Role of corticostriatal circuits in context-induced reinstatement of drug seeking

Brain Research

Volumn 1628, Issue , 2015, Pages 219-232

  Marchant, Nathan J ^a,b   Kaganovsky, Konstantin ^a   Shaham, Yavin ^a   Bossert, Jennifer M ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Abstinence; Alcohol; Cocaine; Context; Craving; Cue; Drug self administration; Extinction; Heroin; Punishment; Reinstatement; Relapse; Review

Indexed keywords

ALCOHOL; BETA GALACTOSIDASE; COCAINE; DIAMORPHINE; DOPAMINE 1 RECEPTOR; GLUTAMATE RECEPTOR;

BASOLATERAL AMYGDALA; BRAIN REGION; CONNECTOME; CORTICOSTRIATAL CIRCUIT; DOPAMINERGIC TRANSMISSION; DORSAL HIPPOCAMPUS; DRUG SEEKING BEHAVIOR; DRUG SELF ADMINISTRATION; DRUG USE; HUMAN; MESOLIMBIC DOPAMINERGIC SYSTEM; NONHUMAN; NUCLEUS ACCUMBENS; NUCLEUS ACCUMBENS SHELL; PREFRONTAL CORTEX; PRIORITY JOURNAL; PUNISHMENT; REVIEW; VENTRAL HIPPOCAMPUS; ANIMAL; BRAIN CORTEX; CORPUS STRIATUM; DRUG DEPENDENCE; NERVE TRACT; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CEREBRAL CORTEX; CORPUS STRIATUM; DRUG-SEEKING BEHAVIOR; HUMANS; NEURAL PATHWAYS; SUBSTANCE-RELATED DISORDERS;

EID: 84959464843     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2014.09.004     Document Type: Review

References (140)

1. P. Backstrom, and P. Hyytia Involvement of AMPA/kainate, NMDA, and mGlu5 receptors in the nucleus accumbens core in cue-induced reinstatement of cocaine seeking in rats Psychopharmacology 192 2007 571 580
2. A. Badiani, D. Belin, D.H. Epstein, D.J. Calu, and Y. Shaham Opiate versus psychostimulant addiction: the differences do matter Nat. Rev. Neurosci. 12 2011 685 700
3. A. Badiani Substance-specific environmental influences on drug use and drug preference in animals and humans Curr. Opin. Neurobiol. 23 2013 588 596
4. M.A. Baptista, R. Martin-Fardon, and F. Weiss Preferential effects of the metabotropic glutamate 2/3 receptor agonist LY379268 on conditioned reinstatement versus primary reinforcement: comparison between cocaine and a potent conventional reinforcer J. Neurosci. 24 2004 4723 4727
5. R.M. Beckstead, V.B. Domesick, and W.J. Nauta Efferent connections of the substantia nigra and ventral tegmental area in the rat Brain Res. 175 1979 191 217
6. J.M. Bossert, S.Y. Liu, L. Lu, and Y. Shaham A role of ventral tegmental area glutamate in contextual cue-induced relapse to heroin seeking J. Neurosci. 24 2004 10726 10730
7. J.M. Bossert, R.F. Busch, and S.M. Gray The novel mGluR2/3 agonist LY379268 attenuates cue-induced reinstatement of heroin seeking Neuroreport 16 2005 1013 1016
8. J.M. Bossert, S.M. Gray, L. Lu, and Y. Shaham Activation of group II metabotropic glutamate receptors in the nucleus accumbens shell attenuates context-induced relapse to heroin seeking Neuropsychopharmacology 31 2006 2197 2209
9. J.M. Bossert, G.C. Poles, S.I. Sheffler-Collins, and U.E. Ghitza The mGluR2/3 agonist LY379268 attenuates context- and discrete cue-induced reinstatement of sucrose seeking but not sucrose self-administration in rats Behav. Brain Res. 173 2006 148 152
10. J.M. Bossert, G.C. Poles, K.A. Wihbey, E. Koya, and Y. Shaham Differential effects of blockade of dopamine D1-family receptors in nucleus accumbens core or shell on reinstatement of heroin seeking induced by contextual and discrete cues J. Neurosci. 27 2007 12655 12663
