Rodent models of nicotine withdrawal syndrome
Abstract
Simple, rapid and inexpensive rodent models of nicotine physical dependence and withdrawal syndrome have proved useful for preliminary screening of smoking cessation treatments. They have led to an exponential increase of knowledge regarding the underlying neurobiological mechanisms of dependence and withdrawal syndrome. The human nicotine withdrawal syndrome in smoking cessation is variable and multidimensional, involving irritability, anxiety, depression, cognitive and attentional impairments, weight gain, sleep disturbances, and craving for nicotine. Aside from sleep disturbances, analogous phenomena have been seen in rodent models using different measures of withdrawal intensity. It appears likely that different withdrawal phenomena may involve some partially divergent mechanisms. For example, depression-like phenomena may involve alterations in mechanisms such as the mesolimbic dopamine pathway from the ventral tegmental area to the nucleus accumbens. Irritability and anxiety may involve alterations in endogenous opioid systems and other regions, such as the amygdala. This chapter reviews many additional anatomical, neurochemical, and developmental elements that impact nicotine physical dependence.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Rodents chronically exposed to nicotine undergo a characteristic withdrawal syndrome that can occur spontaneously or be precipitated by mecamylamine.
“Rodents chronically exposed to nicotine undergo a characteristic withdrawal syndrome which develops spontaneously, after removing the nicotine source, or can be precipitated by administration of a nAChR antagonist such as mecamylamine [7, 11, 81, 163–166].”
From Mechanistic insights into nicotine withdrawal (2011) · cites this paper as [166]
Cites
Diagnostic and Statistical Manual of Mental Disorders (DSM-IV)
Hu, R. J. (2003) · Elsevier eBooks · doi:10.1016/b0-12-226870-9/01070-4 · Cited by 9,167 · see citing works
Shape of the relapse curve and long-term abstinence among untreated smokers
Hughes, J. R., Keely, J., & Naud, S. (2004) · Addiction · doi:10.1111/j.1360-0443.2004.00540.x · Cited by 1,414 · see citing works
Picciotto, M. R., Zoli, M., Rimondini, R., Léna, C., Marubio, L. M., Pich, E. M., Fuxe, K., & Changeux, J.-P. (1998) · Nature · doi:10.1038/34413 · Cited by 1,320 · see citing works
Effects of abstinence from tobacco: Valid symptoms and time course
Hughes, J. (2007) · Nicotine & Tobacco Research · doi:10.1080/14622200701188919 · Cited by 793 · cited 4× · see citing works
“Signs and symptoms include irritability, agitation, anxiety, sleep disturbances, difficulty concentrating, depression, weight gain, and craving for tobacco (Hughes 2007b).”
InfluentialBreslau, N., & Peterson, E. L. (1996) · American Journal of Public Health · doi:10.2105/ajph.86.2.214 · Cited by 682 · see citing works
Role of dopamine in the behavioural actions of nicotine related to addiction
Chiara, G. D. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00122-9 · Cited by 680 · see citing works
Dramatic decreases in brain reward function during nicotine withdrawal
Epping-Jordan, M. P., Watkins, S. S., Koob, G. F., & Markou, A. (1998) · Nature · doi:10.1038/30001 · Cited by 674 · see citing works
Rodent model of nicotine abstinence syndrome
Malin, D. H., Lake, J. R., Newlin-Maultsby, P., Roberts, L. K., Lanier, J. G., Carter, V. A., Cunningham, J. S., & Wilson, O. B. (1992) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(92)90408-8 · Cited by 334 · see citing works
Self-citationCircadian blood nicotine concentrations during cigarette smoking
Benowitz, N. L., Kuyt, F., & Jacob, P. (1982) · Clinical Pharmacology & Therapeutics · doi:10.1038/clpt.1982.233 · Cited by 292 · see citing works
Age-dependent effects of nicotine on locomotor activity and conditioned place preference in rats
Belluzzi, J., Lee, A., Oliff, H., & Leslie, F. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1758-6 · Cited by 280 · see citing works
Selective dopamine antagonists reduce nicotine self-administration
Corrigall, W. A., & Coen, K. M. (1991) · Psychopharmacology · doi:10.1007/bf02244174 · Cited by 276 · see citing works
Smoking withdrawal dynamics in unaided quitters.
