moorman, D. E., Sartor, G. C., and Aston-Jones, G. (2012). Multiple roles for orexin/hypocretin in addiction. Prog. Brain Res. 198, 79-121. doi: 10.1016/B978-0-444-59489-1.00007-0
140. Malinow, R., and Malenka, R. C. (2002). AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103-126. doi: 10.1146/annurev.neuro.25.112701.142758
141. Mangiavacchi, S., and Wolf, M. E. (2004). D1 dopamine receptor stimulation increases the rate of AMPA receptor insertion onto the surface of cultured nucleus accumbens neurons through a pathway dependent on protein kinase A. J. Neurochem. 88, 1261-1271. doi: 10.1046/j.1471-4159.2003.02248.x
142. Mansour, A., Fox, C. A., Akil, H., and Watson, S. J. (1995a). Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends Neurosci. 18, 22-29. doi: 10.1016/0166-2236(95)93946-U
143. Mansour, A., Fox, C. A., Burke, S., Akil, H., and Watson, S. J. (1995b). Immunohistochemical localization of the cloned mu opioid receptor in the rat CNS. J. Chem. Neuroanat. 8, 283-305. doi: 10.1016/0891-0618(95)00055-C
144. Mansour, A., Fox, C. A., Thompson, R. C., Akil, H., and Watson, S. J. (1994). mu-Opioid receptor mRNA expression in the rat CNS: comparison to mu-receptor binding. Brain Res. 643, 245-265. doi: 10.1016/0006-8993(94)90031-0
145. Mansour, A., Khachaturian, H., Lewis, M. E., Akil, H., and Watson, S. J. (1988). Anatomy of CNS opioid receptors. Trends Neurosci. 11, 308-314. doi: 10.1016/0166-2236(88)90093-8
146. Manzoni, O. J., and Williams, J. T. (1999). Presynaptic regulation of glutamate release in the ventral tegmental area during morphine withdrawal. J. Neurosci. 19, 6629-6636.
147. Martin, G., Guadano-Ferraz, A., Morte, B., Ahmed, S., Koob, G. F., De Lecea, L., et al. (2004). Chronic morphine treatment alters N-methyl-D-aspartate receptors in freshly isolated neurons from nucleus accumbens. J. Pharmacol. Exp. Ther. 311, 265-273. doi: 10.1124/jpet.104.067504
148. Martin, G., Nie, Z., and Siggins, G. R. (1997). mu-Opioid receptors modulate NMDA receptor-mediated responses in nucleus accumbens neurons. J. Neurosci. 17, 11-22.
149. Martin, G., Przewlocki, R., and Siggins, G. R. (1999). Chronic morphine treatment selectively augments metabotropic glutamate receptor-induced inhibition of N-methyl-D-aspartate receptor-mediated neurotransmission in nucleus accumbens. J. Pharmacol. Exp. Ther. 288, 30-35.
150. Martin, W. R., and Jasinski, D. R. (1969). Physiological parameters of morphine dependence in man - tolerance, early abstinence, protracted abstinence. J. Psychiatr. Res. 7, 9-17. doi: 10.1016/0022-3956(69)90007-7
151. Matthes, H. W., Maldonado, R., Simonin, F., Valverde, O., Slowe, S., Kitchen, I., et al. (1996). Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature 383, 819-823. doi: 10.1038/383819a0
152. Mattick, R. P., Kimber, J., Breen, C., and Davoli, M. (2008). Buprenorphine maintenance versus placebo or methadone maintenance for opioid dependence. Cochrane Database Syst. Rev. CD002207. doi: 10.1002/14651858.CD002207.pub3
153. Mazei-Robison, M. S., Koo, J. W., Friedman, A. K., Lansink, C. S., Robison, A. J., Vinish, M., et al. (2011). Role for mTOR signaling and neuronal activity in morphine-induced adaptations in ventral tegmental area dopamine neurons. Neuron 72, 977-990. doi: 10.1016/j.neuron.2011.10.012
154. McFarland, K., and Kalivas, P. W. (2001). The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior. J. Neurosci. 21, 8655-8663.
