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Neurochemistry Underlying Relapse to Opiate Seeking Behaviour

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Abstract

Relapse is a major clinical problem and remains a major challenge in the treatment of addictions. A goal of current research is to gain a greater understanding of the neurochemistry underlying relapse to opiate use. Factors which trigger relapse in humans such as stress, exposure to opiates and/or drug-associated cues, can also trigger opiate-seeking in animals. This review will overview preclinical studies relating to the neurochemistry of opiate-seeking with a focus on studies published from 2005 to present.

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References

  1. Darke S, Mattick R (2007) Mortality amongst illicit drug users: epidemiology causes and intervention. Cambridge University Press, Cambridge

    Google Scholar 

  2. UNODC (2008) World Drug Report, United Nations Office on Drugs and Crime

  3. Fry C (2007) Benzodiazepine and pharmaceutical opioid misuse and their relationship to crime: an examination of illlicit prescription drug markets in Melbourne. Hobart and Darwin. N. D. L. E. R. Fund, Hobart, Tasmania

    Google Scholar 

  4. SAMHSA (2007) National survey on drug use and health. department of health and human services

  5. Compton WM, Volkow ND (2006) Abuse of prescription drugs and the risk of addiction. Drug Alcohol Depend 83(Suppl 1):S4–S7. doi:10.1016/j.drugalcdep.2005.10.020

    Article  PubMed  CAS  Google Scholar 

  6. Adams K, Sandy L, Smith L, Triglone B (2007) Drug use monitoring in Australia: 2007 annual report on drug use among police detainees, Australian Institute of Criminology

  7. SAMHSA (2007) The NSDUH Report: Pattern and Trends in Nonmedical Prescription Pain Reliever Use: 2002 to 2005, Department of Health and Human Services

  8. Colliver JD, Compton WM, Gfroerer JC et al (2006) Projecting drug use among aging baby boomers in 2020. Ann Epidemiol 16:257–265. doi:10.1016/j.annepidem.2005.08.003

    Article  PubMed  Google Scholar 

  9. Christie MJ (2008) Cellular neuroadaptations to chronic opioids: tolerance, withdrawal and addiction. Br J Pharmacol 154:384–396. doi:10.1038/bjp.2008.100

    Article  PubMed  CAS  Google Scholar 

  10. Stafford J, Degenhardt E, Black R, Bruno R, Buckingham, K. (2004) Australian drug trends 2004: findings from the illicit drug reporting system (IDRS). Monograph No. 55

  11. O′Brien CP (1997) Progress in the science of addiction. Am J Psychiatry 154:1195–1197

    PubMed  Google Scholar 

  12. Kalivas PW, Volkow ND (2005) The neural basis of addiction: a pathology of motivation and choice. Am J Psychiatry 162:1403–1413. doi:10.1176/appi.ajp.162.8.1403

    Article  PubMed  Google Scholar 

  13. Gossop M, Green L, Phillips G et al (1989) Lapse, relapse and survival among opiate addicts after treatment. A prospective follow-up study. Br J Psychiatry 154:348–353. doi:10.1192/bjp.154.3.348

    Article  PubMed  CAS  Google Scholar 

  14. Hunt WA, Barnett LW, Branch LG (1971) Relapse rates in addiction programs. J Clin Psychol 27:455–456. doi:10.1002/1097-4679(197110)27:4<455::AID-JCLP2270270412>3.0.CO;2-R

    Article  PubMed  CAS  Google Scholar 

  15. Shaham Y, Shalev U, Lu L et al (2003) The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology (Berl) 168:3–20. doi:10.1007/s00213-002-1224-x

    Article  CAS  Google Scholar 

  16. Bossert JM, Ghitza UE, Lu L et al (2005) Neurobiology of relapse to heroin and cocaine seeking: an update and clinical implications. Eur J Pharmacol 526:36–50. doi:10.1016/j.ejphar.2005.09.030