Piasecki, T. M., Niaura, R., Shadel, W. G., Abrams, D., Goldstein, M., Fiore, M. C., & Baker, T. B. (2000) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.109.1.74 · Cited by 262 · see citing works
The effect of bupropion on nicotine craving and withdrawal
Shiffman, S. S., Johnston, J. A., Khayrallah, M. A., Elash, C. A., Gwaltney, C. J., Paty, J. A., Gnys, M., Evoniuk, G. E., & DeVeaugh-Geiss, J. (2000) · Psychopharmacology · doi:10.1007/s002130050022 · Cited by 260 · see citing works
Nicotine-induced conditioned place preference in adolescent and adult rats
Vastola, B. J., Douglas, L. A., Varlinskaya, E. I., & Spear, L. P. (2002) · Physiology & Behavior · doi:10.1016/s0031-9384(02)00818-1 · Cited by 251 · see citing works
Balfour, D. (2004) · Nicotine & Tobacco Research · doi:10.1080/14622200412331324965 · Cited by 251 · see citing works
Castañé, A., Valjent, E., Ledent, C. A., Parmentier, M., Maldonado, R. J., & Valverde, O. (2002) · Neuropharmacology · doi:10.1016/s0028-3908(02)00118-1 · Cited by 240 · see citing works
Effects of nicotine on body weight and food consumption in rats
Grunberg, N. E., Bowen, D. J., & Morse, D. E. (1984) · Psychopharmacology · doi:10.1007/bf00427430 · Cited by 227 · see citing works
Salas, R., Pieri, F., & De Biasi, M. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.1939-04.2004 · Cited by 226 · see citing works
Cryan, J. F., Bruijnzeel, A. W., Skjei, K. L., & Markou, A. (2003) · Psychopharmacology · doi:10.1007/s00213-003-1445-7 · Cited by 223 · see citing works
Berrendero, F., Kieffer, B. L., & Maldonado, R. J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-24-10935.2002 · Cited by 222 · see citing works
Characterization of spontaneous and precipitated nicotine withdrawal in the mouse
Damaj, M. I., Kao, W., & Martin, B. R. (2003) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.054908 · Cited by 222 · see citing works
Effects of systemic nicotine on serotonin release in rat brain
Ribeiro, E. B., Bettiker, R. L., Bogdanov, M. B., & Wurtman, R. J. (1993) · Brain Research · doi:10.1016/0006-8993(93)90121-3 · Cited by 217 · see citing works
Watkins, S. S., Stinus, L., Koob, G. F., & Markou, A. (2000) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)35389-3 · Cited by 214 · see citing works
Nicotine dependence and reward differ between adolescent and adult male mice
Kota, D., Martin, B. R., Robinson, S. E., & Damaj, M. I. (2007) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.107.121616 · Cited by 202 · see citing works
Hildebrand, B. E., Nomikos, G. G., Hertel, P., Schilström, B., & Svensson, T. H. (1998) · Brain Research · doi:10.1016/s0006-8993(97)01135-9 · Cited by 200 · see citing works
Regulations of opioid dependence by opioid receptor types
Narita, M., Funada, M., & Suzuki, T. (2001) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(00)00099-1 · Cited by 190 · see citing works
Pentel, P. R., Malin, D. H., Ennifar, S., Hieda, Y., Keyler, D. E., Lake, J. R., Milstein, J. R., Basham, L., Coy, R., Moon, J. W. D., et al. (2000) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(99)00206-3 · Cited by 179 · see citing works
Self-citationHughes, J. (2007) · Nicotine & Tobacco Research · doi:10.1080/14622200701188927 · Cited by 173 · see citing works
Malin, D. H. (2001) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00699-2 · Cited by 167 · see citing works
Self-citationHarrison, A. A. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(00)00237-2 · Cited by 167 · see citing works
The nicotinic antagonist mecamylamine precipitates nicotine abstinence syndrome in the rat
Malin, D. H., Ronald Lake, J., Carter, V. A., Scott Cunningham, J., Hebert, K. M., Conrad, D. L., & Wilson, O. B. (1994) · Psychopharmacology · doi:10.1007/bf02244770 · Cited by 165 · see citing works
Self-citationKenny, P. J., File, S. E., & Rattray, M. (2000) · Molecular Brain Research · doi:10.1016/s0169-328x(00)00246-1 · Cited by 165 · see citing works
Behavioral and Neurochemical Vulnerability During Adolescence in Mice: Studies with Nicotine
Adriani, W., Granstrem, O., Macrı̀, S., Izykenova, G. A., Dambinova, S. A., & Giovanni Laviola, A. (2003) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300366 · Cited by 164 · see citing works
Smoking withdrawal dynamics: II. Improved tests of withdrawal-relapse relations
Piasecki, T. M., Jorenby, D. E., Smith, S. S., Fiore, M. C., & Baker, T. B. (2003) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.112.1.14 · Cited by 159 · see citing works
Markou, A., & Paterson, N. E. (2001) · Nicotine & Tobacco Research · doi:10.1080/14622200110073380 · Cited by 155 · see citing works
Monoamine oxidase and tobacco dependence.