11. J.M. Bossert, K.A. Wihbey, C.L. Pickens, S.G. Nair, and Y. Shaham Role of dopamine D(1)-family receptors in dorsolateral striatum in context-induced reinstatement of heroin seeking in rats Psychopharmacology 206 2009 51 60
12. J.M. Bossert, A.L. Stern, F.R. Theberge, C. Cifani, E. Koya, B.T. Hope, and Y. Shaham Ventral medial prefrontal cortex neuronal ensembles mediate context-induced relapse to heroin Nat. Neurosci. 14 2011 420 422
13. J.M. Bossert, A.L. Stern, F.R. Theberge, N.J. Marchant, H.L. Wang, M. Morales, and Y. Shaham Role of projections from ventral medial prefrontal cortex to nucleus accumbens shell in context-induced reinstatement of heroin seeking J. Neurosci. 32 2012 4982 4991
14. J.M. Bossert, N.J. Marchant, D.J. Calu, and Y. Shaham The reinstatement model of drug relapse: recent neurobiological findings, emerging research topics, and translational research Psychopharmacology 229 2013 453 476
15. J.M. Bossert, and A.L. Stern Role of ventral subiculum in context-induced reinstatement of heroin seeking in rats Addict. Biol. 19 2014 338 342
16. M.E. Bouton, and R.C. Bolles Role of conditioned contextual stimuli in reinstatement of extinguished fear J. Exp. Psychol. Anim. Behav. Process. 5 1979 368 378
17. M.E. Bouton, and D. Swartzentruber Sources of relapse after extinction in Pavlovian and instrumental learning Clin. Psychol. Rev. 11 1991 123 140
18. M.E. Bouton Context, time, and memory retrieval in the interference paradigms of Pavlovian learning Psychol. Bull. 114 1993 80 99
19. M.E. Bouton Context, ambiguity, and unlearning: sources of relapse after behavioral extinction Biol. Psychiatry 52 2002 976 986
20. J.P. Britt, F. Benaliouad, R.A. McDevitt, G.D. Stuber, A. Wise, and A. Bonci Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens Neuron 76 2012 790 803
21. J.S. Brog, A. Salyapongse, A.Y. Deutch, and D.S. Zahm 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 1993 255 278
22. C. Burattini, T.M. Gill, G. Aicardi, and P.H. Janak The ethanol self-administration context as a reinstatement cue: acute effects of naltrexone Neuroscience 139 2006 877 887
23. S. Burman The challenge of sobriety: natural recovery without treatment and self-help groups J. Subst. Abuse 9 1997 41 61
24. D. Caprioli, M. Celentano, G. Paolone, and A. Badiani Modeling the role of environment in addiction Prog. Neuropsychopharmacol. Biol. Psychiatry 31 2007 1639 1653
25. M.D. Cassell, and D.J. Wright Topography of projections from the medial prefrontal cortex to the amygdala in the rat Brain Res. Bull. 17 1986 321 333
26. N. Chaudhri, L.L. Sahuque, J.J. Cone, and P.H. Janak Reinstated ethanol-seeking in rats is modulated by environmental context and requires the nucleus accumbens core Eur. J. Neurosci. 28 2008 2288 2298
27. N. Chaudhri, L.L. Sahuque, and P.H. Janak Ethanol seeking triggered by environmental context is attenuated by blocking dopamine D1 receptors in the nucleus accumbens core and shell in rats Psychopharmacology 207 2009 303 314
28. N. Chaudhri, L.L. Sahuque, W.W. Schairer, and P.H. Janak Separable roles of the nucleus accumbens core and shell in context- and cue-induced alcohol-seeking Neuropsychopharmacology 35 2010 783 791
29. A. Christakou, T.W. Robbins, and B.J. Everitt Prolonged neglect following unilateral disruption of a prefrontal cortical-dorsal striatal system Eur. J. Neurosci. 21 2005 782 792
