Reward sensitization: Effects of repeated nicotine exposure and withdrawal in mice

Neuropsychopharmacology

Volumn 37, Issue 12, 2012, Pages 2661-2670

  Hilario, Monica R F ^a   Turner, Jill R ^a   Blendy, Julie A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

addiction; ICSS; model; mouse; nicotine; withdrawal

Indexed keywords

NICOTINE; NICOTINIC RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN DEPTH STIMULATION; CONDITIONING; CONTROLLED STUDY; CORPUS STRIATUM; HIPPOCAMPUS; MALE; MOUSE; NEUROPATHOLOGY; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; RECEPTOR UPREGULATION; RELAPSE; REWARD; SELF STIMULATION; TOBACCO DEPENDENCE; WITHDRAWAL SYNDROME;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN; CONDITIONING, OPERANT; ELECTRIC STIMULATION; MECAMYLAMINE; MICE; MICROELECTRODES; MICROINJECTIONS; NICOTINE; NICOTINIC AGONISTS; NICOTINIC ANTAGONISTS; RECEPTORS, NICOTINIC; REWARD; SUBSTANCE WITHDRAWAL SYNDROME; TOBACCO USE DISORDER; UP-REGULATION;

EID: 84867575338     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2012.130     Document Type: Article

References (53)

1. Aggarwal M, Wickens JR (2011). A role for phasic dopamine neuron firing in habit learning. Neuron 72: 892-894.
2. Carlezon Jr WA, Chartoff EH (2007). Intracranial self-stimulation (ICSS) in rodents to study the neurobiology of motivation. Nat Protoc 2: 2987-2995.
3. Changeux JP (2010). Nicotine addiction and nicotinic receptors: lessons from genetically modified mice. Nat Rev Neurosci 11: 389-401.
4. Cohen A, Koob GF, George O (2012). Robust escalation of nicotine intake with extended access to nicotine self-administration and intermittent periods of abstinence. Neuropsychopharmacology; e-pub ahead of print 2 May 2012; doi:10.1038/ npp.2012.67.
5. Collins AC, Luo Y, Selvaag S, Marks MJ (1994). Sensitivity to nicotine and brain nicotinic receptors are altered by chronic nicotine and mecamylamine infusion. J Pharmacol Exp Ther 271: 125-133.
6. Cosgrove KP, Batis J, Bois F, Maciejewski PK, Esterlis I, Kloczynski T et al (2009). beta2-Nicotinic acetylcholine receptor availability during acute and prolonged abstinence from tobacco smoking. Arch Gen Psychiatry 66: 666-676.
7. Cryan JF, Bruijnzeel AW, Skjei KL, Markou A (2003a). Bupropion enhances brain reward function and reverses the affective and somatic aspects of nicotine withdrawal in the rat. Psychopharmacology (Berl) 168: 347-358.
8. Cryan JF, Hoyer D, Markou A (2003b). Withdrawal from chronic amphetamine induces depressive-like behavioral effects in rodents. Biol Psychiatry 54: 49-58.
9. Dani JA, Heinemann S (1996). Molecular and cellular aspects of nicotine abuse. Neuron 16: 905-908.
10. De Biasi M, Dani JA (2011). Reward, addiction, withdrawal to nicotine. Annu Rev Neurosci 34: 105-130.
11. Epping-Jordan MP, Watkins SS, Koob GF, Markou A (1998). Dramatic decreases in brain reward function during nicotine withdrawal. Nature 393: 76-79.
12. Fu SS, Partin MR, Snyder A, An LC, Nelson DB, Clothier B et al (2006). Promoting repeat tobacco dependence treatment: are relapsed smokers interested? Am J Manag Care 12: 235-243.
13. Gaimarri A, Moretti M, Riganti L, Zanardi A, Clementi F, Gotti C (2007). Regulation of neuronal nicotinic receptor traffic and expression. Brain Res Rev 55: 134-143.
14. Grabus SD, Martin BR, Brown SE, Damaj MI (2006). Nicotine place preference in the mouse: influences of prior handling, dose and strain and attenuation by nicotinic receptor antagonists. Psychopharmacology (Berl) 184: 456-463.