Lewis, A., Miller, J. H., & Lea, R. A. (2007) · Neurotoxicology · doi:10.1016/j.neuro.2006.05.019 · Cited by 153 · see citing works
Diminished nicotine withdrawal in adolescent rats: implications for vulnerability to addiction
O’Dell, L. E., Bruijnzeel, A. W., Smith, R. T., Parsons, L. H., Merves, M. L., Goldberger, B. A., Richardson, H. N., Koob, G. F., & Markou, A. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0383-6 · Cited by 153 · see citing works
Naloxone precipitates nicotine abstinence syndrome in the rat
Malin, D. H., Lake, J. R., Carter, V. A., Cunningham, J. S., & Wilson, O. B. (1993) · Psychopharmacology · doi:10.1007/bf02244930 · Cited by 147 · see citing works
Self-citationWithdrawal from Chronic Nicotine Administration Impairs Contextual Fear Conditioning in C57BL/6 Mice
Davis, J. A., James, J. R., Siegel, S. J., & Gould, T. J. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2853-05.2005 · Cited by 146 · see citing works
FMRF-NH2-like mammalian octapeptide: Possible role in opiate dependence and abstinence
Malin, D. H., Lake, J. R., Hammond, M. V., Fowler, D. E., Rogillio, R. B., Brown, S. L., Sims, J. L., Leecraft, B. M., & Yang, H. T. (1990) · Peptides · doi:10.1016/0196-9781(90)90018-z · Cited by 144 · see citing works
Self-citationRada, P., Jensen, K., & Hoebel, B. (2001) · Psychopharmacology · doi:10.1007/s002130100781 · Cited by 141 · see citing works
Berrendero, F., Mendizábal, V. E., Robledo, P., Galeote, L., Bilkei‐Gorzó, A., Zimmer, A., & Maldonado, R. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3008-04.2005 · Cited by 138 · see citing works
Kenny, P. J., Gasparini, F., & Markou, A. (2003) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.052027 · Cited by 138 · see citing works
Barik, J., & Wonnacott, S. (2005) · Molecular Pharmacology · doi:10.1124/mol.105.018184 · Cited by 132 · see citing works
O’Dell, L. E., Chen, S. A., Smith, R. T., Specio, S. E., Balster, R. L., Paterson, N. E., Markou, A., Zorrilla, E. P., & Koob, G. F. (2006) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.106.105270 · Cited by 128 · see citing works
Effects of nicotine on body weight and food consumption in female rats
Grunberg, N., Bowen, D., & Winders, S. E. (1986) · Psychopharmacology · doi:10.1007/bf00172879 · Cited by 124 · see citing works
Hildebrand, B. E., Nomikos, G. G., Bondjers, C., Nisell, M., & Svensson, T. H. (1997) · Psychopharmacology · doi:10.1007/s002130050200 · Cited by 122 · see citing works
Balerio, G. N., Aso, E., Berrendero, F., Murtra, P., & Maldonado, R. J. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03714.x · Cited by 116 · see citing works
Glutamatergic Transmission in Opiate and Alcohol Dependence
Siggins, G. R., Martin, G. E., Roberto, M., Nie, Z., Madamba, S. G., & de Lecea, L. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1300.012 · Cited by 115 · see citing works
Cohen, C., Bergis, O. E., Galli, F., Lochead, A. W., Jegham, S., Biton, B., Léonardon, J., Avenet, P., Sgard, F., Besnard, F., et al. (2003) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.103.049262 · Cited by 114 · see citing works
Cheeta, S., Irvine, E. E., Kenny, P. J., & File, S. E. (2001) · Psychopharmacology · doi:10.1007/s002130100681 · Cited by 113 · see citing works
Rahman, S., Zhang, J., Engleman, E. A., & Corrigall, W. A. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.08.010 · Cited by 110 · see citing works
Ondansetron inhibits a behavioural consequence of withdrawing from drugs of abuse
Costall, B., Jones, B. J., Kelly, M. E., Naylor, R. J., Onaivi, E. S., & Tyers, M. B. (1990) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(90)90414-d · Cited by 109 · see citing works
Effects of nicotine withdrawal on central dopaminergic systems
Fung, Y. K., Schmid, M. J., Anderson, T. M., & Lau, Y. (1996) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)02063-2 · Cited by 109 · see citing works
Conditioned nicotine withdrawal profoundly decreases the activity of brain reward systems
Kenny, P. J., & Markou, A. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4785-04.2005 · Cited by 107 · see citing works
Zarevics, P., & Setler, P. E. (1979) · Brain Research · doi:10.1016/0006-8993(79)90399-8 · Cited by 106 · see citing works
Bruijnzeel, A. W., Zislis, G., Wilson, C., & Gold, M. S. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301192 · Cited by 106 · see citing works