30. R. Ciccocioppo, P.P. Sanna, and F. Weiss Cocaine-predictive stimulus induces drug-seeking behavior and neural activation in limbic brain regions after multiple months of abstinence: reversal by D(1) antagonists Proc. Natl. Acad. Sci. USA 98 2001 1976 1981
31. H.S. Crombag, J.W. Grimm, and Y. Shaham Effect of dopamine receptor antagonists on renewal of cocaine seeking by reexposure to drug-associated contextual cues Neuropsychopharmacology 27 2002 1006 1015
32. H.S. Crombag, and Y. Shaham Renewal of drug seeking by contextual cues after prolonged extinction in rats Behav. Neurosci. 116 2002 169 173
33. H.S. Crombag, J.M. Bossert, E. Koya, and Y. Shaham Review. Context-induced relapse to drug seeking: a review Philos. Trans. R. Soc. London B Biol. Sci. 363 2008 3233 3243
34. F.C. Cruz, K.R. Babin, R.M. Leao, E.M. Goldart, J.M. Bossert, Y. Shaham, and B.T. Hope role of nucleus accumbens shell neuronal ensembles in context-induced reinstatement of cocaine-seeking J. Neurosci. 34 2014 7437 7446
35. F.C. Cruz, E. Koya, D.H. Guez-Barber, J.M. Bossert, C.R. Lupica, Y. Shaham, and B.T. Hope New technologies for examining the role of neuronal ensembles in drug addiction and fear Nature Reviews Neuroscience 14 2013 743 754
36. H. de Wit, and J. Stewart Reinstatement of cocaine-reinforced responding in the rat Psychopharmacology 75 1981 134 143
37. H. de Wit, and J. Stewart Drug reinstatement of heroin-reinforced responding in the rat Psychopharmacology 79 1983 29 31
38. L. Diergaarde, W. de Vries, H. Raaso, A.N. Schoffelmeer, and T.J. De Vries Contextual renewal of nicotine seeking in rats and its suppression by the cannabinoid-1 receptor antagonist Rimonabant (SR141716A) Neuropharmacology 55 2008 712 716
39. D.H. Epstein, K.L. Preston, J. Stewart, and Y. Shaham Toward a model of drug relapse: an assessment of the validity of the reinstatement procedure Psychopharmacology 189 2006 1 16
40. A. Ettenberg Opponent process properties of self-administered cocaine Neurosci. Biobehav. Rev. 27 2004 721 728
41. A. Ettenberg The runway model of drug self-administration Pharmacol. Biochem. Behav. 91 2009 271 277
42. J.H. Fallon, and R.Y. Moore Catecholamine innervation of the basal forebrain. IV. Topography of the dopamine projection to the basal forebrain and neostriatum J. Comp. Neurol. 180 1978 545 580
43. R.A. Fuchs, K.A. Evans, M.C. Parker, and R.E. See Differential involvement of the core and shell subregions of the nucleus accumbens in conditioned cue-induced reinstatement of cocaine seeking in rats Psychopharmacology 176 2004 459 465
44. R.A. Fuchs, K.A. Evans, C.C. Ledford, M.P. Parker, J.M. Case, R.H. Mehta, and R.E. See The role of the dorsomedial prefrontal cortex, basolateral amygdala, and dorsal hippocampus in contextual reinstatement of cocaine seeking in rats Neuropsychopharmacology 30 2005 296 309
45. R.A. Fuchs, R.K. Branham, and R.E. See Different neural substrates mediate cocaine seeking after abstinence versus extinction training: a critical role for the dorsolateral caudate-putamen J. Neurosci. 26 2006 3584 3588
46. R.A. Fuchs, J.L. Eaddy, Z.I. Su, and G.H. Bell Interactions of the basolateral amygdala with the dorsal hippocampus and dorsomedial prefrontal cortex regulate drug context-induced reinstatement of cocaine-seeking in rats Eur. J. Neurosci. 26 2007 487 498
47. R.A. Fuchs, D.R. Ramirez, and G.H. Bell Nucleus accumbens shell and core involvement in drug context-induced reinstatement of cocaine seeking in rats Psychopharmacology 200 2008 545 556