    Article  PubMed  CAS  Google Scholar 

  17. Shalev U, Grimm JW, 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

    Article  PubMed  CAS  Google Scholar 

  18. Stretch R, Gerber GJ, Wood SM (1971) Factors affecting behavior maintained by response-contingent intravenous infusions of amphetamine in squirrel monkeys. Can J Physiol Pharmacol 49:581–589

    PubMed  CAS  Google Scholar 

  19. Carroll ME (1985) The role of food deprivation in the maintenance and reinstatement of cocaine-seeking behavior in rats. Drug Alcohol Depend 16:95–109. doi:10.1016/0376-8716(85)90109-7

    Article  PubMed  CAS  Google Scholar 

  20. Shaham Y, Stewart J (1995) Stress reinstates heroin-seeking in drug-free animals: an effect mimicking heroin, not withdrawal. Psychopharmacology (Berl) 119:334–341. doi:10.1007/BF02246300

    Article  CAS  Google Scholar 

  21. Davis WM, Smith SG (1976) Role of conditioned reinforcers in the initiation, maintenance and extinction of drug-seeking behavior. Pavlov J Biol Sci 11:222–236

    PubMed  CAS  Google Scholar 

  22. O′Brien C, Childress AR, Ehrman R et al (1992) Conditioning mechanisms in drug dependence. Clin Neuropharmacol 15(Suppl 1 Pt A):66A–67A

    PubMed  Google Scholar 

  23. Brown SA, Vik PW, Patterson TL et al (1995) Stress, vulnerability and adult alcohol relapse. J Stud Alcohol 56:538–545

    PubMed  CAS  Google Scholar 

  24. Epstein DH, Preston KL, Stewart J et al (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

    Article  CAS  Google Scholar 

  25. Shaham Y, Stewart J (1996) Effects of opioid and dopamine receptor antagonists on relapse induced by stress and re-exposure to heroin in rats. Psychopharmacology (Berl) 125:385–391. doi:10.1007/BF02246022

    Article  CAS  Google Scholar 

  26. Comer SD, Sullivan MA, Yu E et al (2006) Injectable, sustained-release naltrexone for the treatment of opioid dependence: a randomized, placebo-controlled trial. Arch Gen Psychiatry 63:210–218. doi:10.1001/archpsyc.63.2.210

    Article  PubMed  CAS  Google Scholar 

  27. Parker LA, McDonald RV (2000) Reinstatement of both a conditioned place preference and a conditioned place aversion with drug primes. Pharmacol Biochem Behav 66:559–561. doi:10.1016/S0091-3057(00)00222-7

    Article  PubMed  CAS  Google Scholar 

  28. Lu L, Zhang B, Liu Z et al (2002) Reactivation of cocaine conditioned place preference induced by stress is reversed by cholecystokinin-B receptors antagonist in rats. Brain Res 954:132–140. doi:10.1016/S0006-8993(02)03359-0

    Article  PubMed  CAS  Google Scholar 

  29. Contet C, Kieffer BL, Befort K (2004) Mu opioid receptor: a gateway to drug addiction. Curr Opin Neurobiol 14:370–378. doi:10.1016/j.conb.2004.05.005

    Article  PubMed  CAS  Google Scholar 

  30. Johnson SW, North RA (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12:483–488

    PubMed  CAS  Google Scholar 

  31. 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. doi:10.1073/pnas.85.14.5274

    Article  PubMed  CAS  Google Scholar 

  32. Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18:247–291. doi:10.1016/0165-0173(93)90013-P

    Article  PubMed  CAS  Google Scholar 

  33. Stewart J (1984) Reinstatement of heroin and cocaine self-administration behavior in the rat by intracerebral application of morphine in the ventral tegmental area. Pharmacol Biochem Behav 20:917–923. doi:10.1016/0091-3057(84)90017-0

    Article  PubMed  CAS  Google Scholar 

  34. Ribeiro Do Couto B, Aguilar MA, Rodríguez-Arias M, Miñarro J (2005) Cross-reinstatement by cocaine and amphetamine of morphine-induced place preference in mice. Behav Pharmacol 16:253–259