�sterlund, M. K., Halldin, C., & Hurd, Y. L. (2000) · Synapse · doi:10.1002/(sici)1098-2396(200001)35:1 · Cited by 106 · see citing works
Chronic nicotine and withdrawal effects on body weight and food and water consumption in female rats
Levin, E. D., Morgan, M. M., Galvez, C., & Ellison, G. D. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90370-2 · Cited by 102 · see citing works
Hildebrand, B. E. (1999) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00055-x · Cited by 102 · see citing works
Krishnan‐Sarin, S., Rosen, M. I., & O’Malley, S. S. (1999) · Archives of General Psychiatry · doi:10.1001/archpsyc.56.7.663 · Cited by 101 · see citing works
Region-specific transcriptional response to chronic nicotine in rat brain
Konu, Ö., Kane, J. K., Barrett, T., Vawter, M. P., Chang, R., Ma, J. Z., Donovan, D. M., Sharp, B. M., Becker, K. G., & Li, M. D. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02685-3 · Cited by 98 · see citing works
Pharmacokinetic Considerations in Understanding Nicotine Dependence
Benowitz, N. L. (2007) · Novartis Foundation symposium · doi:10.1002/9780470513965.ch11 · Cited by 97 · see citing works
Sites of action of ondansetron to inhibit withdrawal from drugs of abuse
Costall, B., Jones, B., Kelly, M. E., Naylor, R. J., Onaivi, E. S., & Tyers, M. B. (1990) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(90)90132-2 · Cited by 97 · see citing works
Nicotine physical dependence and tolerance in the mouse following chronic oral administration
Grabus, S. D., Martin, B. R., Batman, A. M., Tyndale, R. F., Sellers, E. M., & Damaj, M. I. (2004) · Psychopharmacology · doi:10.1007/s00213-004-2007-3 · Cited by 97 · see citing works
Paterson, N. E., & Markou, A. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1692-7 · Cited by 96 · see citing works
Nicotine abstinence in the mouse
Isola, R., Vogelsberg, V., Wemlinger, T. A., Neff, N. H., & Hadjiconstantinou, M. (1999) · Brain Research · doi:10.1016/s0006-8993(99)02131-9 · Cited by 96 · see citing works
Carboni, E., Bortone, L., Giua, C., & Di Chiara, G. (2000) · Drug and Alcohol Dependence · doi:10.1016/s0376-8716(99)00064-2 · Cited by 96 · see citing works
Gilbert, D. G., Meliska, C. J., Williams, C. L., & Jensen, R. A. (1992) · Psychopharmacology · doi:10.1007/bf02801984 · Cited by 94 · see citing works
Skjei, K. L., & Markou, A. (2003) · Psychopharmacology · doi:10.1007/s00213-003-1414-1 · Cited by 93 · see citing works
Mecamylamine-precipitated nicotine-withdrawal aversion in rats
Suzuki, T., Ise, Y., Tsuda, M., Maeda, J., & Misawa, M. (1996) · European Journal of Pharmacology · doi:10.1016/s0014-2999(96)00723-6 · Cited by 93 · see citing works
Nicotine Withdrawal in Adolescent and Adult Rats
O’Dell, L. E., Bruijnzeel, A. W., Ghozland, S. G., Markou, A., & Koob, G. F. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1308.022 · Cited by 90 · see citing works
Irvine, E. E., Cheeta, S., & File, S. E. (1999) · Behavioural Pharmacology · doi:10.1097/00008877-199911000-00016 · Cited by 89 · cited 2× · see citing works
“1990a), reduced social interaction (Cheeta et al. 2001; Costall et al. 1990a; Irvine et al. 1999), thigmotaxis, avoid-”
LeSage, M. G., Keyler, D. E., Shoeman, D. W., Raphael, D. E., Collins, G., & Pentel, P. R. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(01)00775-4 · Cited by 88 · see citing works
Deficits in a sustained attention task following nicotine withdrawal in rats
Shoaib, M., & Bizarro, L. (2005) · Psychopharmacology · doi:10.1007/s00213-004-2004-6 · Cited by 87 · see citing works
Helton, D. R., Modlin, D. L., Tizzano, J. P., & Rasmussen, K. (1993) · Psychopharmacology · doi:10.1007/bf02245698 · Cited by 81 · see citing works
Salminen, O., Seppä, T., Gäddnäs, H., & Ahtee, L. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-18-08145.1999 · Cited by 80 · see citing works
Paterson, N. E., Balfour, D. J. K., & Markou, A. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05546.x · Cited by 80 · see citing works
Neuroplasticity within the Mesoaccumbens Dopamine System and its Role in Tobacco Dependence
Balfour, D. J. K. (2002) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1568007023339076 · Cited by 79 · see citing works
Schmidt, B. L., Tambeli, C. H., Gear, R. W., & Levine, J. D. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00264-0 · Cited by 78 · see citing works
