Withdrawal from Chronic Nicotine Administration Impairs Contextual Fear Conditioning in C57BL/6 Mice
Open accessAbstract
The effects of acute nicotine administration (0.09 mg/kg nicotine), chronic nicotine administration (6.3 mg/kg/d nicotine for 14 d), and withdrawal from chronic nicotine administration on fear conditioning in C57BL/6 mice were examined. Mice were trained using two coterminating conditioned stimulus (30 s; 85 dB white noise)–unconditioned stimulus (2 s; 0.57 mA foot shock) pairings and tested 24 h later for contextual and cued fear conditioning. Acute nicotine administration enhanced contextual fear conditioning, chronic nicotine administration had no effect on contextual fear conditioning, and withdrawal from chronic nicotine administration impaired contextual fear conditioning. Plasma nicotine concentrations were similar after acute and chronic treatment and were within the range reported for smokers. During withdrawal, concentrations of nicotine were undetectable. An acute dose of nicotine (0.09 mg/kg) during withdrawal from chronic nicotine treatment reversed withdrawal-associated deficits in contextual fear conditioning. The results suggest that tolerance to the effects of nicotine on contextual fear conditioning develops with chronic nicotine treatment at a physiologically relevant dose, and withdrawal from this chronic nicotine treatment is associated with impairments in contextual fear conditioning. These findings provide a model of how the effects of nicotine on learning may contribute to the development and maintenance of nicotine addiction.
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Contextual fear conditioning depends on hippocampal signaling.
“Contextual FC is dependent upon hippocampal signaling (Davis et al. 2005)”
From Nicotine Withdrawal (2015) · cites this paper as Davis et al. 2005
Administering nicotine to mice undergoing withdrawal ameliorates the contextual fear conditioning deficit.
“Administration of nicotine to mice undergoing withdrawal ameliorates this deficit (Davis et al. 2005).”
From Nicotine Withdrawal (2015) · cites this paper as Davis et al. 2005
During spontaneous withdrawal from nicotine, mice show deficient contextual fear conditioning compared with saline-treated controls.
“and during spontaneous withdrawal from nicotine, mice exhibit deficient contextual FC relative to saline-treated controls (Davis et al. 2005).”
From Nicotine Withdrawal (2015) · cites this paper as Davis et al. 2005
The effect of nicotine on contextual fear conditioning during withdrawal is not simply due to a lowered threshold of fear responses, because cued fear conditioning was equivalent between nicotine-treated and nicotine-naïve groups.
“This effect was not attributable simply to a lowered threshold of fear responses inherent to the effects of nicotine because cued FC was equivalent between nicotine-treated and nicotine-naïve groups.”
From Nicotine Withdrawal (2015) · cites this paper as Davis et al. 2005
Withdrawal from chronic nicotine disrupts contextual learning in mice.
“Withdrawal from chronic nicotine disrupts contextual learning in mice and this deficit is mediated by direct effects of nicotine in the hippocampus.”
From The duration of nicotine withdrawal-associated deficits in contextual fear conditioning parallels changes in hippocampal high affinity nicotinic acetylcholine receptor upregulation (2012) · cites this paper as Davis et al., 2005
The 6.3 mg/kg/day nicotine dose produces plasma nicotine levels of approximately 13.00 ng/ml in mice, within the range seen in smokers.
“The dose of nicotine was chosen based on our prior research demonstrating that it produced withdrawal deficits in contextual fear conditioning (André et al., 2008; Davis and Gould, 2007b) with plasma nicotine levels of approximately 13.00 ng/ml (Davis et al., 2005), which is within the range seen in smokers (Henningfield and Keenan, 1993).”
From The duration of nicotine withdrawal-associated deficits in contextual fear conditioning parallels changes in hippocampal high affinity nicotinic acetylcholine receptor upregulation (2012) · cites this paper as Davis et al., 2005
Acute nicotine reduces withdrawal-related deficits in hippocampus-dependent learning.
“acute nicotine ameliorates withdrawal-related deficits in hippocampus-dependent learning (Davis et al., 2005).”
From The duration of nicotine withdrawal-associated deficits in contextual fear conditioning parallels changes in hippocampal high affinity nicotinic acetylcholine receptor upregulation (2012) · cites this paper as Davis et al., 2005
Nicotine, varenicline, and bupropion reduce nicotine withdrawal-associated deficits in hippocampus-dependent learning.
“It has been shown that nicotine, varenicline, and bupropion ameliorate nicotine withdrawal-associated deficits in hippocampus-dependent learning (Davis et al., 2005; Portugal and Gould, 2007; Raybuck et al., 2008).”
