Incubation of Methamphetamine but not Heroin Craving after Voluntary Abstinence in Male and Female Rats

Neuropsychopharmacology

Volumn 42, Issue 5, 2017, Pages 1126-1135

  Venniro, Marco ^a   Zhang, Michelle ^a   Shaham, Yavin ^a   Caprioli, Daniele ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIAMORPHINE; METHAMPHETAMINE;

ABSTINENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; DRUG CRAVING; DRUG SELF ADMINISTRATION; FEMALE; FOOD; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RELAPSE; SEX DIFFERENCE; ANIMAL; CRAVING; DECISION MAKING; DRUG EFFECTS; DRUG SEEKING BEHAVIOR; FEEDING BEHAVIOR; RECURRENT DISEASE; SEXUAL CHARACTERISTICS; SPRAGUE DAWLEY RAT;

ANIMALS; CHOICE BEHAVIOR; CRAVING; DRUG-SEEKING BEHAVIOR; FEEDING BEHAVIOR; FEMALE; HEROIN; MALE; METHAMPHETAMINE; RATS, SPRAGUE-DAWLEY; RECURRENCE; SELF ADMINISTRATION; SEX CHARACTERISTICS;

EID: 85010886851     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2016.287     Document Type: Article

References (88)

1. Abdolahi A, Acosta G, Breslin FJ, Hemby SE, Lynch WJ (2010). Incubation of nicotine seeking is associated with enhanced protein kinase A-regulated signaling of dopamine-and cAMP-regulated phosphoprotein of 32 kDa in the insular cortex. Eur J Neurosci 31: 733-741.
2. Ahmed SH, Koob GF (1998). Transition from moderate to excessive drug intake: change in hedonic set point. Science 282: 298-300.
3. Anker JJ, Carroll ME (2011). Females are more vulnerable to drug abuse than males: evidence from preclinical studies and the role of ovarian hormones. Curr Top Behav Neurosci 8: 73-96.
4. Badiani A, Belin D, Epstein D, Calu D, Shaham Y (2011). Opiate versus psychostimulant addiction: the differences do matter. Nat Rev Neurosci 12: 685-700.
5. Baldo BA (2016). Prefrontal cortical opioids and dysregulated motivation: a network hypothesis. Trends Neurosci 39: 366-377.
6. Becker JB, Prendergast BJ, Liang JW (2016). Female rats are not more variable than male rats: a meta-analysis of neuroscience studies. Biol Sex Differ 7: 34.
7. Bienkowski P, Rogowski A, Korkosz A, Mierzejewski P, Radwanska K, Kaczmarek L et al (2004). Time-dependent changes in alcohol-seeking behaviour during abstinence. Eur Neuropsychopharmacol 14: 355-360.
8. Calu DJ, Chen YW, Kawa AB, Nair SG, Shaham Y (2014). The use of the reinstatement model to study relapse to palatable food seeking during dieting. Neuropharmacology 76 Pt B: 395-406.
9. Cantin L, Lenoir M, Augier E, Vanhille N, Dubreucq S, Serre F et al (2010). Cocaine is low on the value ladder of rats: possible evidence for resilience to addiction. PLoS ONE 5: e11592.
10. Caprioli D, Venniro M, Zeric T, Li X, Adhikary S, Madangopal R et al (2015a). Effect of the novel positive allosteric modulator of metabotropic glutamate receptor 2 AZD8529 on incubation of methamphetamine craving after prolonged voluntary abstinence in a rat model. Biol Psychiatry 78: 463-473.
11. Caprioli D, Venniro M, Zhang M, Bossert JM, Warren BL, Hope BT et al (2016). Role of dorsomedial striatum neuronal ensembles in incubation of methamphetamine craving after voluntary abstinence. J Neurosci (in press).
12. Caprioli D, Zeric T, Thorndike EB, Venniro M (2015b). Persistent palatable food preference in rats with a history of limited and extended access to methamphetamine self-administration. Addict Biol 20: 913-926.
13. Carroll ME, Campbell UC, Heideman P (2001). Ketoconazole suppresses food restriction-induced increases in heroin self-administration in rats: sex differences. Exp Clin Psychopharmacol 9: 307-316.
14. Carroll ME, Lynch WJ (2016). How to study sex differences in addiction using animal models. Addict Biol.
15. Carroll ME, Lynch WJ, Roth ME, Morgan AD, Cosgrove KP (2004). Sex and estrogen influence drug abuse. Trends Pharmacol Sci 25: 273-279.
16. Chauvet C, Goldberg SR, Jaber M, Solinas M (2012). Effects of environmental enrichment on the incubation of cocaine craving. Neuropharmacology 63: 635-641.
17. Cicero TJ, Aylward SC, Meyer ER (2003). Gender differences in the intravenous self-administration of mu opiate agonists. Pharmacol Biochem Behav 74: 541-549.