    Article  Google Scholar 

  35. Ribeiro Do Couto B, Aguilar MA, Manzanedo C et al (2005) NMDA glutamate but not dopamine antagonists blocks drug-induced reinstatement of morphine place preference. Brain Res Bull 64:493–503. doi:10.1016/j.brainresbull.2004.10.005

    Google Scholar 

  36. Wang B, Luo F, Ge XC et al (2002) Effects of lesions of various brain areas on drug priming or footshock-induced reactivation of extinguished conditioned place preference. Brain Res 950:1–9. doi:10.1016/S0006-8993(02)02980-3

    Article  PubMed  CAS  Google Scholar 

  37. Ventura R, Alcaro A, Puglisi-Allegra S (2005) Prefrontal cortical norepinephrine release is critical for morphine-induced reward, reinstatement and dopamine release in the nucleus accumbens. Cereb Cortex 15:1877–1886. doi:10.1093/cercor/bhi066

    Article  PubMed  Google Scholar 

  38. Wang J, Fang Q, Liu Z et al (2006) Region-specific effects of brain corticotropin-releasing factor receptor type 1 blockade on footshock-stress- or drug-priming-induced reinstatement of morphine conditioned place preference in rats. Psychopharmacology (Berl) 185:19–28. doi:10.1007/s00213-005-0262-6

    Article  CAS  Google Scholar 

  39. Zhou Y, Leri F, Cummins E et al (2008) Involvement of arginine vasopressin and V1b receptor in heroin withdrawal and heroin seeking precipitated by stress and by heroin. Neuropsychopharmacology 33:226–236. doi:10.1038/sj.npp.1301419

    Article  PubMed  CAS  Google Scholar 

  40. Harris GC, Wimmer M, Aston-Jones G (2005) A role for lateral hypothalamic orexin neurons in reward seeking. Nature 437:556–559. doi:10.1038/nature04071

    Article  PubMed  CAS  Google Scholar 

  41. Popik P, Wrobel M, Bisaga A (2006) Reinstatement of morphine-conditioned reward is blocked by memantine. Neuropsychopharmacology 31:160–170

    PubMed  CAS  Google Scholar 

  42. Ma YY, Chu NN, Guo CY et al (2007) NR2B-containing NMDA receptor is required for morphine-but not stress-induced reinstatement. Exp Neurol 203:309–319. doi:10.1016/j.expneurol.2006.08.014

    Article  PubMed  CAS  Google Scholar 

  43. LaLumiere RT, Kalivas PW (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

    Article  PubMed  CAS  Google Scholar 

  44. Everitt BJ, Parkinson JA, Olmstead MC et al (1999) Associative processes in addiction and reward. The role of amygdala-ventral striatal subsystems. Ann N Y Acad Sci 877:412–438. doi:10.1111/j.1749-6632.1999.tb09280.x

    Article  PubMed  CAS  Google Scholar 

  45. McFarland K, Kalivas PW (2001) The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior. J Neurosci 21:8655–8663

    PubMed  CAS  Google Scholar 

  46. Rogers JL, Ghee S, See RE (2008) The neural circuitry underlying reinstatement of heroin-seeking behavior in an animal model of relapse. Neuroscience 151:579–588. doi:10.1016/j.neuroscience.2007.10.012

    Article  PubMed  CAS  Google Scholar 

  47. Ettenberg A, Pettit HO, Bloom FE et al (1982) Heroin and cocaine intravenous self-administration in rats: mediation by separate neural systems. Psychopharmacology (Berl) 78:204–209. doi:10.1007/BF00428151

    Article  CAS  Google Scholar 

  48. De Vries TJ, Shippenberg TS (2002) Neural systems underlying opiate addiction. J Neurosci 22:3321–3325

    PubMed  Google Scholar 

  49. De Vries TJ, Schoffelmeer AN, Binnekade R et al (1998) Drug-induced reinstatement of heroin- and cocaine-seeking behaviour following long-term extinction is associated with expression of behavioural sensitization. Eur J NeuroSci 10:3565–3571. doi:10.1046/j.1460-9568.1998.00368.x