48. D. Gaffan, E.A. Murray, and M. Fabre-Thorpe Interaction of the amygdala with the frontal lobe in reward memory Eur. J. Neurosci. 5 1993 968 975
49. S. Geisler, C. Derst, R.W. Veh, and D.S. Zahm Glutamatergic afferents of the ventral tegmental area in the rat J. Neurosci. 27 2007 5730 5743
50. H.T. Ghashghaei, and H. Barbas Pathways for emotion: interactions of prefrontal and anterior temporal pathways in the amygdala of the Rhesus monkey Neuroscience 115 2002 1261 1279
51. U.E. Ghitza, A.T. Fabbricatore, V. Prokopenko, A.P. Pawlak, and M.O. West Persistent cue-evoked activity of accumbens neurons after prolonged abstinence from self-administered cocaine J. Neurosci. 23 2003 7239 7245
52. R.M. Gold Aphagia and adipsia produced by unilateral hypothalamic lesions in rats Am. J. Physiol. 211 1966 1274 1276
53. R.G. Greenslade, and S.N. Mitchell Selective action of (-)-2-oxa-4-aminobicyclo[3.1.0]hexane-4,6-dicarboxylate (LY379268), a group II metabotropic glutamate receptor agonist, on basal and phencyclidine-induced dopamine release in the nucleus accumbens shell Neuropharmacology 47 2004 1 8
54. H.J. Groenewegen, E. Vermeulen-Van der Zee, A. te Kortschot, and M.P. Witter 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 1987 103 120
55. H.J. Groenewegen, C.I. Wright, A.V. Beijer, and P. Voorn Convergence and segregation of ventral striatal inputs and outputs Ann. N. Y. Acad. Sci. 877 1999 49 63
56. A.S. Hamlin, K.E. Blatchford, and G.P. McNally Renewal of an extinguished instrumental response: neural correlates and the role of D1 dopamine receptors Neuroscience 143 2006 25 38
57. A.S. Hamlin, J. Newby, and G.P. McNally The neural correlates and role of D1 dopamine receptors in renewal of extinguished alcohol-seeking Neuroscience 146 2007 525 536
58. A.S. Hamlin, K.J. Clemens, and G.P. McNally Renewal of extinguished cocaine-seeking Neuroscience 151 2008 659 670
59. A.S. Hamlin, K.J. Clemens, E.A. Choi, and G.P. McNally Paraventricular thalamus mediates context-induced reinstatement (renewal) of extinguished reward seeking Eur. J. Neurosci. 29 2009 802 812
60. P.C. Holland Occasion setting in Pavlovian conditioning D.L. Medlin, The Psychology of Learning and Motivation 1992 Academic Press San Diego, CA 69 125
61. P.C. Holland, and M.E. Bouton Hippocampus and context in classical conditioning Curr. Opin. Neurobiol. 9 1999 195 202
62. W.A. Hunt, L.W. Barnett, and L.G. Branch Relapse rates in addiction programs J. Clin. Psychol. 27 1971 455 456
63. J.L. Katz, and S.T. Higgins The validity of the reinstatement model of craving and relapse to drug use Psychopharmacology 168 2003 21 30
64. A.E. Kelley, V.B. Domesick, and W.J. Nauta The amygdalostriatal projection in the rat - an anatomical study by anterograde and retrograde tracing methods Neuroscience 7 1982 615 630
65. H.K.H. Klingemann The motivation for change from problem alcohol and heroin use Br. J. Addict. 86 1991 727 744
66. E. Koya, S.A. Golden, B.K. Harvey, D.H. Guez-Barber, A. Berkow, D.E. Simmons, J.M. Bossert, S.G. Nair, J.L. Uejima, M.T. Marin, and et al. Targeted disruption of cocaine-activated nucleus accumbens neurons prevents context-specific sensitization Nat. Neurosci. 12 2009 1069 1073
67. V. Kumaresan, M. Yuan, J. Yee, K.R. Famous, S.M. Anderson, H.D. Schmidt, and R.C. Pierce Metabotropic glutamate receptor 5 (mGluR5) antagonists attenuate cocaine priming- and cue-induced reinstatement of cocaine seeking Behav. Brain Res. 202 2009 238 244
