Behavioral effects of nicotine withdrawal differ by genetic strain in male and female adolescent rats

Nicotine and Tobacco Research

Volumn 12, Issue 12, 2010, Pages 1236-1245

  Hamilton, Kristen R ^a   Perry, Michael E ^a   Berger, Sarah Shafer ^a   Grunberg, Neil E ^a  

^a Uniformed Services University of the Health Sciences and the Walter Reed National Military Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINE; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR CHANGE; BODY POSTURE; CONTROLLED STUDY; DIARRHEA; FEMALE; GENETIC STRAIN; GROOMING; MALE; MOVEMENT (PHYSIOLOGY); NONHUMAN; OSMOTIC MINIPUMP; PRIORITY JOURNAL; PTOSIS; RAT; SMOKELESS TOBACCO; SMOKING CESSATION;

ADOLESCENT; ADOLESCENT BEHAVIOR; AGE FACTORS; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG ADMINISTRATION SCHEDULE; FEMALE; HUMANS; MALE; MODELS, ANIMAL; MOTOR ACTIVITY; NICOTINE; NICOTINIC AGONISTS; RATS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY; RATS, WISTAR; SEX FACTORS; SPECIES SPECIFICITY; SUBSTANCE WITHDRAWAL SYNDROME;

EID: 78649568227     PISSN: 14622203     EISSN: 1469994X     Source Type: Journal    
DOI: 10.1093/ntr/ntq179     Document Type: Article

References (65)