15. Grieder TE, George O, Tan H, George SR, Le Foll B, Laviolette SR et al (2012). Phasic D1 and tonic D2 dopamine receptor signaling double dissociate the motivational effects of acute nicotine and chronic nicotine withdrawal. Proc Natl Acad Sci USA 109: 3101-3106.
16. Harris AC, Pentel PR, Burroughs D, Staley MD, Lesage MG (2011). A lack of association between severity of nicotine withdrawal and individual differences in compensatory nicotine self-administration in rats. Psychopharmacology (Berl) 217: 153-166.
17. Harrison AA, Gasparini F, Markou A (2002). Nicotine potentiation of brain stimulation reward reversed by DH beta E and SCH 23390, but not by eticlopride, LY 314582 or MPEP in rats. Psychopharmacology (Berl) 160: 56-66.
18. Ho N, Balu DT, Hilario MR, Blendy JA, Lucki I (2012). Depressive phenotypes evoked by experimental diabetes are reversed by insulin. Physiol Behav 105: 702-708.
19. Hulihan-Giblin BA, Lumpkin MD, Kellar KJ (1990). Effects of chronic administration of nicotine on prolactin release in the rat: inactivation of prolactin response by repeated injections of nicotine. J Pharmacol Exp Ther 252: 21-25.
20. Hutcheson DM, Everitt BJ, Robbins TW, Dickinson A (2001). The role of withdrawal in heroin addiction: enhances reward or promotes avoidance? Nat Neurosci 4: 943-947.
21. Johnson PM, Hollander JA, Kenny PJ (2008). Decreased brain reward function during nicotine withdrawal in C57BL6 mice: evidence from intracranial self-stimulation (ICSS) studies. Pharmacol Biochem Behav 90: 409-415.
22. Kenny PJ, Chen SA, Kitamura O, Markou A, Koob GF (2006a). Conditioned withdrawal drives heroin consumption and decreases reward sensitivity. J Neurosci 26: 5894-5900.
23. Kenny PJ, Gasparini F, Markou A (2003a). Group II metabotropic and alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate (AMPA)/kainate glutamate receptors regulate the deficit in brain reward function associated with nicotine withdrawal in rats. J Pharmacol Exp Ther 306: 1068-1076.
24. Kenny PJ, Markou A (2006b). Nicotine self-administration acutely activates brain reward systems and induces a long-lasting increase in reward sensitivity. Neuropsychopharmacology 31: 1203-1211.
25. Kenny PJ, Paterson NE, Boutrel B, Semenova S, Harrison AA, Gasparini F et al (2003b). Metabotropic glutamate 5 receptor antagonist MPEP decreased nicotine and cocaine self-administration but not nicotine and cocaine-induced facilitation of brain reward function in rats. Ann NY Acad Sci 1003: 415-418.
26. Koob GF (1996). Drug addiction: the yin and yang of hedonic homeostasis. Neuron 16: 893-896.
27. Koob GF, Volkow ND (2010). Neurocircuitry of addiction. Neuropsychopharmacology 35: 217-238.
28. Krall EA, Garvey AJ, Garcia RI (2002). Smoking relapse after 2 years of abstinence: findings from the VA Normative Aging Study. Nicotine Tob Res 4: 95-100.
29. Lerman C, LeSage MG, Perkins KA, O'Malley SS, Siegel SJ, Benowitz NL et al (2007). Translational research in medication development for nicotine dependence. Nat Rev Drug Discov 6: 746-762.
30. Markou A, Koob GF (1992). Construct validity of a self-stimulation threshold paradigm: effects of reward and performance manipulations. Physiol Behav 51: 111-119.
31. Matta SG, Balfour DJ, Benowitz NL, Boyd RT, Buccafusco JJ, Caggiula AR et al (2007). Guidelines on nicotine dose selection for in vivo research. Psychopharmacology (Berl) 190: 269-319.
32. Ockene JK, Emmons KM, Mermelstein RJ, Perkins KA, Bonollo DS, Voorhees CC et al (2000). Relapse and maintenance issues for smoking cessation. Health Psychol 19(1 Suppl): 17-31.
33. Owesson-White CA, Cheer JF, Beyene M, Carelli RM, Wightman RM (2008). Dynamic changes in accumbens dopamine correlate with learning during intracranial self-stimulation. Proc Natl Acad Sci USA 105: 11957-11962.