18. Cifani C, Koya E, Navarre BM, Calu DJ, Baumann MH, Marchant NJ et al (2012). Medial prefrontal cortex neuronal activation and synaptic alterations after stress-induced reinstatement of palatable food seeking: a study using c-fos-GFP transgenic female rats. J Neurosci 32: 8480-8490.
19. Cox BM, Young AB, See RE, Reichel CM (2013). Sex differences in methamphetamine seeking in rats: impact of oxytocin. Psycho-neuroendocrinology 38: 2343-2353.
20. Deroche-Gamonet V, Belin D, Piazza PV (2004). Evidence for addiction-like behavior in the rat. Science 305: 1014-1017.
21. Dole VP (1988). Implications of methadone maintenance for theories of narcotic addiction. J Am Med Assoc 260: 3025-3029.
22. Dole VP, Nyswander M (1965). A medical treatment for diacetylmorphine (heroin) addiction. a clinical trial with metha-done hydrochloride. JAMA 193: 646-650.
23. Donny EC, Caggiula AR, Rowell PP, Gharib MA, Maldovan V, Booth S et al (2000). Nicotine self-administration in rats: estrous cycle effects, sex differences and nicotinic receptor binding. Psychopharmacology (Berl) 151: 392-405.
24. Epstein DH, Preston KL (2003). The reinstatement model and relapse prevention: a clinical perspective. Psychopharmacology 168: 31-41.
25. Epstein DH, Preston KL, Stewart J, Shaham Y (2006). Toward a model of drug relapse: an assessment of the validity of the reinstatement procedure. Psychopharmacology (Berl) 189: 1-16.
26. Epstein DH, Schmittner J, Umbricht A, Schroeder JR, Moolchan ET, Preston KL (2009). Promoting abstinence from cocaine and heroin with a methadone dose increase and a novel contingency. Drug Alcohol Depend 101: 92-100.
27. Ettenberg A (2009). The runway model of drug self-administration. Pharmacol Biochem Behav 91: 271-277.
28. Ettenberg A, Pettit HO, Bloom FE, Koob GF (1982). Heroin and cocaine intravenous self-administration in rats: mediation by separate neural systems. Psychopharmacology (Berl) 78: 204-209.
29. Fanous S, Goldart EM, Theberge FR, Bossert JM, Shaham Y, Hope BT (2012). Role of orbitofrontal cortex neuronal ensembles in the expression of incubation of heroin craving. J Neurosci 32: 11600-11609.
30. Fuchs RA, Branham RK, See RE (2006). Different neural substrates mediate cocaine seeking after abstinence versus extinction training: a critical role for the dorsolateral caudate-putamen. J Neurosci 26: 3584-3588.
31. Funk D, Coen K, Tamadon S, Hope BT, Shaham Y, Lê AD (2016). Role of central amygdala neuronal ensembles in incubation of nicotine craving. J Neurosci 36: 8612-8623.
32. Gawin FH, Kleber HD (1986). Abstinence symptomatology and psychiatric diagnosis in cocaine abusers. Clinical observations. Arch Gen Psychiatry 43: 107-113.
33. Gosnell BA, Levine AS (2009). Reward systems and food intake: role of opioids. Int J Obes (Lond) 33: S54-S58.
34. Grimm JW, Hope BT, Wise RA, Shaham Y (2001). Incubation of cocaine craving after withdrawal. Nature 412: 141-142.
35. Heilig M, Epstein DH, Nader MA, Shaham Y (2016). Time to connect: bringing social context into addiction neuroscience. Nat Rev Neurosci 17: 592-599.
36. Higgins ST, Heil SH, Lussier JP (2004). Clinical implications of reinforcement as a determinant of substance use disorders. Annual Rev Psychol 55: 431-461.
37. Holtz NA, Lozama A, Prisinzano TE, Carroll ME (2012). Reinstatement of methamphetamine seeking in male and female rats treated with modafinil and allopregnanolone. Drug Alcohol Dependence 120: 233-237.
38. Hunt WA, Barnett LW, Branch LG (1971). Relapse rates in addiction programs. J Clin Psychol 27: 455-456.
39. Joel D, McCarthy MM (2016). Incorporating sex as a biological variable in neuropsychiatric research: where are we now and where should we be? Neuropsychopharmacology 42: 379-385.
40. Katz JL, Higgins ST (2003). The validity of the reinstatement model of craving and relapse to drug use. Psychopharmacology (Berl) 168: 21-30.
41. Kelley AE, Berridge KC (2002). The neuroscience of natural rewards: relevance to addictive drugs. J Neurosci 22: 3306-3311.
42. Kerstetter KA, Aguilar VR, Parrish AB, Kippin TE (2008). Protracted time-dependent increases in cocaine-seeking behavior during cocaine withdrawal in female relative to male rats. Psychopharmacology (Berl) 198: 63-75.