Clinical significance of tobacco withdrawal
Hughes, J. R. (2006) · Nicotine & Tobacco Research · doi:10.1080/14622200500494856 · Cited by 78 · see citing works
Pandey, S. C., Roy, A., Xu, T., & Mittal, N. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00309.x · Cited by 75 · see citing works
Besson, M., David, V., Suarez, S., Cormier, A., Cazala, P., Changeux, J.-P., & Granon, S. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0418-z · Cited by 73 · see citing works
Liechti, M. E., & Markou, A. (2006) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2006.10.011 · Cited by 71 · see citing works
The biologicalbases of drug tolerance and dependence
Cox, F. E. (1992) · Parasitology Today · doi:10.1016/0169-4758(92)90154-t · Cited by 69 · see citing works
Bupropion attenuates nicotine abstinence syndrome in the rat
Malin, D. H., Lake, J. R., Smith, T. D., Khambati, H. N., Meyers-Paal, R. L., Montellano, A. L., Jennings, R. E., Erwin, D. S., Presley, S. E., & Perales, B. A. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0135-z · Cited by 68 · see citing works
Self-citationGuilloux, J., David, D. J. P., Guiard, B. P., Chenu, F., Repérant, C., Tóth, M., Bourin, M., & Gardier, A. M. (2006) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301019 · Cited by 68 · see citing works
Altered disposition of repeated nicotine doses in rats immunized against nicotine
Keyler, D. E., Hieda, Y., Peter, J. V. S., & Pentel, P. R. (1999) · Nicotine & Tobacco Research · doi:10.1080/14622299050011361 · Cited by 67 · see citing works
Pietilä, K., Lähde, T., Attila, M., Ahtee, L., & Nordberg, A. (1998) · Naunyn-Schmiedeberg's Archives of Pharmacology · doi:10.1007/pl00005152 · Cited by 67 · see citing works
Withdrawal from chronic nicotine in adolescent and adult rats
Wilmouth, C. E., & SPEAR, L. P. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.10.021 · Cited by 65 · see citing works
O’Dell, L. E., & Koob, G. F. (2007) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2007.01.004 · Cited by 65 · see citing works
Bohus, B., Koolhaas, J. M., Luiten, P. G. M., Korte, S. M., Roozendaal, B., & Wiersma, A. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)61881-6 · Cited by 64 · see citing works
Modulation of opioidergic system on mecamylamine-precipitated nicotine-withdrawal aversion in rats
Ise, Y., Narita, M., Nagase, H., & Suzuki, T. (2000) · Psychopharmacology · doi:10.1007/s002130000482 · Cited by 63 · see citing works
Bruijnzeel, A. W., & Markou, A. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.05.005 · Cited by 60 · see citing works
Nicotine alleviation of nicotine abstinence syndrome is naloxone-reversible
Malin, D. H. (1996) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)00202-2 · Cited by 60 · see citing works
Self-citationMarttila, K., Raattamaa, H., & Ahtee, L. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.02.014 · Cited by 59 · see citing works
Rasmussen, K., Calligaro, D. O., Czachura, J. F., Dreshfield, L. J., Evans, D. C., Hemrick-Luecke, S. K., Kallman, M. J., Kendrick, W. T., Leander, J. D., Nelson, D. L. G., et al. (2000) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)39123-2 · Cited by 58 · see citing works
Passive immunization against nicotine prevents nicotine alleviation of nicotine abstinence syndrome
Malin, D. H., Lake, J. R., Lin, A., Saldaña, M., Balch, L., Irvin, M. L. L., Chandrasekara, H., Alvarado, C. L., Hieda, Y., & Keyler, D. E. (2001) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(00)00436-6 · Cited by 56 · see citing works
Self-citationMarkou, A. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.053 · Cited by 56 · see citing works
Semba, J., Wakuta, M., Maeda, J., & Suhara, T. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(03)00024-6 · Cited by 53 · see citing works
Atomoxetine Reverses Nicotine Withdrawal-Associated Deficits in Contextual Fear Conditioning
Davis, J. A., & Gould, T. J. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301315 · Cited by 52 · see citing works
Mannucci, C., Tedesco, M., Bellomo, M., Caputi, A. P., & Calapai, G. (2006) · Neurochemistry International · doi:10.1016/j.neuint.2006.03.010 · Cited by 51 · see citing works
Malin, D. H. (1998) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(98)00028-8 · Cited by 50 · see citing works