    Article  PubMed  Google Scholar 

  50. De Vries TJ, Schoffelmeer AN, Binnekade R et al (1999) Dopaminergic mechanisms mediating the incentive to seek cocaine and heroin following long-term withdrawal of IV drug self-administration. Psychopharmacology (Berl) 143:254–260. doi:10.1007/s002130050944

    Article  Google Scholar 

  51. Lenoir M, Ahmed SH (2007) Heroin-induced reinstatement is specific to compulsive heroin use and dissociable from heroin reward and sensitization. Neuropsychopharmacology 32:616–624. doi:10.1038/sj.npp.1301083

    Article  PubMed  CAS  Google Scholar 

  52. Yao L, McFarland K, Fan P et al (2005) Activator of G protein signaling 3 regulates opiate activation of protein kinase A signaling and relapse of heroin-seeking behavior. Proc Natl Acad Sci USA 102:8746–8751. doi:10.1073/pnas.0503419102

    Article  PubMed  CAS  Google Scholar 

  53. Bowers MS, McFarland K, Lake RW et al (2004) Activator of G protein signaling 3: a gatekeeper of cocaine sensitization and drug seeking. Neuron 42:269–281. doi:10.1016/S0896-6273(04)00159-X

    Article  PubMed  CAS  Google Scholar 

  54. Yao L, McFarland K, Fan P et al (2006) Adenosine A2a blockade prevents synergy between mu-opiate and cannabinoid CB1 receptors and eliminates heroin-seeking behavior in addicted rats. Proc Natl Acad Sci USA 103:7877–7882. doi:10.1073/pnas.0602661103

    Article  PubMed  CAS  Google Scholar 

  55. Pickel VM, Chan J, Kash TL et al (2004) Compartment-specific localization of cannabinoid 1 (CB1) and mu-opioid receptors in rat nucleus accumbens. Neuroscience 127:101–112. doi:10.1016/j.neuroscience.2004.05.015

    Article  PubMed  CAS  Google Scholar 

  56. Salio C, Fischer J, Franzoni MF et al (2001) CB1-cannabinoid and mu-opioid receptor co-localization on postsynaptic target in the rat dorsal horn. Neuroreport 12:3689–3692. doi:10.1097/00001756-200112040-00017

    Article  PubMed  CAS  Google Scholar 

  57. Carriba P, Ortiz O, Patkar K et al (2007) Striatal adenosine A2A and cannabinoid CB1 receptors form functional heteromeric complexes that mediate the motor effects of cannabinoids. Neuropsychopharmacology 32:2249–2259. doi:10.1038/sj.npp.1301375

    Article  PubMed  CAS  Google Scholar 

  58. Fattore L, Fadda P, Fratta W (2007) Endocannabinoid regulation of relapse mechanisms. Pharmacol Res 56:418–427. doi:10.1016/j.phrs.2007.09.004

    Article  PubMed  CAS  Google Scholar 

  59. Brown RM, Short JL (2008) Adenosine A(2A) receptors and their role in drug addiction. J Pharm Pharmacol 60:1409–1430. doi:10.1211/jpp/60.11.0001

    Article  PubMed  CAS  Google Scholar 

  60. Brown RM, Short JL, Cowen MS et al (2009) A differential role for the adenosine A2A receptor in opiate reinforcement vs opiate-seeking behavior. Neuropsychopharmacology 34(4):844–856. doi:10.1038/sj.npp.1301627

    Article  PubMed  CAS  Google Scholar 

  61. Ferre S, Diamond I, Goldberg SR et al (2007) Adenosine A2A receptors in ventral striatum, hypothalamus and nociceptive circuitry implications for drug addiction, sleep and pain. Prog Neurobiol 83:332–347. doi:10.1016/j.pneurobio.2007.04.002