68. R.T. LaLumiere, and P.W. Kalivas Glutamate release in the nucleus accumbens core is necessary for heroin seeking J. Neurosci. 28 2008 3170 3317
69. H.C. Lasseter, D.R. Ramirez, X. Xie, and R.A. Fuchs Involvement of the lateral orbitofrontal cortex in drug context-induced reinstatement of cocaine-seeking behavior in rats Eur. J. Neurosci. 30 2009 1370 1381
70. H.C. Lasseter, X. Xie, D.R. Ramirez, and R.A. Fuchs Sub-region specific contribution of the ventral hippocampus to drug context-induced reinstatement of cocaine-seeking behavior in rats Neuroscience 171 2010 830 839
71. H.C. Lasseter, A.M. Wells, X. Xie, and R.A. Fuchs Interaction of the basolateral amygdala and orbitofrontal cortex is critical for drug context-induced reinstatement of cocaine-seeking behavior in rats Neuropsychopharmacology 36 2011 711 720
72. H.C. Lasseter, X. Xie, A.A. Arguello, A.M. Wells, M.A. Hodges, and R.A. Fuchs Contribution of a mesocorticolimbic subcircuit to drug context-induced reinstatement of cocaine-seeking behavior in rats Neuropsychopharmacology 39 2014 660 669
73. M.E. Liechti, L. Lhuillier, K. Kaupmann, and A. Markou Metabotropic glutamate 2/3 receptors in the ventral tegmental area and the nucleus accumbens shell are involved in behaviors relating to nicotine dependence J. Neurosci. 27 2007 9077 9085
74. A.H. Luo, P. Tahsili-Fahadan, R.A. Wise, C.R. Lupica, and G. Aston-Jones Linking context with reward: a functional circuit from hippocampal CA3 to ventral tegmental area Science 333 2011 353 357
75. O.J. Manzoni, and J.T. Williams Presynaptic regulation of glutamate release in the ventral tegmental area during morphine withdrawal J. Neurosci. 19 1999 6629 6636
76. N.J. Marchant, A.S. Hamlin, and G.P. McNally Lateral hypothalamus is required for context-induced reinstatement of extinguished reward seeking J. Neurosci. 29 2009 1331 1342
77. N.J. Marchant, T.N. Khuc, C.L. Pickens, A. Bonci, and Y. Shaham Context-induced relapse to alcohol seeking after punishment in a rat model Biol. Psychiatry 73 2013 256 262
78. N.J. Marchant, X. Li, and Y. Shaham Recent developments in animal models of drug relapse Curr. Opin. Neurobiol. 23 2013 675 683
79. N.J. Marchant, R. Rabei, K. Kaganovsky, D. Caprioli, J.M. Bossert, A. Bonci, and Y. Shaham A critical role of lateral hypothalamus in context-induced relapse to alcohol seeking after punishment-imposed abstinence J. Neurosci. 34 2014 7447 7457
80. P.W. Marinelli, D. Funk, W. Juzytsch, Z. Li, and A.D. Le Effects of opioid receptor blockade on the renewal of alcohol seeking induced by context: relationship to c-fos mRNA expression Eur. J. Neurosci. 26 2007 2815 2823
81. P.W. Marinelli, D. Funk, W. Juzytsch, and A.D. Le Opioid receptors in the basolateral amygdala but not dorsal hippocampus mediate context-induced alcohol seeking Behav. Brain Res. 211 2010 58 63
82. G.A. Marlatt Do animal models provide a valid analogue for human drug lapse and relapse? Comment on Leri and Stewart (2002) Exp. Clin. Psychopharmacol. 10 2002 359 360
83. A.J. McDonald Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain Neuroscience 44 1991 15 33
84. A.J. McDonald, F. Mascagni, and L. Guo Projections of the medial and lateral prefrontal cortices to the amygdala: a Phaseolus vulgaris leucoagglutinin study in the rat Neuroscience 71 1996 55 75
