Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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Conditioned Place Preference and Self-Administration Induced by Nicotine in Adolescent and Adult Rats

  • Ahsan, Hafiz Muhammad (Uimyung Research Institute for Neuroscience, Department of Pharmacy, Sahmyook University) ;
  • de la Pena, June Bryan I. (Uimyung Research Institute for Neuroscience, Department of Pharmacy, Sahmyook University) ;
  • Botanas, Chrislean Jun (Uimyung Research Institute for Neuroscience, Department of Pharmacy, Sahmyook University) ;
  • Kim, Hee Jin (Uimyung Research Institute for Neuroscience, Department of Pharmacy, Sahmyook University) ;
  • Yu, Gu Yong (Department of Chemistry, Sahmyook University) ;
  • Cheong, Jae Hoon (Uimyung Research Institute for Neuroscience, Department of Pharmacy, Sahmyook University)
  • Received : 2014.05.14
  • Accepted : 2014.06.24
  • Published : 2014.09.30
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Abstract

Nicotine addiction is a worldwide problem. However, previous studies characterizing the rewarding and reinforcing effects of nicotine in animal models have reported inconsistent findings. It was observed that the addictive effects are variable on different factors (e.g. route, dose, and age). Here, we evaluated the rewarding and reinforcing effects of nicotine in different routes of administration, across a wide dose range, and in different age groups. Two of the most widely used animal models of drug addiction were employed: the conditioned place preference (CPP) and self-administration (SA) tests. Nicotine CPP was evaluated in different routes [intraperitoneal (i.p.) and subcutaneous (s.c.)], doses (0.05 to 1.0 mg/kg) and age [adolescent and adult rats]. Similarly, intravenous nicotine SA was assessed in different doses (0.01 to 0.06 mg/kg/infusion) and age (adolescent and adult rats). In the CPP test, s.c. nicotine produced greater response than i.p. The 0.2 mg/kg dose produced highest CPP response in adolescent, while 0.6 mg/kg in adult rats; which were also confirmed in 7 days pretreated rats. In the SA test, adolescent rats readily self-administer 0.03 mg/kg/infusion of nicotine. Doses that produced nicotine CPP and SA induced blood nicotine levels that corresponded well with human smokers. In conclusion, we have demonstrated that nicotine produces reliable CPP [0.2 mg/kg dose (s.c.)] in adolescents and [0.6 mg/kg dose (s.c.)] in adults, and SA [0.03 mg/kg/infusion] in adolescent rats. Both tests indicate that adolescent rats are more sensitive to the rewarding and reinforcing effects of nicotine.

Keywords

References

  1. Bardo, M., Rowlett, J. and Harris, M. (1995) Conditioned place preference using opiate and stimulant drugs: a meta-analysis. Neurosci. Biobehav. Rev. 19, 39-51. https://doi.org/10.1016/0149-7634(94)00021-R
  2. Benowitz, N. L. (2010) Nicotine addiction. N. Engl. J. Med. 362, 2295-2303. https://doi.org/10.1056/NEJMra0809890
  3. Benowitz, N. L., Hukkanen, J. and Jacob, P. 3rd. (2009) Nicotine chemistry, metabolism, kinetics and biomarkers. Handb. Exp. Pharmacol. 29-60.