1. Abreu-Villaça, Y., Seidler, F. J., Qiao, D., Tate, C. A., Cousins, M. M., Thillai, I., et al. (2003). Short-term adolescent nicotine exposure has immediate and persistent effects on cholinergic systems: Critical periods, patterns of exposure, dose thresholds. Neuropsychopharmacology, 28, 1935-1949.
2. American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders, fourth edition, text revision (4th ed.). Washington, DC: Author.
3. Audrain-McGovern, J., Lerman, C., Wileyto, E., Rodriguez, D., & Shields, P. (2004). Interacting effects of genetic predisposition and depression on adolescent smoking. American Journal of Psychiatry, 161, 1224-1230.
4. Backinger, C. L., Fagan, P., Matthews, E., & Grana, R. (2003). Adolescent and young adult tobacco prevention and cessation: Current status and future directions. Tobacco Control, 12(Suppl. 4), 46-53.
5. Bailey, S. R., Harrison, C. T., Jeffery, C. J., Ammerman, S., Bryson, S. W., Killen, D. T., et al. (2009). Withdrawal symptoms over time among adolescents in a smoking cessation intervention: Do symptoms vary by level of nicotine dependence? Addictive Behavior, 3, 1017-1022.
6. Blitstein, J. L., Robinson, L. A., Murray, D. M., Klesges, R. C., & Zbikowski, S. M. (2003). Rapid progression to regular cigarette smoking among nonsmoking adolescents: Interactions with gender and ethnicity. Preventive Medicine, 36, 455-463.
7. Carboni, E., Bortone, L., Guia, C., & Chiara, G. (2000). Dissociation of physical abstinence signs from changes in extracellular dopamine in the nucleus accumbens and in the prefrontal cortex of nicotine dependent rats. Drug and Alcohol Dependence, 58, 93-102.
8. Centers for Disease Control and Prevention. (2008). Cigarette smoking among adults and trends in smoking cessation-United States. Morbidity and Mortality Weekly Report, 2009, 1227-1232.
9. Chapillon, P., Patin, V., Roy, V., Vincent, A., & Caston, J. (2002). Effects of pre and postnatal stimulation on developmental, emotional, and cognitive aspects in rodents: A review. Developmental Psychobiology, 41, 373-387.
10. Colby, S. M., Tiffany, S. T., Shiffman, S., & Niaura, R. S. (2000). Measuring nicotine dependence among youth: A review of available approaches and instruments. Drug and Alcohol Dependence, 59(Suppl. 1), S23-S39.
11. Cryan, J. F., Bruijnzeel, A. W., Skjei, K. L., & Markou, A. (2003). Bupropion enhances brain reward function and reverses the affective and somatic aspects of nicotine withdrawal in the rat. Psychopharmacology, 168, 347-358.
12. Derby, K. S., Cuthrell, K., Caberto, C., Carmella, S. G., Franke, A. A., Hecht, S. S., et al. (2008). Nicotine metabolism in three ethnic/racial groups with different risks of lung cancer. Cancer Epidemiology, Biomarkers & Prevention, 17, 3526-3535.
13. Dickman, P. J., Mooney, M. E., Allen, S. S., Hanson, K., & Hatsukami, D. K. (2009). Nicotine withdrawal and craving in adolescents: Effects of sex and hormonal contraceptive use. Addictive Behaviors, 34, 620-623.
14. DiFranza, J.R. (2007). Hooked from the first cigarette. The Journal of Family Practice, 56, 1017-1022.
15. DiFranza, J. R., Rigotti, N. A., McNeill, A. D., Ockene, J. K., Savageau, J. A., Cyr, D. S., et al. (2000). Initial symptoms of nicotine dependence in adolescents. Tobacco Control, 9, 313-319.
16. DiFranza, J. R., Savageau, J. A., Fletcher, K., O'Loughlin, J., Pbert, L., Ockene, J.K., et al. (2007). Symptoms of tobacco dependence after brief intermittent use. Archives of Pediatrics & Adolescent Medicine, 61, 707-710.
17. Epping-Jordan, M. P., Watkins, S. S., Koob, G. F., & Markou, A. (1998). Dramatic decreases in brain reward function during nicotine withdrawal. Nature, 393, 76-9.
18. Fagerström, K., & Schneider, N. B. (1989). Measuring nicotine dependence: A review of the Fagerstrom tolerance questionnaire. Journal of Behavioral Medicine, 12, 159-182.
19. Faraday, M. M. (2002). Rat sex and strain differences in response to stress. Physiology and Behavior, 754, 507-522.
20. Faraday, M. M., Blakeman, K. H., & Grunberg, N. E. (2005). Strain and sex alter effects of stress and nicotine on feeding, body weight, and HPA axis hormones. Pharmacology, Biochemistry, and Behavior, 80, 577-589.
21. Faraday, M. M., & Grunberg, N. E. (2000). The importance of acclimation in acoustic startle amplitude and pre-pulse inhibition testing of male and female rats. Pharmacology, Biochemistry, and Behavior, 66, 375-381.