85. A.J. McDonald Cortical pathways to the mammalian amygdala Prog. Neurobiol. 55 1998 257 332
86. K. McFarland, and A. Ettenberg Reinstatement of drug-seeking behavior produced by heroin-predictive environmental stimuli Psychopharmacology 131 1997 86 92
87. J. McLaughlin, and R.E. See Selective inactivation of the dorsomedial prefrontal cortex and the basolateral amygdala attenuates conditioned-cued reinstatement of extinguished cocaine-seeking behavior in rats Psychopharmacology 168 2003 57 65
88. G.P. McNally Extinction of drug seeking: neural circuits and approaches to augmentation Neuropharmacology 76 Pt B 2014 528 532
89. W.M. Meil, and R.E. See Conditioned cued recovery of responding following prolonged withdrawal from self-administered cocaine in rats: an animal model of relapse Behav. Pharmacol. 7 1996 754 763
90. W.M. Meil, and R.E. See Conditioned cued recovery of responding following prolonged withdrawal from self-administered cocaine in rats: an animal model of relapse Behav. Pharmacol. 7 1996 754 763
91. E.Z. Millan, T.M. Furlong, and G.P. McNally Accumbens shell-hypothalamus interactions mediate extinction of alcohol seeking J. Neurosci. 30 2010 4626 4635
92. E.Z. Millan, and G.P. McNally Accumbens shell AMPA receptors mediate expression of extinguished reward seeking through interactions with basolateral amygdala Learn. Mem. 18 2011 414 421
93. E.Z. Millan, and G.P. McNally Cocaine- and amphetamine-regulated transcript in the nucleus accumbens shell attenuates context-induced reinstatement of alcohol seeking Behav. Neurosci. 126 2012 690 698
94. J.I. Morgan, and T. Curran Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun Ann. Rev. Neurosci. 14 1991 421 451
95. S. Nakajima, S. Tanaka, K. Urushihara, and H. Imada renewal of extinguished lever-press responses upon return to the training context Learn. Motiv. 31 2000 416 431
96. C.P. O'Brien, A.R. Childress, A.T. McLellan, and R. Ehrman Classical conditioning in drug-dependent humans Ann. N. Y. Acad. Sci. 654 1992 400 415
97. C.P. O'Brien Anticraving medications for relapse prevention: a possible new class of psychoactive medications Am. J. Psychiatry 162 2005 1423 1431
98. R.D. Oades, and G.M. Halliday Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity Brain Res. 434 1987 117 165
99. C.J. Perry, and G.P. McNally mu-Opioid receptors in the nucleus accumbens shell mediate context-induced reinstatement (renewal) but not primed reinstatement of extinguished alcohol seeking Behav. Neurosci. 127 2013 535 543
100. J. Peters, R.T. LaLumiere, and P.W. Kalivas Infralimbic prefrontal cortex is responsible for inhibiting cocaine seeking in extinguished rats J. Neurosci. 28 2008 6046 6053
101. J. Peters, P.W. Kalivas, and G.J. Quirk Extinction circuits for fear and addiction overlap in prefrontal cortex Learn. Mem. 16 2009 279 288
102. C.L. Pickens, M. Airavaara, F. Theberge, S. Fanous, B.T. Hope, and Y. Shaham Neurobiology of the incubation of drug craving Trends Neurosci. 34 2011 411 420
103. A. Pitkanen Connectivity of the rat amygdaloid complex J.P. Aggelton, The Amygdala: A Functional Analysis 2000 Oxford University Press Oxford, U.K. 31 115
104. R.A. Rescorla, P.J. Durlach, and J.W. Grau Contextual learning in Pavlovian conditioning P. Balsam, A. Tomie, Context and Learning 1985 Erlbaum Hillsdale, NJ 23 56