155. Mello, N. K., and Negus, S. S. (1996). Preclinical evaluation of pharmacotherapies for treatment of cocaine and opioid abuse using drug self-administration procedures. Neuropsychopharmacology 14, 375-424. doi: 10.1016/0893-133X(95)00274-H
156. Mickiewicz, A. L., and Napier, T. C. (2011). Repeated exposure to morphine alters surface expression of AMPA receptors in the rat medial prefrontal cortex. Eur. J. Neurosci. 33, 259-265. doi: 10.1111/j.1460-9568.2010.07502.x
157. Mink, J. W. (1996). The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol. 50, 381-425. doi: 10.1016/S0301-0082(96)00042-1
158. Mogenson, G. J., Jones, D. L., and Yim, C. Y. (1980). From motivation to action - functional interface between the limbic system and the motor system. Prog. Neurobiol. 14, 69-97. doi: 10.1016/0301-0082(80)90018-0
159. Monyer, H., Sprengel, R., Schoepfer, R., Herb, A., Higuchi, M., Lomeli, H., et al. (1992). Heteromeric NMDA receptors: molecular and functional distinction of subtypes. Science 256, 1217-1221. doi: 10.1126/science.256.5060.1217
160. Murray, F., Harrison, N. J., Grimwood, S., Bristow, L. J., and Hutson, P. H. (2007). Nucleus accumbens NMDA receptor subunit expression and function is enhanced in morphine-dependent rats. Eur. J. Pharmacol. 562, 191-197. doi: 10.1016/j.ejphar.2007.01.027
161. Myers, K. M., and Carlezon, W. A. Jr. (2010a). D-Cycloserine facilitates extinction of naloxone-induced conditioned place aversion in morphine-dependent rats. Biol. Psychiatry 67, 85-87. doi: 10.1016/j.biopsych.2009.08.015
162. Myers, K. M., and Carlezon, W. A. Jr. (2010b). Extinction of drug- and withdrawal-paired cues in animal models: relevance to the treatment of addiction. Neurosci. Biobehav. Rev. 35, 285-302. doi: 10.1016/j.neubiorev.2010.01.011
163. Nair-Roberts, R. G., Chatelain-Badie, S. D., Benson, E., White-Cooper, H., Bolam, J. P., and 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. doi: 10.1016/j.neuroscience.2008.01.046
164. Nestler, E. J., and Aghajanian, G. K. (1997). Molecular and cellular basis of addiction. Science 278, 58-63. doi: 10.1126/science.278.5335.58
165. Nestler, E. J., and Tallman, J. F. (1988). Chronic morphine treatment increases cyclic AMP-dependent protein kinase activity in the rat locus coeruleus. Mol. Pharmacol. 33, 127-132.
166. Niehaus, J. L., Murali, M., and Kauer, J. A. (2010). Drugs of abuse and stress impair LTP at inhibitory synapses in the ventral tegmental area. Eur. J. Neurosci. 32, 108-117. doi: 10.1111/j.1460-9568.2010.07256.x
167. NSDUH. (2013). Results from the 2012 National Survey on Drug Use and Health: Summary of National Findings. Rockville: Substance Abuse and Mental Health Services Administration.
168. O'Brien, C. P., Ehrman, R. N., and Ternes, J. W. (1986). "Classical conditioning in human opioid dependence," in Behavioral Analysis of Drug Dependence, ed. S. Goldberg (Orlando: Academic Press), 329-356.
169. Olds, M. E. (1982). Reinforcing effects of morphine in the nucleus accumbens. Brain Res. 237, 429-440. doi: 10.1016/0006-8993(82)90454-1
170. Paolone, G., Botreau, F., and Stewart, J. (2009). The facilitative effects of D-cycloserine on extinction of a cocaine-induced conditioned place preference can be long lasting and resistant to reinstatement. Psychopharmacology (Berl.) 202, 403-409. doi: 10.1007/s00213-008-1280-y
171. Pasternak, G. W. (2012). Preclinical pharmacology and opioid combinations. Pain Med. 13(Suppl. 1), S4-S11. doi: 10.1111/j.1526-4637.2012.01335.x
172. Peoples, L. L., and West, M. O. (1996). Phasic firing of single neurons in the rat nucleus accumbens correlated with the timing of intravenous cocaine self-administration. J. Neurosci. 16, 3459-3473.