  4. Biala, G. and Weglinska, B. (2004) Calcium channel antagonists attenuate cross-sensitization to the rewarding and/or locomotor effects of nicotine, morphine and MK-801. J. Pharm. Pharmacol. 56, 1021-1028. https://doi.org/10.1211/0022357043888
  5. Brielmaier, J., McDonald, C. G. and Smith, R. F. (2012) Effects of acute stress on acquisition of nicotine conditioned place preference in adolescent rats: a role for corticotropin-releasing factor 1 receptors. Psychopharmacology (Berl) 219, 73-82. https://doi.org/10.1007/s00213-011-2378-1
  6. Brunzell, D. H., Mineur, Y. S., Neve, R. L. and Picciotto, M. R. (2009) Nucleus accumbens CREB activity is necessary for nicotine conditioned place preference. Neuropsychopharmacology 34, 1993-2001. https://doi.org/10.1038/npp.2009.11
  7. Carboni, E., Acquas, E., Leone, P. and Di Chiara, G. (1989). 5HT3 receptor antagonists block morphine-and nicotine-but not amphetamine-induced reward. Psychopharmacology (Berl) 97, 175-178. https://doi.org/10.1007/BF00442245
  8. Clarke, P. B. and Fibiger, H. C. (1987) Apparent absence of nicotineinduced conditioned place preference in rats. Psychopharmacology (Berl) 92, 84-88. https://doi.org/10.1007/BF00215484
  9. Dani, J. A. and De Biasi, M. (2001) Cellular mechanisms of nicotine addiction. Pharmacol. Biochem. Behav. 70, 439-446. https://doi.org/10.1016/S0091-3057(01)00652-9
  10. de la Pena, J. B. I., Lee, H. C., de la Pena, I. C., Woo, T. S., Yoon, S. Y., Lee, H. L., Han, J. S., Lee, J. I., Cho, Y. J. Shin, C. Y. and Cheong, J. H. (2012) Rewarding and reinforcing effects of the NMDA receptor antagonist-benzodiazepine combination, zoletil(R): Difference between acute and repeated exposure. Behav. Brain Res. 233, 434-442. https://doi.org/10.1016/j.bbr.2012.05.038
  11. de la Pena, J. B., dela Pena, I. J., Lee, H. L., dela Pena, I, Shin, C.Y., Sohn, A. R. and Cheong, J. H. (2013a) Pre-exposure to ethanol, but not to caffeine and nicotine, induced place preference and selfadministration of the NMDA receptor antagonist-benzodiazepine combination, Zoletil(R). Pharmacol. Biochem. Behav. 110, 231-237. https://doi.org/10.1016/j.pbb.2013.07.016
  12. de la Pena, J. B., Yoon, S. Y., de la Pena, I. C., Lee, H. L., I de la Pena, I. J. and Cheong, J. H. (2013b) Pre-exposure to related substances induced place preference and self-administration of the NMDA receptor antagonist-benzodiazepine combination, zoletil. Behav. Pharmacol. 24, 20-28. https://doi.org/10.1097/FBP.0b013e32835cf442
  13. Donny, E. C., Caggiula, A. R., Knopf, S. and Brown, C. (1995) Nicotine self-administration in rats. Psychopharmacology (Berl) 122, 390-394. https://doi.org/10.1007/BF02246272
  14. Fudala, P. J. and Iwamoto, E. T. (1986) Further studies on nicotineinduced conditioned place preference in the rat. Pharmacol. Biochem. Behav. 25, 1041-1049. https://doi.org/10.1016/0091-3057(86)90083-3
  15. Gilpin, E. A., Choi, W. S., Berry, C. and Pierce, J. P. (1999) How many adolescents start smoking each day in the United States? J. Adolesc. Health 25, 248-255. https://doi.org/10.1016/S1054-139X(99)00024-5
  16. 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. https://doi.org/10.1146/annurev.neuro.29.051605.113009
  17. Jain, A. (2003) Extracts from "BestTreatments": Treating nicotine addiction. BMJ 327, 1394. https://doi.org/10.1136/bmj.327.7428.1394
  18. Jorenby, D. E., Steinpreis, R. E., Sherman, J. E. and Baker, T. B. (1990) Aversion instead of preference learning indicated by nicotine place conditioning in rats. Psychopharmacology (Berl) 101, 533-538. https://doi.org/10.1007/BF02244233
  19. Kota, D., Martin, B. R., Robinson, S. E. and Damaj, M. I. (2007) Nicotine dependence and reward differ between adolescent and adult male mice. J. Pharmacol. Exp. Ther. 322, 399-407. https://doi.org/10.1124/jpet.107.121616
  20. Lantz, P. M. (2003) Smoking on the rise among young adults: implications for research and policy. Tob. Control 12, i60-i70. https://doi.org/10.1136/tc.12.suppl_1.i60
  21. Le Foll, B. and Goldberg, S. R. (2005) Nicotine induces conditioned place preferences over a large range of doses in rats. Psychopharmacology (Berl) 178, 481-492. https://doi.org/10.1007/s00213-004-2021-5
  22. Le Houezec, J. (2003) Role of nicotine pharmacokinetics in nicotine addiction and nicotine replacement therapy: a review. Int. J. Tuberc. Lung Dis. 7, 811-819.