22. Grunberg, N. E. (1982). The effects of nicotine and cigarette smoking on food consumption and taste preferences. Addictive Behavior, 7, 317-331.
23. Hamilton, K. R., Berger, S. S., Perry, M. E., & Grunberg, N. E. (2009). Behavioral effects of nicotine withdrawal in adult male and female rats. Pharmacology, Biochemistry, and Behavior, 92, 51-59.
24. Hildebrand, B. E., Nomikos, G. G., Bondjers, C., Nisell, M., & Svensson, T. H. (1997). Behavioral manifestations of the nicotine abstinence syndrome in the rat: peripheral versus central mechanisms. Psychopharmacology, 129, 348-356.
25. Hildebrand, B. E., Nomikos, G. G., Hertel, P., Schilstrom, B., & Svensson, T. H. (1998). Reduced dopamine output in the nucleus accumbens but not in the medial prefrontal cortex in rats displaying mecamylamine-precipitated nicotine withdrawal syndrome. Brain Research, 779, 214-225.
26. Horn, K., Fernandes, A., Dino, G., Massey, C. J., & Kalsekar, I. (2003). Adolescent nicotine dependence and smoking cessation outcomes. Addictive Behaviors, 28, 769-776.
27. Hughes, J. R. (2007). Effects of abstinence from tobacco: Valid symptoms and time course. Nicotine and Tobacco Research, 9, 315-327.
28. Hurt, R. D., Croghan, G. A., Beede, S. D., Wolter, T. D., Croghan, I. T., & Patten, C. A. (2000). Nicotine patch therapy in 101 adolescent smokers. Archives of Pediatric and Adolescent Medicine, 154, 31-37.
29. Kandel, D. B., Kiros, G. E., Schaffran, C., & Hu, M. C. (2004). Racial/ethnic differences in cigarette smoking initiation and progression to daily smoking: A multilevel analysis. American Journal of Public Health, 94, 128-135.
30. Kota, D., Martin, B. R., & Damaj, M. I. (2008). Age-dependent differences in nicotine reward and withdrawal in female mice. Psychopharmacology, 198, 201-210.
31. Kota, D., Martin, B. R., Robinson, S. E., & Damaj, M. I. (2007). Nicotine dependence and reward differ between adolescent and adult male mice. The Journal of Pharmacology and Experimental Therapeutics, 322, 399-407.
32. Kyerematen, G. A., Owens, G. F., Chattopadhyay, B., deBithizy, J. D., & Vesell, E. S. (1988). Sexual dimorphism of nicotine metabolism and distribution in the rat. Studies in vivo and in vitro. Drug Metabolism and Disposition, 16, 823-828.
33. Lawlor, M. M. (2002). Comfortable quarters for rats in research institutions. In A. Reihardt & V. Reinhardt (Eds.), Comfortable quarters for laboratory animals (9th ed.). Washington, DC: Animal Welfare Institute, 26-32.
34. Leventhal, A. M., Waters, A. J., Boyd, S., Moolchan, E. T., Lerman, C., & Pickworth, W. B. (2007). Gender differences in acute tobacco withdrawal: effects on subjective, cognitive, and physiological measures. Experimental and Clinical Psychopharmacology, 15, 21-36.
35. Levine, S. (2005). Developmental determinants of sensitivity and resistance to stress. Psychoneuroendocrinology, 30, 939-946.
36. Malaiyandi, V., Sellers, E. M., & Tyndale, R. F. (2005). Implications of CYP2A6 genetic variation for smoking behaviors and nicotine dependence. Clinical Pharmacology and Therapeutics, 77, 145-158.
37. Malin, D. H. (2001). Nicotine dependence: Studies with a laboratory model. Pharmacology, Biochemistry, and Behavior, 70, 551-9.
38. Malin, D. H., Lake, J. R., Carter, V. A., Cunningham, J. S., Hebert, K. M., Payne, M. C., et al. (1994). The nicotinic antagonist mecamylamine precipitates nicotine abstinence syndrome in the rat. Psychopharmacology, 115, 180-184.
39. Malin, D. H., Lake, J. R., Carter, V. A., Cunningham, J. S., Wilson, O. B., & Payne, M. C. (1993). Naloxone precipitates nicotine abstinence syndrome in the rat. Psychopharmacology, 112, 339-342.
40. Malin, D. H., Lake, J. R., Newlin-Maultsby, P., Roberts, L. K., Lanier, J. G., Carter, V. A., et al. (1992). Rodent model of nicotine abstinence syndrome. Pharmacology, Biochemistry, and Behavior, 43, 779-784.
41. Malin, D. H., Lake, J. R., Upchurch, T. P., Shenoi, M., Rajan, N., & Schweinle, W. E. (1998). Nicotine abstinence syndrome precipitated by the competitive nicotinic antagonist dihydrobetaerythroidine. Pharmacology, Biochemistry, and Behavior, 60, 609-613.
42. Mermelstein, R. (1999). Explanations of ethnic and gender differences in youth smoking: A multi-site, qualitative investigation. Nicotine & Tobacco, 1, S91-S98.
43. Moolchan, E. T., Franken, F. H., & Jaszyna-Gasior, M. (2006). Adolescent nicotine metabolism: Ethnoracial differences among dependent smokers. Ethnicity & Disease, 16, 239-243.