34. Packard MG, McGaugh JL (1996). Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol Learn Mem 65: 65-72.
35. Papke RL, Sanberg PR, Shytle RD (2001). Analysis of mecamylamine stereoisomers on human nicotinic receptor subtypes. J Pharmacol Exp Ther 297: 646-656.
36. Paterson NE, Balfour DJ, Markou A (2007). Chronic bupropion attenuated the anhedonic component of nicotine withdrawal in rats via inhibition of dopamine reuptake in the nucleus accumbens shell. Eur J Neurosci 25: 3099-3108.
37. Paterson NE, Myers C, Markou A (2000). Effects of repeated withdrawal from continuous amphetamine administration on brain reward function in rats. Psychopharmacology (Berl) 152: 440-446.
38. Paxinos GF, Franklin K (2003). The Mouse Brain in Stereotaxic Coordinates, 3rd edn. Elsevier Academic Press: San Diego, CA.
39. Petersen DR, Norris KJ, Thompson JA (1984). A comparative study of the disposition of nicotine and its metabolites in three inbred strains of mice. Drug Metab Dispos 12: 725-731.
40. Pidoplichko VI, DeBiasi M, Williams JT, Dani JA (1997). Nicotine activates and desensitizes midbrain dopamine neurons. Nature 390: 401-404.
41. Pietila K, Lahde T, Attila M, Ahtee L, Nordberg A (1998). Regulation of nicotinic receptors in the brain of mice withdrawn from chronic oral nicotine treatment. Naunyn Schmiedebergs Arch Pharmacol 357: 176-182.
42. Prus AJ, James JR, Rosecrans JA (2009). Conditioned place preference. In: Buccafusco JJ (ed). Methods of Behavior Analysis in Neuroscience, 2nd edn. CRC Press: Boca Raton (FL). Ch. 4.
43. Quick MW, Lester RA (2002). Desensitization of neuronal nicotinic receptors. J Neurobiol 53: 457-478.
44. Risinger FO, Oakes RA (1995). Nicotine-induced conditioned place preference and conditioned place aversion in mice. Pharmacol Biochem Behav 51: 457-461.
45. Scott D, Hiroi N (2010). Emergence of dormant conditioned incentive approach by conditioned withdrawal in nicotine addiction. Biol Psychiatry 68: 726-732.
46. Skjei KL, Markou A (2003). Effects of repeated withdrawal episodes, nicotine dose, and duration of nicotine exposure on the severity and duration of nicotine withdrawal in rats. Psychopharmacology (Berl) 168: 280-292.
47. Stoker AK, Olivier B, Markou A (2012). Role of alpha7-and beta4-containing nicotinic acetylcholine receptors in the affective and somatic aspects of nicotine withdrawal: studies in knockout mice. Behav Genet 42: 423-436.
48. Stoker AK, Semenova S, Markou A (2008). Affective and somatic aspects of spontaneous and precipitated nicotine withdrawal in C57BL/6J and BALB/cByJ mice. Neuropharmacology 54: 1223-1232.
49. Stolerman IP (2010). Encyclopedia of Psychopharmacology, Vol 2, 1st edn. Springer: New York.
50. Turner JR, Castellano LM, Blendy JA (2011). Parallel anxiolytic-like effects and upregulation of neuronal nicotinic acetylcholine receptors following chronic nicotine and varenicline. Nicotine Tob Res 13: 41-46.
51. Vlachou S, Paterson NE, Guery S, Kaupmann K, Froestl W, Banerjee D et al (2011). Both GABA(B) receptor activation and blockade exacerbated anhedonic aspects of nicotine withdrawal in rats. Eur J Pharmacol 655: 52-58.
52. Yamada H, Bishnoi M, Keijzers KF, van Tuijl IA, Small E, Shah HP et al (2010). Preadolescent tobacco smoke exposure leads to acute nicotine dependence but does not affect the rewarding effects of nicotine or nicotine withdrawal in adulthood in rats. Pharmacol Biochem Behav 95: 401-409.
53. Zhang L, Dong Y, Doyon WM, Dani JA (2012). Withdrawal from chronic nicotine exposure alters dopamine signaling dynamics in the nucleus accumbens. Biol Psychiatry 71: 184-191.