173. Pettit, H. O., Ettenberg, A., Bloom, F. E., and Koob, G. F. (1984). Destruction of dopamine in the nucleus accumbens selectively attenuates cocaine but not heroin self-administration in rats. Psychopharmacology (Berl.) 84, 167-173. doi: 10.1007/BF00427441
174. Pierce, R. C., and Wolf, M. E. (2013). Psychostimulant-induced neuroadaptations in nucleus accumbens AMPA receptor transmission. Cold Spring Harb. Perspect. Med. 3, a012021. doi: 10.1101/cshperspect.a012021
175. Popik, P., and Kolasiewicz, W. (1999). Mesolimbic NMDA receptors are implicated in the expression of conditioned morphine reward. Naunyn Schmiedebergs Arch. Pharmacol. 359, 288-294. doi: 10.1007/PL00005354
176. Reimers, J. M., Milovanovic, M., and Wolf, M. E. (2011). Quantitative analysis of AMPA receptor subunit composition in addiction-related brain regions. Brain Res. 1367, 223-233. doi: 10.1016/j.brainres.2010.10.016
177. Reynolds, S. M., and Berridge, K. C. (2002). Positive and negative motivation in nucleus accumbens shell: bivalent rostrocaudal gradients for GABA-elicited eating, taste "liking"/"disliking" reactions, place preference/avoidance, and fear. J. Neurosci. 22, 7308-7320.
178. Robbe, D., Alonso, G., Chaumont, S., Bockaert, J., and Manzoni, O. J. (2002a). Role of p/q-Ca2+ channels in metabotropic glutamate receptor 2/3-dependent presynaptic long-term depression at nucleus accumbens synapses. J. Neurosci. 22, 4346-4356.
179. Robbe, D., Bockaert, J., and Manzoni, O. J. (2002b). Metabotropic glutamate receptor 2/3-dependent long-term depression in the nucleus accumbens is blocked in morphine withdrawn mice. Eur. J. Neurosci. 16, 2231-2235. doi: 10.1046/j.1460-9568.2002.02273.x
180. Rodriguez-Munoz, M., Sanchez-Blazquez, P., Vicente-Sanchez, A., Berrocoso, E., and Garzon, J. (2012). The mu-opioid receptor and the NMDA receptor associate in PAG neurons: implications in pain control. Neuropsychopharmacology 37, 338-349. doi: 10.1038/npp.2011.155
181. Rogawski, M. A., and Loscher, W. (2004). The neurobiology of antiepileptic drugs. Nat. Rev. Neurosci. 5, 553-564. doi: 10.1038/nrn1430
182. Roitman, M. F., Wheeler, R. A., and Carelli, R. M. (2005). Nucleus accumbens neurons are innately tuned for rewarding and aversive taste stimuli, encode their predictors, and are linked to motor output. Neuron 45, 587-597. doi: 10.1016/j.neuron.2004.12.055
183. Rossetti, Z. L., Hmaidan, Y., and Gessa, G. L. (1992). Marked inhibition of mesolimbic dopamine release: a common feature of ethanol, morphine, cocaine and amphetamine abstinence in rats. Eur. J. Pharmacol. 221, 227-234. doi: 10.1016/0014-2999(92)90706-A
184. Rothwell, P. E., Thomas, M. J., and Gewirtz, J. C. (2012). Protracted manifestations of acute dependence after a single morphine exposure. Psychopharmacology (Berl.) 219, 991-998. doi: 10.1007/s00213-011-2425-y
185. Saal, D., Dong, Y., Bonci, A., and Malenka, R. C. (2003). Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37, 577-582. doi: 10.1016/S0896-6273(03)00021-7
186. Salamone, J. D., and Correa, M. (2012). The mysterious motivational functions of mesolimbic dopamine. Neuron 76, 470-485. doi: 10.1016/j.neuron.2012.10.021
187. Schildein, S., Agmo, A., Huston, J. P., and Schwarting, R. K. (1998). Intraaccumbens injections of substance P, morphine and amphetamine: effects on conditioned place preference and behavioral activity. Brain Res. 790, 185-194. doi: 10.1016/S0006-8993(98)00062-6
188. Schilstrom, B., Yaka, R., Argilli, E., Suvarna, N., Schumann, J., Chen, B. T., et al. (2006). Cocaine enhances NMDA receptor-mediated currents in ventral tegmental area cells via dopamine D5 receptor-dependent redistribution of NMDA receptors. J. Neurosci. 26, 8549-8558. doi: 10.1523/JNEUROSCI.5179-05.2006
189. Schlaepfer, T. E., Strain, E. C., Greenberg, B. D., Preston, K. L., Lancaster, E., Bigelow, G. E., et al. (1998). Site of opioid action in the human brain: mu and kappa agonists' subjective and cerebral blood flow effects. Am. J. Psychiatry 155, 470-473.