44. Moolchan, E. T., Robinson, M. L., Ernst, M., Cadet, J. L., Pickworth, W. B., Heishman, S. J., et al. (2005). Safety and efficacy of the nicotine patch and gum for the treatment of adolescent tobacco addiction. Pediatrics, 115, e407-e414.
45. Mowery, P. D., Brick, P. D., & Farrelly, M. C. (2000). Legacy first look report 3. Pathways to established smoking: Results from the 1999 National Youth Tobacco Survey. Washington, DC: American Legacy Foundation.
46. National Institute on Drug Abuse. (2006). Tobacco addiction, (Research Report Series. NIH Publication Number 06-4342). Baltimore, MD: Author.
47. National Institutes of Health Guide for Care and Use of Laboratory Animals. (1996). National Institutes of Health. Bethesda, MD: National Academy Press.
48. O'Dell, L. E., Bruijnzeel, A. W., Ghozland, S., Markou, A., & Koob, G. F. (2004). Nicotine withdrawal in adolescent and adult rats. Annals of the New York Academy of Sciences, 1021, 167-174.
49. O'Loughlin, J., Kishchuk, N., DiFranza, J., Tremblay, M., & Paradis, G. (2002). The hardest thing is the habit: A qualitative investigation of adolescent smokers' experience of nicotine dependence. Nicotine & Tobacco Research, 4, 201-209.
50. Panday, S., Reddy, P., Ruiter, R. A. C., Bergström, E., & de Vries, H. (2007). Nicotine dependence and withdrawal symptoms among occasional smokers. Journal of Adolescent Health, 40, 144-150.
51. Pérez-Stable, E. J., Herrera, B., Jacob, P., & Benowitz, N. L. (1998). Nicotine metabolism and intake in Black and White smokers. Journal of the American Medical Association, 280, 152-156.
52. Phillips, J. M., Schechter, L. E., & Grunberg, N. E. (2004). Nicotine abstinence syndrome in rats depends on form of nicotine. Scottsdale, AZ: Society for Research on Nicotine and Tobacco.
53. Pomerleau, O. F., Collins, A. C., Shiffman, S., & Pomerleau, C. S. (1993). Why some people smoke and others do not: New perspectives. Journal of Consulting and Clinical Psychology, 61, 723-731.
54. Russell, W. (2002). The ill-effects of uncomfortable quarters. In A. Reihardt & V. Reinhardt (Eds.), Comfortable quarters for laboratory animals (9th ed.). (pp. 1-5) Washington, DC: Animal Welfare Institute.
55. 3H] acetylcholine recognition sites in brain by nicotinic cholinergic drugs. Journal of Neurochemistry, 45, 427-433.
56. Semenova, S., Stolerman, I. P., & Markou, A. (2007). Chronic nicotine administration improves attention while nicotine withdrawal induces performance deficits in the 5-choice serial reaction time task in rats. Pharmacology, Biochemistry, and Behavior, 87, 360-368.
57. Shoaib, M., Schindler, C. W., & Goldberg, S. R. (1997). Nicotine self-administration in rats: Strain and nicotine pre-exposure effects on acquisition. Psychopharmacology, 129, 35-43.
58. Smith, A. E., Cavallo, D. A., Dahl, T., Wu, R., George, T. P., & Krishnan-Sarin, S. (2008). Effects of acute tobacco abstinence in adolescent smokers compared with nonsmokers. Journal of Adolescent Health, 43, 46-54.
59. Spear, L. P. (2000). The adolescent brain and age-related behavioral manifestations. Neuroscience and Biobehavioral Reviews, 24, 417-463.
60. Substance Abuse and Mental Health Services Administration. (2008). Results from the 2007 National Survey on Drug Use and Health. (NSDUH Series H-34, DHHS Publication No. SMA 08-4343). Rockville, MD: Office of Applied Studies.
61. Trauth, J. A., Seidler, F. J., & Slotkin, T. A. (2000). An animal model of adolescent nicotine exposure: Effects on gene expression and macromolecular constituents in rat brain regions. Brain Research, 867, 29-39.
62. Tuli, J. S., Smith, J. A., & Morton, D. B. (1995). Stress measurements in mice after transportation. Lab Animal, 29, 132-138.
63. United States Department of Heath and Human Services (1988). The health consequences of smoking: Nicotine addiction. In N. L. Benowitz, N. E. Grunberg, J. E. Henningfield, H. A. Lando (Eds). A Report of the Surgeon General. Rockville, MD: U.S. Government Printing Office.
64. Watkins, S., Stinus, L., Koob, G., & Markou, A. (2000). Reward and somatic changes during precipitated nicotine withdrawal in rats: Centrally and peripherally mediated effects. Journal of Pharmacology and Experimental Therapeutics, 292, 1053-1064.
65. Wilmouth, C. E., & Spear, L. P. (2006). Withdrawal from chronic nicotine in adolescent and adult rats. Pharmacology, Biochemistry, and Behavior, 85, 648-657.