Self-citationHarris, C. M., Emmett‐Oglesby, M. W., Robinson, N., & Lal, H. (1986) · Psychopharmacology · doi:10.1007/bf00172876 · Cited by 46 · see citing works
Nicotine modulates nitric oxide in rat brain
Pöğün, Ş., Demirgören, S., Taşkıran, D., Kanıt, L., Yilmaz, O., Koylu, E. O., Balkan, B., & London, E. D. (2000) · European Neuropsychopharmacology · doi:10.1016/s0924-977x(00)00116-4 · Cited by 46 · see citing works
Biała, G., Budzyńska, B., & Kruk, M. (2005) · PubMed · Cited by 46 · see citing works
Aricioǧlu-Kartal, F., Kayır, H., & Uzbay, T. I. (2003) · Life Sciences · doi:10.1016/s0024-3205(03)00647-7 · Cited by 45 · see citing works
Fornari, A., Pedrazzi, P., Lippi, G., Picciotto, M. R., Zoli, M., & Zini, I. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.10.014 · Cited by 45 · see citing works
Nicotine withdrawal in the rat: role of α7 nicotinic receptors in the ventral tegmental area
Nomikos, G. G., Hildebrand, B. E., Panagis, G., & Svensson, T. H. (1999) · Neuroreport · doi:10.1097/00001756-199903170-00007 · Cited by 45 · see citing works
Nicotine Abstinence Syndrome Precipitated by Central But Not Peripheral Hexamethonium
Malin, D. H. (1997) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(97)90006-x · Cited by 43 · see citing works
Self-citationMet-enkephalin and preproenkephalin mRNA changes in the striatum of the nicotine abstinence mouse
Isola, R., Zhang, H., Duchemin, A., Tejwani, G. A., Neff, N. H., & Hadjiconstantinou, M. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(02)00240-9 · Cited by 41 · see citing works
Decrease of ventral tegmental area dopamine neuronal activity in nicotine withdrawal rats
Liu, Z.-H., & Jin, W.-Q. (2004) · Neuroreport · doi:10.1097/01.wnr.0000126218.25235.b6 · Cited by 41 · see citing works
Tzavara, E. T., Monory, K., Hanoune, J., & Nomikos, G. G. (2002) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2002.02061.x · Cited by 40 · see citing works
Bishop, C., Parker, G. C., & Coscina, D. V. (2002) · Psychopharmacology · doi:10.1007/s00213-002-1101-7 · Cited by 39 · see citing works
LeSage, M. G., Burroughs, D., & Pentel, P. R. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.03.021 · Cited by 39 · see citing works
Pluzarev, O., & Pandey, S. C. (2004) · Journal of Neuroscience Research · doi:10.1002/jnr.20216 · Cited by 39 · see citing works
Passive immunization against nicotine attenuates nicotine discrimination
Malin, D. H., Alvarado, C. L., Woodhouse, K. S., Karp, H. J., Urdiales, E., Lay, D., Appleby, P., Moon, W. D., Ennifar, S., Basham, L., et al. (2002) · Life Sciences · doi:10.1016/s0024-3205(02)01523-0 · Cited by 38 · see citing works
Self-citationBiała, G., & Weglińska, B. (2005) · Pharmacological Research · doi:10.1016/j.phrs.2004.11.009 · Cited by 38 · see citing works
Malin, D. H., Lake, J. R., Shenoi, M., Upchurch, T. P., Johnson, S. C., Schweinle, W. E., & Cadle, C. D. (1998) · Psychopharmacology · doi:10.1007/s002130050778 · Cited by 36 · see citing works
Self-citationNicotine causes age-dependent changes in gene expression in the adolescent female rat brain
Polesskaya, O. O., Fryxell, K. J., Merchant, A. D., Locklear, L. L., Ker, K.-F., McDonald, C. G., Eppolito, A. K., Smith, L. N., Wheeler, T. L., & Smith, R. F. (2007) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2006.11.005 · Cited by 36 · see citing works
Semenova, S., & Markou, A. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00240-3 · Cited by 34 · see citing works
Semenova, S., Bespalov, A., & Markou, A. (2003) · European Journal of Pharmacology · doi:10.1016/s0014-2999(03)01904-6 · Cited by 34 · see citing works
Glycyl-glutamine inhibits nicotine conditioned place preference and withdrawal
Göktalay, G., Çavun, S., Levendusky, M. C., Hamilton, J. R., & Millington, W. R. (2006) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.11.034 · Cited by 34 · see citing works
Vann, R. E., Balster, R. L., & Beardsley, P. M. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0037-0 · Cited by 33 · see citing works
Neurosteroids in nicotine and morphine dependence
Concas, A., Sogliano, C., Porcu, P., Marra, C., Brundu, A., & Biggio, G. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0111-7 · Cited by 33 · see citing works
Impact of nicotine withdrawal on novelty reward and related behaviors.