  23. Levin, E. D., Rezvani, A. H., Montoya, D., Rose, J. E. and Swartzwelder, H. S. (2003) Adolescent-onset nicotine self-administration modeled in female rats. Psychopharmacology (Berl) 169, 141-149. https://doi.org/10.1007/s00213-003-1486-y
  24. Lunell, E., Molander, L., Ekberg, K. and Wahren, J. (2000) Site of nicotine absorption from a vapour inhaler-comparison with cigarette smoking. Eur. J. Clin. Pharmacol. 55, 737-741. https://doi.org/10.1007/s002280050007
  25. Matta, S. G., Balfour, D. J., Benowitz, N. L., Boyd, R. T., Buccafusco, J. J., Caggiula, A. R., Craig, C. R., Collins, A. C., Damaj, M. I., Donny, E. C., Gardiner, P. S., Grady, S. R., Heberlein, U., Leonard, S. S., Levin, E. D., Lukas, R. J., Markou, A., Marks, M. J., McCallum, S. E., Parameswaran, N., Perkins, K. A., Picciotto, M. R., Quik, M., Rose, J. E., Rothenfluh, A., Schafer, W. R., Stolerman, I. P., Tyndale, R. F., Wehner, J. M. and Zirger, J. M. (2007) Guidelines on nicotine dose selection for in vivo research. Psychopharmacology (Berl) 190, 269-319. https://doi.org/10.1007/s00213-006-0441-0
  26. Meyer, J. S. and Quenzer, L. F. (2005) Psychopharmacology: Drugs, the brain, and behavior. Sinauer Associates, Inc. Publishers., Sunderland, Massachusetts USA.
  27. Natarajan, R., Wright, J. W. and Harding, J. W. (2011) Nicotine-induced conditioned place preference in adolescent rats. Pharmacol. Biochem. Behav. 99, 519-523. https://doi.org/10.1016/j.pbb.2011.05.004
  28. O'Dell, L. E. and Khroyan, T. V. (2009) Rodent models of nicotine reward: what do they tell us about tobacco abuse in humans? Pharmacol. Biochem. Behav. 91, 481-488. https://doi.org/10.1016/j.pbb.2008.12.011
  29. Papp, M., Gruca, P. and Willner, P. (2002) Selective blockade of druginduced place preference conditioning by ACPC, a functional NDMA-receptor antagonist. Neuropsychopharmacology 27, 727-743. https://doi.org/10.1016/S0893-133X(02)00349-4
  30. Prokhorov, A. V., Pallonen, U. E., Fava, J. L., Ding, L. and Niaura, R. (1996) Measuring nicotine dependence among high-risk adolescent smokers. Addict. Behav. 21, 117-127. https://doi.org/10.1016/0306-4603(96)00048-2
  31. Rogge, W. F., Hildemann, L. M., Mazurek, M. A., Cass, G. R. and Simoneit, B. R. (1994) Sources of fine organic aerosol. 6. Cigaret smoke in the urban atmosphere. Environ. Sci. Technol. 28, 1375-1388. https://doi.org/10.1021/es00056a030
  32. Rose, J. E., Behm, F. M., Westman, E. C. and Coleman, R. E. (1999) Arterial nicotine kinetics during cigarette smoking and intravenous nicotine administration: implications for addiction. Drug Alcohol Depend. 56, 99-107. https://doi.org/10.1016/S0376-8716(99)00025-3
  33. Schoffelmeer, A. N., De Vries, T. J., Wardeh, G., van de Ven, H. W. and Vanderschuren, L. J. (2002) Psychostimulant-induced behavioral sensitization depends on nicotinic receptor activation. J. Neurosci. 22, 3269-3276.