43. Kerstetter KA, Ballis MA, Duffin-Lutgen S, Carr AE, Behrens AM, Kippin TE (2012). Sex differences in selecting between food and cocaine reinforcement are mediated by estrogen. Neuropsycho-pharmacology 37: 2605-2614.
44. Klump KL, Racine S, Hildebrandt B, Sisk CL (2013). Sex differences in binge eating patterns in male and female adult rats. Int J Eat Disord 46: 729-736.
45. Knackstedt LA, Moussawi K, Lalumiere R, Schwendt M, Klugmann M, Kalivas PW (2010). Extinction training after cocaine self-administration induces glutamatergic plasticity to inhibit cocaine seeking. J Neurosci 30: 7984-7992.
46. Krasnova IN, Marchant NJ, Ladenheim B, McCoy MT, Panlilio LV, Bossert JM et al (2014). Incubation of methamphetamine and palatable food craving after punishment-induced abstinence. Neuropsychopharmacology 39: 2008-2016.
47. Lenoir M, Cantin L, Vanhille N, Serre F, Ahmed SH (2013). Extended heroin access increases heroin choices over a potent nondrug alternative. Neuropsychopharmacology 38: 1209-1220.
48. Lenoir M, Serre F, Cantin L, Ahmed SH (2007). Intense sweetness surpasses cocaine reward. PLoS ONE 2: e698.
49. Levine AS, Morley JE, Gosnell BA, Billington CJ, Bartness TJ (1985). Opioids and consummatory behavior. Brain Res Bull 14: 663-672.
50. Li X, Zeric T, Kambhampati S, Bossert JM, Shaham Y (2015). The central amygdala nucleus is critical for incubation of methamphetamine craving. Neuropsychopharmacology 40: 1297-1306.
51. Lu L, Grimm JW, Hope BT, Shaham Y (2004). Incubation of cocaine craving after withdrawal: a review of preclinical data. Neuropharmacology 47: 214-226.
52. Lussier JP, Heil SH, Mongeon JA, Badger GJ, Higgins ST (2006). A meta-analysis of voucher-based reinforcement therapy for substance use disorders. Addiction 101: 192-203.
53. Lynch WJ, Carroll ME (1999). Sex differences in the acquisition of intravenously self-administered cocaine and heroin in rats. Psychopharmacology (Berl) 144: 77-82.
54. Lynch WJ, Roth ME, Carroll ME (2002). Biological basis of sex differences in drug abuse: preclinical and clinical studies. Psychopharmacology (Berl) 164: 121-137.
55. Madsen HB, Ahmed SH (2015). Drug versus sweet reward: greater attraction to and preference for sweet versus drug cues. Addict Biol 20: 433-444.
56. Marchant NJ, Li X, Shaham Y (2013). Recent developments in animal models of drug relapse. Curr Opin Neurobiol 23: 675-683.
57. Marlatt AG (1996). Models of relapse and relapse prevention: a commentary. Exp Clin Psychopharmacol 4: 55-60.
58. Mead AN, Zamanillo D, Becker N, Stephens DN (2007). AMPA-receptor GluR1 subunits are involved in the control over behavior by cocaine-paired cues. Neuropsychopharmacology 32: 343-353.
59. Mello NK, Negus SS (1996). Preclinical evaluation of pharma-cotherapies for treatment of cocaine and opioid abuse using drug self-administration procedures. Neuropsychopharmacology 14: 375-424.
60. Mena JD, Selleck RA, Baldo BA (2013). Mu-opioid stimulation in rat prefrontal cortex engages hypothalamic orexin/hypocretin-containing neurons, and reveals dissociable roles of nucleus accumbens and hypothalamus in cortically driven feeding. J Neurosci 33: 18540-18552.
61. Neisewander JL, Baker DA, Fuchs RA, Tran-Nguyen LT, Palmer A, Marshall JF (2000). Fos protein expression and cocaine-seeking behavior in rats after exposure to a cocaine self-administration environment. J Neurosci 20: 798-805.
62. O'Brien CP, Childress AR, McLellan AT, Ehrman R (1992). Classical conditioning in drug-dependent humans. Ann N Y Acad Sci 654: 400-415.
63. Pecina S, Berridge KC (2005). Hedonic hot spot in nucleus accumbens shell: where do mu-opioids cause increased hedonic impact of sweetness? J Neurosci 25: 11777-11786.
64. Perry AN, Westenbroek C, Becker JB (2013). The development of a preference for cocaine over food identifies individual rats with addiction-like behaviors. PLoS ONE 8: e79465.
65. Pickens CL, Airavaara M, Theberge F, Fanous S, Hope BT, Shaham Y (2011). Neurobiology of the incubation of drug craving. Trends Neurosci 34: 411-420.
66. Pickens CL, Cifani C, Navarre BM, Eichenbaum H, Theberge FR, Baumann MH et al (2012). Effect of fenfluramine on reinstatement of food seeking in female and male rats: implications for the predictive validity of the reinstatement model. Psychopharmacol-ogy (Berl) 221: 341-353.