    Article  PubMed  CAS  Google Scholar 

  62. Adams CL, Cowen MS, Short JL et al (2008) Combined antagonism of glutamate mGlu5 and adenosine A2A receptors interact to regulate alcohol-seeking in rats. Int J Neuropsychopharmacol 11:229–241. doi:10.1017/S1461145707007845

    Article  PubMed  CAS  Google Scholar 

  63. Spano MS, Fattore L, Fratta W et al (2007) The GABAB receptor agonist baclofen prevents heroin-induced reinstatement of heroin-seeking behavior in rats. Neuropharmacology 52:1555–1562. doi:10.1016/j.neuropharm.2007.02.012

    Article  PubMed  CAS  Google Scholar 

  64. Xi ZX, Stein EA (1999) Baclofen inhibits heroin self-administration behavior and mesolimbic dopamine release. J Pharmacol Exp Ther 290:1369–1374

    PubMed  CAS  Google Scholar 

  65. Fadda P, Scherma M, Fresu A et al (2003) Baclofen antagonizes nicotine-, cocaine-, and morphine-induced dopamine release in the nucleus accumbens of rat. Synapse 50:1–6. doi:10.1002/syn.10238

    Article  PubMed  CAS  Google Scholar 

  66. Ling W, Shoptaw S, Majewska D (1998) Baclofen as a cocaine anti-craving medication: a preliminary clinical study. Neuropsychopharmacology 18:403–404. doi:10.1016/S0893-133X(97)00128-0

    Article  PubMed  CAS  Google Scholar 

  67. Haney M, Hart CL, Foltin RW (2006) Effects of baclofen on cocaine self-administration: opioid- and nonopioid-dependent volunteers. Neuropsychopharmacology 31:1814–1821. doi:10.1038/sj.npp.1300999

    Article  PubMed  CAS  Google Scholar 

  68. Sorge RE, Rajabi H, Stewart J (2005) Rats maintained chronically on buprenorphine show reduced heroin and cocaine seeking in tests of extinction and drug-induced reinstatement. Neuropsychopharmacology 30:1681–1692. doi:10.1038/sj.npp.1300712

    Article  PubMed  CAS  Google Scholar 

  69. Sinha R, Kimmerling A, Doebrick C et al (2007) Effects of lofexidine on stress-induced and cueinduced opioid craving and opioid abstinence rates: preliminary findings. Psychopharmacology (Berl) 190:569–574. doi:10.1007/s00213-006-0640-8

  70. Hyman SM, Fox H, Hong KI et al (2007) Stress and drug-cue-induced craving in opioid-dependent individuals in naltrexone treatment. Exp Clin Psychopharmacol 15:134–143. doi:10.1037/1064-1297.15.2.134

    Article  PubMed  CAS  Google Scholar 

  71. Sinha R, Catapano D, O′Malley S (1999) Stress-induced craving and stress response in cocaine dependent individuals. Psychopharmacology (Berl) 142:343–351. doi:10.1007/s002130050898

    Article  CAS  Google Scholar 

  72. Sinha R (2001) How does stress increase risk of drug abuse and relapse? Psychopharmacology 158:343–359

    Article  PubMed  CAS  Google Scholar 

  73. Shalev U, Highfield D, Yap J et al (2000) Stress and relapse to drug seeking in rats: studies on the generality of the effect. Psychopharmacology (Berl) 150:337–346. doi:10.1007/s002130000441

    Article  CAS  Google Scholar 

  74. Shalev U, Yap J, Shaham Y (2001) Leptin attenuates acute food deprivation-induced relapse to heroin seeking. J Neurosci 21:RC129

    PubMed  CAS  Google Scholar 

  75. Shaham Y, Funk D, Erb S et al (1997) Corticotropin-releasing factor, but not corticosterone, is involved in stress-induced relapse to heroin-seeking in rats. J Neurosci 17:2605–2614