  34. Seeman, J. I., Fournier, J. A., Paine, J. B., 3rd and Waymack, B. E. (1999) The form of nicotine in tobacco. Thermal transfer of nicotine and nicotine acid salts to nicotine in the gas phase. J. Agric. Food Chem. 47, 5133-5145. https://doi.org/10.1021/jf990409b
  35. Shoaib, M., Schindler, C. W. and Goldberg, S. R. (1997) Nicotine selfadministration in rats: strain and nicotine pre-exposure effects on acquisition. Psychopharmacology (Berl) 129, 35-43. https://doi.org/10.1007/s002130050159
  36. Shoaib, M., Stolerman, I. P. and Kumar, R. C. (1994) Nicotine-induced place preferences following prior nicotine exposure in rats. Psychopharmacology (Berl) 113, 445-452. https://doi.org/10.1007/BF02245221
  37. Shram, M. J., Funk, D., Li, Z. and Le, A. D. (2006) Periadolescent and adult rats respond differently in tests measuring the rewarding and aversive effects of nicotine. Psychopharmacology (Berl) 186, 201-208. https://doi.org/10.1007/s00213-006-0373-8
  38. Shram, M. J., Funk, D., Li, Z. and Le, A. D. (2008) Nicotine self-administration, extinction responding and reinstatement in adolescent and adult male rats: evidence against a biological vulnerability to nicotine addiction during adolescence. Neuropsychopharmacology 33, 739-748. https://doi.org/10.1038/sj.npp.1301454
  39. Shram, M. J. and Le, A. D. (2010) Adolescent male Wistar rats are more responsive than adult rats to the conditioned rewarding effects of intravenously administered nicotine in the place conditioning procedure. Behav. Brain Res. 206, 240-244. https://doi.org/10.1016/j.bbr.2009.09.018
  40. Small, E., Shah, H. P., Davenport, J. J., Geier, J. E., Yavarovich, K. R., Yamada, H., Sabarinath, S. N., Derendorf, H., Pauly, J. R., Gold, M. S. and Bruijnzeel, A. W. (2010) Tobacco smoke exposure induces nicotine dependence in rats. Psychopharmacology (Berl) 208, 143-158. https://doi.org/10.1007/s00213-009-1716-z
  41. Stanton, W. R., McClelland, M., Elwood, C., Ferry, D. and Silva, P. A. (1996) Prevalence, reliability and bias of adolescents' reports of smoking and quitting. Addiction 91, 1705-1714. https://doi.org/10.1111/j.1360-0443.1996.tb02273.x
  42. Thiel, K. J., Sanabria, F. and Neisewander, J. L. (2009) Synergistic interaction between nicotine and social rewards in adolescent male rats. Psychopharmacology (Berl) 204, 391-402. https://doi.org/10.1007/s00213-009-1470-2
  43. Torres, O. V., Tejeda, H. A., Natividad, L. A. and O'Dell, L. E. (2008) Enhanced vulnerability to the rewarding effects of nicotine during the adolescent period of development. Pharmacol. Biochem. Behav. 90, 658-663. https://doi.org/10.1016/j.pbb.2008.05.009
  44. Tzschentke, T. M. (1998) Measuring reward with the conditioned place preference paradigm: a comprehensive review of drug effects, recent progress and new issues. Prog. Neurobiol. 56, 613-672. https://doi.org/10.1016/S0301-0082(98)00060-4
  45. van der Kooy, D. (1987) Place conditioning: a simple and effective method for assessing the motivational properties of drugs. In Methods of assessing the reinforcing properties of abused drugs (Michael A. Bozarth, Ed), pp. 229-240. Springer, New York.
  46. Vastola, B. J., Douglas, L. A., Varlinskaya, E. I. and Spear, L. P. (2002) Nicotine-induced conditioned place preference in adolescent and adult rats. Physiol. Behav. 77, 107-114. https://doi.org/10.1016/S0031-9384(02)00818-1
  47. Walters, C. L., Brown, S., Changeux, J. P., Martin, B. and Damaj, M. I. (2006) The ${\beta}$2 but not ${\alpha}$7 subunit of the nicotinic acetylcholine receptor is required for nicotine-conditioned place preference in mice. Psychopharmacology (Berl) 184, 339-344. https://doi.org/10.1007/s00213-005-0295-x
  48. World Health Organization. (2013) Report on the global tobacco epidemic. WHO Press, World Health Organization., Geneva, Switzerland.
  49. Yararbas, G., Keser, A., Kanit, L. and Pogun, S. (2010) Nicotine-induced conditioned place preference in rats: sex differences and the role of mGluR5 receptors. Neuropharmacology 58, 374-382. https://doi.org/10.1016/j.neuropharm.2009.10.001

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