105. L.N. Robins, D.H. Davis, and D.W. Goodwin Drug use by U.S. Army enlisted men in Vietnam: a follow-up on their return home Am. J. Epidemiol. 99 1974 235 249
106. J.L. Rogers, S. Ghee, and R.E. See The neural circuitry underlying reinstatement of heroin-seeking behavior in an animal model of relapse Neuroscience 151 2008 579 588
107. S.T. Rouse, M.J. Marino, S.R. Bradley, H. Awad, M. Wittmann, and P.J. Conn Distribution and roles of metabotropic glutamate receptors in the basal ganglia motor circuit: implications for treatment of Parkinson's disease and related disorders Pharmacol. Ther. 88 2000 427 435
108. D.D. Schoepp Unveiling the functions of presynaptic metabotropic glutamate receptors in the central nervous system J. Pharmacol. Exp. Ther. 299 2001 12 20
109. D.W. Self, W.J. Barnhart, D.A. Lehman, and E.J. Nestler Opposite modulation of cocaine-seeking behavior by D1- and D2-like dopamine receptor agonists Science 271 1996 1586 1589
110. S.R. Sesack, A.Y. Deutch, R.H. Roth, and B.S. Bunney Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin J. Comp. Neurol. 290 1989 213 242
111. S.R. Sesack, D.B. Carr, N. Omelchenko, and A. Pinto Anatomical substrates for glutamate-dopamine interactions: evidence for specificity of connections and extrasynaptic actions Ann. N. Y. Acad. Sci. 1003 2003 36 52
112. B. Setlow, P.C. Holland, and M. Gallagher Disconnection of the basolateral amygdala complex and nucleus accumbens impairs appetitive pavlovian second-order conditioned responses Behav. Neurosci. 116 2002 267 275
113. Y. Shaham, and J. Stewart Stress reinstates heroin-seeking in drug-free animals: an effect mimicking heroin, not withdrawal Psychopharmacology 119 1995 334 341
114. Y. Shaham, and J. Stewart Effects of opioid and dopamine receptor antagonists on relapse induced by stress and re-exposure to heroin in rats Psychopharmacology 125 1996 385 391
115. Y. Shaham, S. Erb, and J. Stewart Stress-induced relapse to heroin and cocaine seeking in rats: a review Brain Res. Rev. 33 2000 13 33
116. U. Shalev, J. Yap, and Y. Shaham Leptin attenuates acute food deprivation-induced relapse to heroin seeking J. Neurosci. 21 2001 RC129
117. U. Shalev, J.W. Grimm, and Y. Shaham Neurobiology of relapse to heroin and cocaine seeking: a review Pharmacol. Rev. 54 2002 1 42
118. Y. Shinonaga, M. Takada, and N. Mizuno Topographic organization of collateral projections from the basolateral amygdaloid nucleus to both the prefrontal cortex and nucleus accumbens in the rat Neuroscience 58 1994 389 397
119. C.M. Sinclair, R.M. Cleva, L.E. Hood, M.F. Olive, and J.T. Gass mGluR5 receptors in the basolateral amygdala and nucleus accumbens regulate cue-induced reinstatement of ethanol-seeking behavior Pharmacol. Biochem. Behav. 101 2012 329 335
120. R. Sinha, Y. Shaham, and M. Heilig Translational and reverse translational research on the role of stress in drug craving and relapse Psychopharmacology (Berl) 218 2011 69 82
121. R.D. Spealman, R.L. Barrett-Larimore, J.K. Rowlett, D.M. Platt, and T.V. Khroyan Pharmacological and environmental determinants of relapse to cocaine-seeking behavior Pharmacol. Biochem. Behav. 64 1999 327 336
122. N.M. Stankeviciute, M.D. Scofield, P.W. Kalivas, and C.D. Gipson Rapid, transient potentiation of dendritic spines in context-induced relapse to cocaine seeking Addict. Biol 2013 in press