Besheer, J., & Bevins, R. A. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.2.327 · Cited by 33 · see citing works
Ise, Y., Narita, M., Nagase, H., & Suzuki, T. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(02)00074-5 · Cited by 32 · see citing works
Imaging localised dynamic changes in the nucleus accumbens following nicotine withdrawal in rats
Shoaib, M. C., Lowe, A., & Williams, S. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.01.026 · Cited by 32 · see citing works
Nicotine abstinence syndrome precipitated by an analog of neuropeptide FF
Malin, D. H. (1996) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)02279-1 · Cited by 32 · see citing works
Self-citationHypericum perforatum attenuates nicotine withdrawal signs in mice
Catania, M. A., Firenzuoli, F., Crupi, A., Mannucci, C., Caputi, A. P., & Calapai, G. (2003) · Psychopharmacology · doi:10.1007/s00213-003-1492-0 · Cited by 31 · see citing works
Yasuda, K., Suemaru, K., Araki, H., et al. (2002) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-002-0592-4 · Cited by 31 · see citing works
Suzuki, T., Ise, Y., Mori, T., & Misawa, M. (1997) · Life Sciences · doi:10.1016/s0024-3205(97)00745-5 · Cited by 30 · see citing works
Nitric oxide mediates mecamylamine- and naloxone-precipitated nicotine withdrawal
Adams, M. L., & Cicero, T. J. (1998) · European Journal of Pharmacology · doi:10.1016/s0014-2999(98)00089-2 · Cited by 29 · see citing works
Nicotine withdrawal leads to increased firing rates of midbrain dopamine neurons.
Rasmussen, K., & Czachura, J. F. (1995) · PubMed · Cited by 29 · see citing works
Subcutaneous injection of an analog of neuropeptide FF precipitates morphine abstinence syndrome
Malin, D. H., Lake, J. R., Arcangeli, K. R., Deshotel, K. D., Hausam, D. D., Witherspoon, W. E., Carter, V. A., Yang, H.-Y. T., Pal, B., & Burgess, K. (1993) · Life Sciences · doi:10.1016/0024-3205(93)90601-x · Cited by 27 · see citing works
Self-citationLindblom, N., de Villiers, S. H. L., Semenova, S., Kalayanov, G., Gordon, S. L., Schilström, B., Johansson, A. M., Markou, A., & Svensson, T. H. (2005) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-005-0019-0 · Cited by 26 · see citing works
Suemaru, K., Araki, H., Kitamura, Y., et al. (2001) · Psychopharmacology · doi:10.1007/s002130100866 · Cited by 26 · see citing works
Nicotine withdrawal leads to increased firing rates of midbrain dopamine neurons
Rasmussen, K., & Czachura, J. F. (1995) · Neuroreport · doi:10.1097/00001756-199512290-00079 · Cited by 22 · see citing works
Paterson, N. E., Bruijnzeel, A. W., Kenny, P. J., Wright, C., Froestl, W., & Markou, A. (2005) · Neuropharmacology · doi:10.1016/j.neuropharm.2005.04.031 · Cited by 21 · see citing works
Salmon, A., Evrard, A., Damaj, M. I., & Changeux, J. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.02.031 · Cited by 20 · see citing works
Ethological analysis of scopolamine treatment or pretreatment in morphine dependent rats
Xiang, X., Wang, H., Wu, W.-R., et al. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.03.029 · Cited by 18 · see citing works
Nicotine reversal effects of the benzoflavone moiety from Passiflora incarnata Linneaus in mice
Dhawan, K., Kumar, S., & Sharma, A. (2002) · Addiction Biology · doi:10.1080/1355621021000006044 · Cited by 18 · see citing works
Changes in sympathetic nerve activity during morphine abstinence in the rat
Delle, M., & Thorén, P. (1987) · Acta Physiologica Scandinavica · doi:10.1111/j.1748-1716.1987.tb08110.x · Cited by 17 · see citing works