67. Prendergast BJ, Onishi KG, Zucker I (2014). Female mice liberated for inclusion in neuroscience and biomedical research. Neurosci Biobehav Rev 40: 1-5.
68. Preston KL, Umbricht A, Epstein DH (2002). Abstinence reinforcement maintenance contingency and one-year follow-up. Drug Alcohol Depend 67: 125-137.
69. Rawson RA, Marinelli-Casey P, Anglin MD, Dickow A, Frazier Y, Gallagher C et al (2004). A multi-site comparison of psychosocial approaches for the treatment of methamphetamine dependence. Addiction 99: 708-717.
70. Reichel CM, Chan CH, Ghee SM, See RE (2012). Sex differences in escalation of methamphetamine self-administration: cognitive and motivational consequences in rats. Psychopharmacology (Berl) 223: 371-380.
71. Reichelt AC, Abbott KN, Westbrook RF, Morris MJ (2016). Differential motivational profiles following adolescent sucrose access in male and female rats. Physiol Behav 157: 13-19.
72. Roll JM (2007). Contingency management: an evidence-based component of methamphetamine use disorder treatments. Addiction 102: 114-120.
73. Roll JM, Chudzynski J, Cameron JM, Howell DN, McPherson S (2013). Duration effects in contingency management treatment of methamphetamine disorders. Addict Behav 38: 2455-2462.
74. Roth ME, Carroll ME (2004). Sex differences in the acquisition of IV methamphetamine self-administration and subsequent maintenance under a progressive ratio schedule in rats. Psychopharma-cology (Berl) 172: 443-449.
75. Scheyer AF, Loweth JA, Christian DT, Uejima J, Rabei R, Le T et al (2016). AMPA receptor plasticity in accumbens core contributes to incubation of methamphetamine craving. Biol Psychiatry 80: 661-670.
76. Self DW, Choi KH, Simmons D, Walker JR, Smagula CS (2004). Extinction training regulates neuroadaptive responses to withdrawal from chronic cocaine self-administration. Learn Mem 11: 648-657.
77. Shaham Y, Shalev U, Lu L, De Wit H, Stewart J (2003). The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology (Berl) 168: 3-20.
78. Shalev U, Morales M, Hope B, Yap J, Shaham Y (2001). Time-dependent changes in extinction behavior and stress-induced reinstatement of drug seeking following withdrawal from heroin in rats. Psychopharmacology 156: 98-107.
79. Shepard JD, Bossert JM, Liu SY, Shaham Y (2004). The anxiogenic drug yohimbine reinstates methamphetamine seeking in a rat model of drug relapse. Biol Psychiatry 55: 1082-1089.
80. Silverman K, DeFulio A, Sigurdsson SO (2012). Maintenance of reinforcement to address the chronic nature of drug addiction. Prev Med 55: S46-S53.
81. Stewart J, Woodside B, Shaham Y (1996). Ovarian hormones do not affect the initiation and maintenance of intravenous self-administration of heroin in the female rat. Psychobiology 24: 115-159.
82. Stitzer M, Petry N (2006). Contingency management for treatment of substance abuse. Annu Rev Clin Psychol 2: 411-434.
83. Theberge FR, Li X, Kambhampati S, Pickens CL St, Laurent R, Bossert JM et al (2013). Effect of chronic delivery of the Toll-like receptor 4 antagonist (+)-naltrexone on incubation of heroin craving. Biol Psychiatry 73: 729-737.
84. Thiel KJ, Painter MR, Pentkowski NS, Mitroi D, Crawford CA, Neisewander JL (2012). Environmental enrichment counters cocaine abstinence-induced stress and brain reactivity to cocaine cues but fails to prevent the incubation effect. Addict Biol 17: 365-377.
85. Vandaele Y, Cantin L, Serre F, Vouillac-Mendoza C, Ahmed SH (2016). Choosing under the influence: a drug-specific mechanism by which the setting controls drug choices in rats. Neuropsycho-pharmacology 41: 646-657.
86. Venniro M, Caprioli D, Shaham Y (2016). Animal models of drug relapse and craving: from drug priming-induced reinstatement to incubation of craving after voluntary abstinence. Prog Brain Res 224: 25-52.
87. Wikler A (1973). Dynamics of drug dependence. Implications of a conditioning theory for research and treatment. Arch Gen Psychiatry 28: 611-616.
88. Wolf ME (2016). Synaptic mechanisms underlying persistent cocaine craving. Nat Rev Neurosci 17: 351-365.