190. Schlosburg, J. E., Whitfield, T. W. Jr., Park, P. E., Crawford, E. F., George, O., Vendruscolo, L. F., et al. (2013). Long-term antagonism of kappa opioid receptors prevents escalation of and increased motivation for heroin intake. J. Neurosci. 33, 19384-19392. doi: 10.1523/JNEUROSCI.1979-13.2013
191. Seeburg, P. H. (1993). The TINS/TiPS Lecture. The molecular biology of mammalian glutamate receptor channels. Trends Neurosci. 16, 359-365. doi: 10.1016/0166-2236(93)90093-2
192. Seeburg, P. H., Burnashev, N., Kohr, G., Kuner, T., Sprengel, R., and Monyer, H. (1995). The NMDA receptor channel: molecular design of a coincidence detector. Recent Prog. Horm. Res. 50, 19-34.
193. Self, D. W., Mcclenahan, A. W., Beitner-Johnson, D., Terwilliger, R. Z., and Nestler, E. J. (1995). Biochemical adaptations in the mesolimbic dopamine system in response to heroin self-administration. Synapse 21, 312-318. doi: 10.1002/syn.890210405
194. Sepulveda, J., Oliva, P., and Contreras, E. (2004). Neurochemical changes of the extracellular concentrations of glutamate and aspartate in the nucleus accumbens of rats after chronic administration of morphine. Eur. J. Pharmacol. 483, 249-258. doi: 10.1016/j.ejphar.2003.10.037
195. Sepulveda, M. J., Hernandez, L., Rada, P., Tucci, S., and Contreras, E. (1998). Effect of precipitated withdrawal on extracellular glutamate and aspartate in the nucleus accumbens of chronically morphine-treated rats: an in vivo microdialysis study. Pharmacol. Biochem. Behav. 60, 255-262. doi: 10.1016/S0091-3057(97)00550-9
196. Sesack, S. R., and Grace, A. A. (2010). Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 35, 27-47. doi: 10.1038/npp.2009.93
197. Shabat-Simon, M., Levy, D., Amir, A., Rehavi, M., and Zangen, A. (2008). Dissociation between rewarding and psychomotor effects of opiates: differential roles for glutamate receptors within anterior and posterior portions of the ventral tegmental area. J. Neurosci. 28, 8406-8416. doi: 10.1523/JNEUROSCI.1958-08.2008
198. Shalev, U., Grimm, J. W., and Shaham, Y. (2002). Neurobiology of relapse to heroin and cocaine seeking: a review. Pharmacol. Rev. 54, 1-42. doi: 10.1124/pr.54.1.1
199. Shaw-Lutchman, T. Z., Barrot, M., Wallace, T., Gilden, L., Zachariou, V., Impey, S., et al. (2002). Regional and cellular mapping of cAMP response element-mediated transcription during naltrexone-precipitated morphine withdrawal. J. Neurosci. 22, 3663-3672.