    PubMed  CAS  Google Scholar 

  76. Lee B, Tiefenbacher S, Platt DM et al (2004) Pharmacological blockade of alpha2-adrenoceptors induces reinstatement of cocaine-seeking behavior in squirrel monkeys. Neuropsychopharmacology 29:686–693. doi:10.1038/sj.npp.1300391

    Article  PubMed  CAS  Google Scholar 

  77. Shepard JD, Bossert JM, Liu SY et al (2004) The anxiogenic drug yohimbine reinstates methamphetamine seeking in a rat model of drug relapse. Biol Psychiatry 55:1082–1089. doi:10.1016/j.biopsych.2004.02.032

    Article  PubMed  CAS  Google Scholar 

  78. Ribeiro Do Couto B, Aguilar MA, Manzanedo C et al (2006) Social stress is as effective as physical stress in reinstating morphine-induced place preference in mice. Psychopharmacology (Berl) 185:459–470. doi:10.1007/s00213-006-0345-z

    Article  CAS  Google Scholar 

  79. Shaham Y, Erb S, Stewart J (2000) Stress-induced relapse to heroin and cocaine seeking in rats: a review. Brain Res Brain Res Rev 33:13–33. doi:10.1016/S0165-0173(00)00024-2

    Article  PubMed  CAS  Google Scholar 

  80. Wang X, Cen X, Lu L (2001) Noradrenaline in the bed nucleus of the stria terminalis is critical for stress-induced reactivation of morphine-conditioned place preference in rats. Eur J Pharmacol 432:153–161. doi:10.1016/S0014-2999(01)01487-X

    Article  PubMed  CAS  Google Scholar 

  81. Highfield D, Yap J, Grimm JW et al (2001) Repeated lofexidine treatment attenuates stress-induced, but not drug cues-induced reinstatement of a heroin-cocaine mixture (speedball) seeking in rats. Neuropsychopharmacology 25:320–331. doi:10.1016/S0893-133X(01)00227-5

    Article  PubMed  CAS  Google Scholar 

  82. Egli RE, Kash TL, Choo K et al (2005) Norepinephrine modulates glutamatergic transmission in the bed nucleus of the stria terminalis. Neuropsychopharmacology 30:657–668

    PubMed  CAS  Google Scholar 

  83. Delfs JM, Zhu Y, Druhan JP et al (2000) Noradrenaline in the ventral forebrain is critical for opiate withdrawal-induced aversion. Nature 403:430–434. doi:10.1038/35000212

    Article  PubMed  CAS  Google Scholar 

  84. Kash TL, Nobis WP, Matthews RT et al (2008) Dopamine enhances fast excitatory synaptic transmission in the extended amygdala by a CRF-R1-dependent process. J Neurosci 28:13856–13865. doi:10.1523/JNEUROSCI.4715-08.2008

    Article  PubMed  CAS  Google Scholar 

  85. Wang B, Shaham Y, Zitzman D et al (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. doi:10.1523/JNEUROSCI.0955-05.2005

    Article  PubMed  CAS  Google Scholar 

  86. Raber J, Bloom FE (1996) Arginine vasopressin release by acetylcholine or norepinephrine: region-specific and cytokine-specific regulation. Neuroscience 71:747–759. doi:10.1016/0306-4522(95)00517-X

    Article  PubMed  CAS  Google Scholar 

  87. Lu L, Shepard JD, Hall FS et al (2003) Effect of environmental stressors on opiate and psychostimulant reinforcement, reinstatement and discrimination in rats: a review. Neurosci Biobehav Rev 27:457–491. doi:10.1016/S0149-7634(03)00073-3

    Article  PubMed  CAS  Google Scholar 

  88. Friedman JM, Halaas JL (1998) Leptin and the regulation of body weight in mammals. Nature 395:763–770. doi:10.1038/27376

    Article  PubMed  CAS  Google Scholar 

  89. Shalev U, Finnie PS, Quinn T et al (2006) A role for corticotropin-releasing factor, but not corticosterone, in acute food-deprivation-induced reinstatement of heroin seeking in rats. Psychopharmacology (Berl) 187:376–384. doi:10.1007/s00213-006-0427-y