Suh, H., Hudson, P. M., McMillian, M., Das, K. P., Wilson, B. C., Wu, G.-Q., & Hong, J. (1995) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)12231-3 · Cited by 17 · see citing works
Andersson, K., Fuxé, K., Eneroth, P. H. E., Jansson, A., & H�rfstrand, A. (1989) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/bf00736052 · Cited by 16 · see citing works
Jonkman, S., & Markou, A. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2006.02.030 · Cited by 13 · see citing works
SPECIFIC DETECTION OF κ LIGHT CHAIN IN URIC ACID STONES
Hashimoto, Y., Kohri, K., Hayashi, Y., Moriyama, A., Iguchi, M., Asai, K., & Kato, T. (1997) · Life Sciences · doi:10.1016/s0024-3205(97)00380-9 · Cited by 11 · see citing works
Mannucci, C., Catania, M. A., Adamo, E. B., Bellomo, M., Caputi, A. P., & Calapai, G. (2005) · Journal of Pharmacological Sciences · doi:10.1254/jphs.fpe05001x · Cited by 10 · see citing works
Pandey, S. C., Xu, T., & Zhang, D. (1999) · Neuroscience Letters · doi:10.1016/s0304-3940(99)00172-x · Cited by 9 · see citing works
Katsura, M., Shuto, K., Mohri, Y., Tsujimura, A., & Ohkuma, S. (2001) · Molecular Brain Research · doi:10.1016/s0169-328x(01)00310-2 · Cited by 8 · see citing works
Efficacy of Providing Nicotine in a Liquid Diet to Rats
Halladay, A. K., Schwartz, M., Wagner, G. C., et al. (1999) · Proceedings of The Society for Experimental Biology and Medicine · doi:10.1046/j.1525-1373.1999.d01-79.x · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Reward, addiction, withdrawal to nicotine
De Biasi, M., & Dani, J. A. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113734 · Cited by 366 · see citing works
“Like humans, rodents manifest both somatic and nonsomatic signs of withdrawal (Malin & Goyarzu 2009).”
BackgroundTurner, J. R., Castellano, L. M., & Blendy, J. A. (2010) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.110.166280 · Cited by 88 · see citing works
Mechanistic insights into nicotine withdrawal
Paolini, M., & De Biasi, M. (2011) · Biochemical Pharmacology · doi:10.1016/j.bcp.2011.07.075 · Cited by 66 · see citing works
- Authors
- Malin, D. H., & Goyarzu, P.
- Affiliations
- University of Houston - Clear Lake (US)
- Corresponding author
- Malin, David H.
- ORCID
- Malin, David H.
- Venue
- Handbook of experimental pharmacology
- Publisher
- Springer Berlin Heidelberg
- Published
- 2009
- Issue
- 192
- Pages
- 401-434
- ISSN
- 0171-2004 (ISSN-L)
- OpenAlex
- W180320970
- Cited by
- 89
- References
- 151
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 3 · 2023: 1 · 2022: 1 · 2021: 7 · 2020: 23 · 2019: 4 · 2018: 5 · 2017: 1 · 2016: 3 · 2015: 7 · 2014: 7 · 2013: 8 · 2012: 4
- FWCI
- 16.56
- Type
- book chapter
- Language
- en
- Open access
- closed
- Licence
- Locations
- Handbook of experimental pharmacology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Keywords
- nicotine withdrawal, rodent models, smoking cessation, nicotine craving, sleep disorders, depression-like behavior, anxiety, irritability, mesolimbic dopamine system, ventral tegmental area, nucleus accumbens, endogenous opioid system, amygdala
- MeSH terms
- Animals, Disease Models, Animal, Nicotine, Severity of Illness Index, Smoking, Substance Withdrawal Syndrome, Tobacco Use Disorder, Gene Expression, Smoking Cessation, Nicotinic Agonists, Mice, Rats, Validation Studies as Topic
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review