200. Shen, H., and Kalivas, P. W. (2013). Reduced LTP and LTD in prefrontal cortex synapses in the nucleus accumbens after heroin self-administration. Int. J. Neuropsychopharmacol. 16, 1165-1167. doi: 10.1017/S1461145712001071
201. Shen, H., Moussawi, K., Zhou, W., Toda, S., and Kalivas, P. W. (2011). Heroin relapse requires long-term potentiation-like plasticity mediated by NMDA2b-containing receptors. Proc. Natl. Acad. Sci. U.S.A. 108, 19407-19412. doi: 10.1073/pnas.1112052108
202. Shi, J., Li, S. X., Zhang, X. L., Wang, X., Le Foll, B., Zhang, X. Y., et al. (2009). Time-dependent neuroendocrine alterations and drug craving during the first month of abstinence in heroin addicts. Am. J. Drug Alcohol Abuse 35, 267-272. doi: 10.1080/00952990902933878
203. Sigmon, S. C., Dunn, K. E., Saulsgiver, K., Patrick, M. E., Badger, G. J., Heil, S. H., et al. (2013). A randomized, double-blind evaluation of buprenorphine taper duration in primary prescription opioid abusers. JAMA Psychiatry 70, 1347-1354. doi: 10.1001/jamapsychiatry.2013.2216
204. Snyder, G. L., Galdi, S., Fienberg, A. A., Allen, P., Nairn, A. C., and Greengard, P. (2003). Regulation of AMPA receptor dephosphorylation by glutamate receptor agonists. Neuropharmacology 45, 703-713. doi: 10.1016/S0028-3908(03)00319-8
205. Sommer, B., Kohler, M., Sprengel, R., and Seeburg, P. H. (1991). RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67, 11-19. doi: 10.1016/0092-8674(91)90568-J
206. Song, I., and Huganir, R. L. (2002). Regulation of AMPA receptors during synaptic plasticity. Trends Neurosci. 25, 578-588. doi: 10.1016/S0166-2236(02)02270-1
207. Spijker, S., Houtzager, S. W., De Gunst, M. C., De Boer, W. P., Schoffelmeer, A. N., and Smit, A. B. (2004). Morphine exposure and abstinence define specific stages of gene expression in the rat nucleus accumbens. FASEB J. 18, 848-850. doi: 10.1096/fj.03-0612fje
208. Stewart, J., De Wit, H., and Eikelboom, R. (1984). Role of unconditioned and conditioned drug effects in the self-administration of opiates and stimulants. Psychol. Rev. 91, 251-268. doi: 10.1037/0033-295X.91.2.251
209. Stinus, L., Le Moal, M., and Koob, G. F. (1990). Nucleus accumbens and amygdala are possible substrates for the aversive stimulus effects of opiate withdrawal. Neuroscience 37, 767-773. doi: 10.1016/0306-4522(90)90106-E
210. Straub, C., and Tomita, S. (2012). The regulation of glutamate receptor trafficking and function by TARPs and other transmembrane auxiliary subunits. Curr. Opin. Neurobiol. 22, 488-495. doi: 10.1016/j.conb.2011.09.005
211. Surmeier, D. J., Ding, J., Day, M., Wang, Z., and Shen, W. (2007). D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci. 30, 228-235. doi: 10.1016/j.tins.2007.03.008
212. Suto, N., Wise, R. A., and Vezina, P. (2011). Dorsal as well as ventral striatal lesions affect levels of intravenous cocaine and morphine self-administration in rats. Neurosci. Lett. 493, 29-32. doi: 10.1016/j.neulet.2011.02.011
213. Svingos, A. L., Garzon, M., Colago, E. E., and Pickel, V. M. (2001). Mu-opioid receptors in the ventral tegmental area are targeted to presynaptically and directly modulate mesocortical projection neurons. Synapse 41, 221-229. doi: 10.1002/syn.1079
214. Swanson, L. W. (1982). The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res. Bull. 9, 321-353. doi: 10.1016/0361-9230(82)90145-9
215. Takahashi, T., Svoboda, K., and Malinow, R. (2003). Experience strengthening transmission by driving AMPA receptors into synapses. Science 299, 1585-1588. doi: 10.1126/science.1079886
216. Tang, Y. P., Shimizu, E., Dube, G. R., Rampon, C., Kerchner, G. A., Zhuo, M., et al. (1999). Genetic enhancement of learning and memory in mice. Nature 401, 63-69. doi: 10.1038/43432
217. Tenorio, G., Connor, S. A., Guevremont, D., Abraham, W. C., Williams, J., O'Dell, T. J., et al. (2010). 'Silent' priming of translation-dependent LTP by ss-adrenergic receptors involves phosphorylation and recruitment of AMPA receptors. Learn. Mem. 17, 627-638. doi: 10.1101/lm.1974510
218. Tepper, J. M., Martin, L. P., and Anderson, D. R. (1995). GABAA receptor-mediated inhibition of rat substantia nigra dopaminergic neurons by pars reticulata projection neurons. J. Neurosci. 15, 3092-3103.
219. Terwilliger, R. Z., Beitner-Johnson, D., Sevarino, K. A., Crain, S. M., and Nestler, E. J. (1991). A general role for adaptations in G-proteins and the cyclic AMP system in mediating the chronic actions of morphine and cocaine on neuronal function. Brain Res. 548, 100-110. doi: 10.1016/0006-8993(91)91111-D
220. The National Center on Addiction and Substance Abuse, Columbia University. (2011). Adolescent Substance Use: America's #1 Public Health Problem. New York: Columbia University.