    Article  CAS  Google Scholar 

  90. Shalev U, Robarts P, Shaham Y et al (2003) Selective induction of c-Fos immunoreactivity in the prelimbic cortex during reinstatement of heroin seeking induced by acute food deprivation in rats. Behav Brain Res 145:79–88. doi:10.1016/S0166-4328(03)00103-7

    Article  PubMed  CAS  Google Scholar 

  91. Sideroff SI, Jarvik ME (1980) Conditioned responses to a videotape showing heroin-related stimuli. Int J Addict 15:529–536

    PubMed  CAS  Google Scholar 

  92. Cardinal RN, Parkinson JA, Hall J et al (2002) Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26:321–352. doi:10.1016/S0149-7634(02)00007-6

    Article  PubMed  Google Scholar 

  93. LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184. doi:10.1146/annurev.neuro.23.1.155

    Article  PubMed  CAS  Google Scholar 

  94. Ciccocioppo R, Sanna PP, Weiss F (2001) 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 98:1976–1981. doi:10.1073/pnas.98.4.1976

    Article  PubMed  CAS  Google Scholar 

  95. Kruzich PJ, See RE (2001) Differential contributions of the basolateral and central amygdala in the acquisition and expression of conditioned relapse to cocaine-seeking behavior. J Neurosci 21:RC155

    PubMed  CAS  Google Scholar 

  96. Kantak KM, Black Y, Valencia E et al (2002) Dissociable effects of lidocaine inactivation of the rostral and caudal basolateral amygdala on the maintenance and reinstatement of cocaine-seeking behavior in rats. J Neurosci 22:1126–1136

    PubMed  CAS  Google Scholar 

  97. McLaughlin J, See RE (2003) Selective inactivation of the dorsomedial prefrontal cortex and the basolateral amygdala attenuates conditioned-cued reinstatement of extinguished cocaine-seeking behavior in rats. Psychopharmacology (Berl) 168:57–65. doi:10.1007/s00213-002-1196-x

    Article  CAS  Google Scholar 

  98. Koya E, Spijker S, Voorn P et al (2006) Enhanced cortical and accumbal molecular reactivity associated with conditioned heroin, but not sucrose-seeking behaviour. J Neurochem 98:905–915. doi:10.1111/j.1471-4159.2006.03917.x

    Article  PubMed  CAS  Google Scholar 

  99. Volkow ND, Fowler JS, Wang GJ et al (2002) Role of dopamine, the frontal cortex and memory circuits in drug addiction: insight from imaging studies. Neurobiol Learn Mem 78:610–624. doi:10.1006/nlme.2002.4099

    Article  PubMed  CAS  Google Scholar 

  100. Christie MJ, Summers RJ, Stephenson JA et al (1987) Excitatory amino acid projections to the nucleus accumbens septi in the rat: a retrograde transport study utilizing D[3H]aspartate and [3H]GABA. Neuroscience 22:425–439. doi:10.1016/0306-4522(87)90345-9

    Article  PubMed  CAS  Google Scholar 

  101. Kalivas PW, Volkow N, Seamans J (2005) Unmanageable motivation in addiction: a pathology in prefrontal-accumbens glutamate transmission. Neuron 45:647–650. doi:10.1016/j.neuron.2005.02.005

    Article  PubMed  CAS  Google Scholar 

  102. Bossert JM, Busch RF, Gray SM (2005) The novel mGluR2/3 agonist LY379268 attenuates cue-induced reinstatement of heroin seeking. NeuroReport 16:1013–1016. doi:10.1097/00001756-200506210-00026

    Article  PubMed  CAS  Google Scholar 

  103. Alvarez-Jaimes L, Polis I, Parsons LH (2008) Attenuation of cue-induced heroin-seeking behavior by cannabinoid CB1 antagonist infusions into the nucleus accumbens core and prefrontal cortex, but not basolateral amygdala. Neuropsychopharmacology 33(10):2483–2493