123. J. Stewart Reinstatement of heroin and cocaine self-administration behavior in the rat by intracerebral application of morphine in the ventral tegmental area Pharmacol. Biochem. Behav. 20 1984 917 923
124. S.T. Tiffany, and C.A. Conklin The promise and pitfalls of animal and human models of relapse: comment on Leri and Stewart (2002) Exp. Clin. Psychopharmacol. 10 2002 361 363
125. G.P. Urcelay, and R.R. Miller The functions of contexts in associative learning Behav. Process. 104 2014 2 12
126. I. Usuda, K. Tanaka, and T. Chiba Efferent projections of the nucleus accumbens in the rat with special reference to subdivision of the nucleus: biotinylated dextran amine study Brain Res. 797 1998 73 93
127. J. Vandergriff, and K. Rasmussen The selective mGlu2/3 receptor agonist LY354740 attenuates morphine-withdrawal-induced activation of locus coeruleus neurons and behavioral signs of morphine withdrawal Neuropharmacology 38 1999 217 222
128. F. Weiss, C.S. Maldonado-Vlaar, L.H. Parsons, T.M. Kerr, D.L. Smith, and O. Ben-Shahar Control of cocaine-seeking behavior by drug-associated stimuli in rats: effects on recovery of extinguished operant-responding and extracellular dopamine levels in amygdala and nucleus accumbens Proc. Natl. Acad. Sci. USA 97 2000 4321 4326
129. F. Weiss, R. Martin-Fardon, R. Ciccocioppo, T.M. Kerr, D.L. Smith, and O. Ben-Shahar Enduring resistance to extinction of cocaine-seeking behavior induced by drug-related cues Neuropsychopharmacology 25 2001 361 372
130. J.J. Widholm, J.T. Gass, R.M. Cleva, and M.F. Olive The mGluR5 positive allosteric modulator CDPPB does not alter extinction or contextual reinstatement of methamphetamine-seeking behavior in rats J. Addict. Res. Ther. S1 2011 S1 S12
131. A. Wikler Dynamics of drug dependence. Implications of a conditioning theory for research and treatment Arch. Gen. Psychiatry 28 1973 611 616
132. A.L. Willcocks, and G.P. McNally The role of medial prefrontal cortex in extinction and reinstatement of alcohol-seeking in rats Eur. J. Neurosci 37 2012 259 268
133. V.C. Wing, and M. Shoaib Contextual stimuli modulate extinction and reinstatement in rodents self-administering intravenous nicotine Psychopharmacology 200 2008 357 365
134. R.A. Wise Opiate reward: sites and substrates Neurosci. Biobehav. Rev. 13 1989 129 133
135. X. Xie, D.R. Ramirez, H.C. Lasseter, and R.A. Fuchs Effects of mGluR1 antagonism in the dorsal hippocampus on drug context-induced reinstatement of cocaine-seeking behavior in rats Psychopharmacology 208 2010 1 11
136. X. Xie, H.C. Lasseter, D.R. Ramirez, K.L. Ponds, A.M. Wells, and R.A. Fuchs Subregion-specific role of glutamate receptors in the nucleus accumbens on drug context-induced reinstatement of cocaine-seeking behavior in rats Addict. Biol. 17 2012 287 299
137. X. Xie, A.A. Arguello, A.M. Wells, A.M. Reittinger, and R.A. Fuchs Role of a hippocampal SRC-family kinase-mediated glutamatergic mechanism in drug context-induced cocaine seeking Neuropsychopharmacology 38 2013 2657 2665
138. X. Xie, A.M. Wells, and R.A. Fuchs Cocaine seeking and taking: role of hippocampal dopamine D1-like receptors Int. J. Neuropsychopharmacol. 9 2014 1533 1538
139. T. Yamaguchi, W. Sheen, and M. Morales Glutamatergic neurons are present in the rat ventral tegmental area Eur. J. Neurosci. 25 2007 106 118
140. T. Yamaguchi, H.L. Wang, X. Li, T.H. Ng, and M. Morales Mesocorticolimbic glutamatergic pathway J. Neurosci. 31 2011 8476 8490