221. Todtenkopf, M. S., Parsegian, A., Naydenov, A., Neve, R. L., Konradi, C., and Carlezon, W. A. Jr. (2006). Brain reward regulated by AMPA receptor subunits in nucleus accumbens shell. J. Neurosci. 26, 11665-11669. doi: 10.1523/JNEUROSCI.3070-06.2006
222. Tokuyama, S., Wakabayashi, H., and Ho, I. K. (1996). Direct evidence for a role of glutamate in the expression of the opioid withdrawal syndrome. Eur. J. Pharmacol. 295, 123-129. doi: 10.1016/0014-2999(95)00645-1
223. Trujillo, K. A. (2002). The neurobiology of opiate tolerance, dependence and sensitization: mechanisms of NMDA receptor-dependent synaptic plasticity. Neurotox. Res. 4, 373-391. doi: 10.1080/10298420290023954
224. Trujillo, K. A., and Akil, H. (1991). Inhibition of morphine tolerance and dependence by the NMDA receptor antagonist MK-801. Science 251, 85-87. doi: 10.1126/science.1824728
225. Turrigiano, G. G. (2008). The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135, 422-435. doi: 10.1016/j.cell.2008.10.008
226. Ungless, M. A., Whistler, J. L., Malenka, R. C., and Bonci, A. (2001). Single cocaine exposure in vivo induces long-term potentiation in dopamine neurons. Nature 411, 583-587. doi: 10.1038/35079077
227. Vaccarino, F. J., Bloom, F. E., and Koob, G. F. (1985). Blockade of nucleus accumbens opiate receptors attenuates intravenous heroin reward in the rat. Psychopharmacology (Berl.) 86, 37-42. doi: 10.1007/BF00431681
228. Van Vliet, B. J., De Vries, T. J., Wardeh, G., Mulder, A. H., and Schoffelmeer, A. N. (1991). mu-Opioid receptor-regulated adenylate cyclase activity in primary cultures of rat striatal neurons upon chronic morphine exposure. Eur. J. Pharmacol. 208, 105-111. doi: 10.1016/0922-4106(91)90060-U
229. Vekovischeva, O. Y., Zamanillo, D., Echenko, O., Seppala, T., Uusi-Oukari, M., Honkanen, A., et al. (2001). Morphine-induced dependence and sensitization are altered in mice deficient in AMPA-type glutamate receptor-A subunits. J. Neurosci. 21, 4451-4459.
230. Volman, S. F., Lammel, S., Margolis, E. B., Kim, Y., Richard, J. M., Roitman, M. F., et al. (2013). New insights into the specificity and plasticity of reward and aversion encoding in the mesolimbic system. J. Neurosci. 33, 17569-17576. doi: 10.1523/JNEUROSCI.3250-13.2013
231. Waldhoer, M., Bartlett, S. E., and Whistler, J. L. (2004). Opioid receptors. Annu. Rev. Biochem. 73, 953-990. doi: 10.1146/annurev.biochem.73.011303.073940
232. Weiner, D. M., Levey, A. I., Sunahara, R. K., Niznik, H. B., O'Dowd, B. F., Seeman, P., et al. (1991). D1 and D2 dopamine receptor mRNA in rat brain. Proc. Natl. Acad. Sci. U.S.A. 88, 1859-1863. doi: 10.1073/pnas.88.5.1859
233. Weinshenker, D., and Schroeder, J. P. (2007). There and back again: a tale of norepinephrine and drug addiction. Neuropsychopharmacology 32, 1433-1451. doi: 10.1038/sj.npp.1301263
234. Weiss, R. D., Potter, J. S., Fiellin, D. A., Byrne, M., Connery, H. S., Dickinson, W., et al. (2011). Adjunctive counseling during brief and extended buprenorphine-naloxone treatment for prescription opioid dependence: a 2-phase randomized controlled trial. Arch. Gen. Psychiatry 68, 1238-1246. doi: 10.1001/archgenpsychiatry.2011.121
235. Wenthold, R. J., Petralia, R. S., Blahos, J., Ii., and Niedzielski, A. S. (1996). Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons. J. Neurosci. 16, 1982-1989.