    Google Scholar 

  104. Zhou W, Kalivas PW (2008) N-acetylcysteine reduces extinction responding and induces enduring reductions in cue- and heroin-induced drug-seeking. Biol Psychiatry 63:338–340. doi:10.1016/j.biopsych.2007.06.008

    Article  PubMed  CAS  Google Scholar 

  105. Bossert JM, Poles GC, Wihbey KA et al (2007) 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 27:12655–12663. doi:10.1523/JNEUROSCI.3926-07.2007

    Article  PubMed  CAS  Google Scholar 

  106. Bouton ME (2002) Context, ambiguity, and unlearning: sources of relapse after behavioral extinction. Biol Psychiatry 52:976–986. doi:10.1016/S0006-3223(02)01546-9

    Article  PubMed  Google Scholar 

  107. Bossert JM, Poles GC, Sheffler-Collins SI et al (2006) 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 173:148–152. doi:10.1016/j.bbr.2006.06.008

    Article  PubMed  CAS  Google Scholar 

  108. Bossert JM, Liu SY, Lu L et al (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

    Article  PubMed  CAS  Google Scholar 

  109. Bossert JM, Gray SM, Lu L et al (2006) Activation of group II metabotropic glutamate receptors in the nucleus accumbens shell attenuates context-induced relapse to heroin seeking. Neuropsychopharmacology 31:2197–2209

    PubMed  CAS  Google Scholar 

  110. Crombag HS, Bossert JM, Koya E et al (2008) Context-induced relapse to drug seeking: a review. Philos Trans R Soc Lond B Biol Sci 363:3233–3243. doi:10.1098/rstb.2008.0090

    Article  PubMed  Google Scholar 

  111. Gawin F, Kleber H (1986) Pharmacologic treatments of cocaine abuse. Psychiatr Clin North Am 9:573–583

    PubMed  CAS  Google Scholar 

  112. Shalev U, Morales M, Hope B et al (2001) Time-dependent changes in extinction behavior and stress-induced reinstatement of drug seeking following withdrawal from heroin in rats. Psychopharmacology (Berl) 156:98–107. doi:10.1007/s002130100748

    Article  CAS  Google Scholar 

  113. Grimm JW, Hope BT, Wise RA et al (2001) Neuroadaptation. Incubation of cocaine craving after withdrawal. Nature 412:141–142. doi:10.1038/35084134

    Article  PubMed  CAS  Google Scholar 

  114. Lu L, Grimm JW, Hope BT et al (2004) Incubation of cocaine craving after withdrawal: a review of preclinical data. Neuropharmacology 47(Suppl 1):214–226. doi:10.1016/j.neuropharm.2004.06.027

    Article  PubMed  CAS  Google Scholar 

  115. Lu L, Hope BT, Dempsey J et al (2005) Central amygdala ERK signaling pathway is critical to incubation of cocaine craving. Nat Neurosci 8:212–219. doi:10.1038/nn1383

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We are grateful for ongoing support from the NHMRC Australia, of which AJL is a Senior Fellow.

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Authors and Affiliations

  1. Howard Florey Institute, University of Melbourne, Parkville, VIC, 3010, Australia

    Robyn M. Brown & Andrew J. Lawrence

  2. Monash Institute of Pharmaceutical Sciences, Parkville, VIC, 3052, Australia

    Robyn M. Brown

  3. Centre for Neuroscience, University of Melbourne, Parkville, VIC, 3010, Australia

    Andrew J. Lawrence

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  1. Robyn M. Brown
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  2. Andrew J. Lawrence
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Correspondence to Andrew J. Lawrence.

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Brown, R.M., Lawrence, A.J. Neurochemistry Underlying Relapse to Opiate Seeking Behaviour. Neurochem Res 34, 1876–1887 (2009). https://doi.org/10.1007/s11064-009-9967-y

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  • DOI: https://doi.org/10.1007/s11064-009-9967-y

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