236. Wheeler, R. A., and Carelli, R. M. (2009). Dissecting motivational circuitry to understand substance abuse. Neuropharmacology 56(Suppl. 1), 149-159. doi: 10.1016/j.neuropharm.2008.06.028
237. Wikler, A. (1973). Dynamics of drug dependence. Implications of a conditioning theory for research and treatment. Arch. Gen. Psychiatry 28, 611-616. doi: 10.1001/archpsyc.1973.01750350005001
238. Williams, J. T., Christie, M. J., and Manzoni, O. (2001). Cellular and synaptic adaptations mediating opioid dependence. Physiol. Rev. 81, 299-343.
239. Williams, J. T., Ingram, S. L., Henderson, G., Chavkin, C., Von Zastrow, M., Schulz, S., et al. (2013). Regulation of mu-opioid receptors: desensitization, phosphorylation, internalization, and tolerance. Pharmacol. Rev. 65, 223-254. doi: 10.1124/pr.112.005942
240. Wilson, C. J., and Groves, P. M. (1980). Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: a study employing intracellular inject of horseradish peroxidase. J. Comp. Neurol. 194, 599-615. doi: 10.1002/cne.901940308
241. Wise, R. A. (1989). Opiate reward: sites and substrates. Neurosci. Biobehav. Rev. 13, 129-133. doi: 10.1016/S0149-7634(89)80021-1
242. Wise, R. A. (2004). Dopamine, learning and motivation. Nat. Rev. Neurosci. 5, 483-494. doi: 10.1038/nrn1406
243. Wolf, M. E. (2010). Regulation of AMPA receptor trafficking in the nucleus accumbens by dopamine and cocaine. Neurotox. Res. 18, 393-409. doi: 10.1007/s12640-010-9176-0
244. Wolf, M. E., Mangiavacchi, S., and Sun, X. (2003). Mechanisms by which dopamine receptors may influence synaptic plasticity. Ann. N. Y. Acad. Sci. 1003, 241-249. doi: 10.1196/annals.1300.015
245. Wolf, M. E., Sun, X., Mangiavacchi, S., and Chao, S. Z. (2004). Psychomotor stimulants and neuronal plasticity. Neuropharmacology 47(Suppl. 1), 61-79. doi: 10.1016/j.neuropharm.2004.07.006
246. Woody, G. E., Poole, S. A., Subramaniam, G., Dugosh, K., Bogenschutz, M., Abbott, P., et al. (2008). Extended vs short-term buprenorphine-naloxone for treatment of opioid-addicted youth: a randomized trial. JAMA 300, 2003-2011. doi: 10.1001/jama.2008.574
247. Xi, Z. X., and Stein, E. A. (2002). Blockade of ionotropic glutamatergic transmission in the ventral tegmental area reduces heroin reinforcement in rat. Psychopharmacology (Berl.) 164, 144-150. doi: 10.1007/s00213-002-1190-3
248. Yuferov, V., Fussell, D., Laforge, K. S., Nielsen, D. A., Gordon, D., Ho, A., et al. (2004). Redefinition of the human kappa opioid receptor gene (OPRK1) structure and association of haplotypes with opiate addiction. Pharmacogenetics 14, 793-804. doi: 10.1097/00008571-200412000-00002
249. Zahm, D. S., and Brog, J. S. (1992). On the significance of subterritories in the "accumbens" part of the rat ventral striatum. Neuroscience 50, 751-767. doi: 10.1016/0306-4522(92)90202-D
250. Zahm, D. S., and Heimer, L. (1990). Two transpallidal pathways originating in the rat nucleus accumbens. J. Comp. Neurol. 302, 437-446. doi: 10.1002/cne.903020302
251. Zito, K. A., Vickers, G., and Roberts, D. C. (1985). Disruption of cocaine and heroin self-administration following kainic acid lesions of the nucleus accumbens. Pharmacol. Biochem. Behav. 23, 1029-1036. doi: 10.1016/0091-3057(85)90110-8
252. Zullino, D. F., Krenz, S., Zimmerman, G., Miozzari, A., Rajeswaran, R., Kolly, S., et al. (2004). Topiramate in opiate withdrawal - comparison with clonidine and with carbamazepine/mianserin. Subst. Abus. 25, 27-33. doi: 10.1300/J465v25n04_04