From The duration of nicotine withdrawal-associated deficits in contextual fear conditioning parallels changes in hippocampal high affinity nicotinic acetylcholine receptor upregulation (2012) · cites this paper as Davis et al., 2005
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“…learning (Davis and Gould, 2009), that direct infusion of acute nicotine into the hippocampus enhances learning (Davis et al., 2007; Gulick and Gould, 2009; Raybuck and Gould, 2010), and acute nicotine ameliorates withdrawal-related deficits in hippocampus-dependent learning (Davis et al., 2005).”
InfluentialSelf-citationRaybuck, J. D., & Gould, T. J. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06580.x · Cited by 53 · see citing works
Self-citationAtomoxetine 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
Self-citationBupropion dose-dependently reverses nicotine withdrawal deficits in contextual fear conditioning
Portugal, G. S., & Gould, T. J. (2007) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2007.08.004 · Cited by 51 · see citing works
Self-citationAssociative Learning, the Hippocampus, and Nicotine Addiction
Gould, T. J., & Davis, J. A. (2008) · Current Drug Abuse Reviews · doi:10.2174/1874473710801010009 · Cited by 49 · see citing works
Self-citationGulick, D., & Gould, T. J. (2007) · Psychopharmacology · doi:10.1007/s00213-007-0982-x · Cited by 49 · see citing works
Self-citationTian, S., Gao, J., Han, L., Fu, J., Li, C., & Li, Z. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.03.005 · Cited by 48 · see citing works
Nicotine enhances context learning but not context-shock associative learning.
Kenney, J. W., & Gould, T. J. (2008) · Behavioral Neuroscience · doi:10.1037/a0012807 · Cited by 45 · see citing works
Self-citationViveros, M., Marco, E. M., Llorente, R., & Lamota, L. (2007) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e3282d28fb4 · Cited by 44 · see citing works
Nicotine withdrawal disrupts new contextual learning
Portugal, G. S., & Gould, T. J. (2008) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2008.11.001 · Cited by 43 · see citing works
Self-citationAcute nicotine delays extinction of contextual fear in mice
Kutlu, M. G., & Gould, T. J. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.01.031 · Cited by 42 · see citing works
Self-citationNicotinic Receptors, Memory, and Hippocampus
Kutlu, M. G., & Gould, T. J. (2015) · Current topics in behavioral neurosciences · doi:10.1007/978-3-319-13665-3_6 · Cited by 41 · see citing works
Self-citationOptimizing treatments for nicotine dependence by increasing cognitive performance during withdrawal
Ashare, R. L., & Schmidt, H. D. (2014) · Expert Opinion on Drug Discovery · doi:10.1517/17460441.2014.908180 · Cited by 40 · see citing works
Saravia, R., Ten-Blanco, M., Grande, M. T., Maldonado, R. J., & Berrendero, F. (2018) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2018.11.003 · Cited by 39 · see citing works
Goldberg, L. R., Zeid, D., Kutlu, M. G., Cole, R. D., Lallai, V., Sebastian, A., Albert, I. U., Fowler, C. D., Parikh, V., & Gould, T. J. (2019) · Addiction Biology · doi:10.1111/adb.12859 · Cited by 38 · see citing works
Self-citationHolliday, E. D., Nucero, P., Kutlu, M. G., Oliver, C., Connelly, K. L., Gould, T. J., & Unterwald, E. M. (2016) · European Journal of Neuroscience · doi:10.1111/ejn.13398 · Cited by 38 · see citing works
Self-citationAndré, J. M., Gulick, D., Portugal, G. S., & Gould, T. J. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.02.018 · Cited by 38 · see citing works
Self-citationNicotine and extinction of fear conditioning
Elias, G. A., Gulick, D., Wilkinson, D. S., & Gould, T. J. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2009.11.022 · Cited by 36 · see citing works
Self-citationDifferential effects of nicotine exposure on the hippocampus across lifespan
Zeid, D., Kutlu, M. G., & Gould, T. J. (2018) · Current Neuropharmacology · doi:10.2174/1570159x15666170714092436 · Cited by 36 · see citing works
Self-citationWilkinson, D. S., Turner, J. R., Blendy, J. A., & Gould, T. J. (2013) · Psychopharmacology · doi:10.1007/s00213-012-2808-8 · Cited by 32 · see citing works
Self-citationSaravia, R., Flores, Á., Plaza‐Zabala, A., Busquets-García, A., Pastor, A., de la Torre, R., Marzo, V. D., Marsicano, G., Ozaita, A., Maldonado, R. J., et al. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.07.007 · Cited by 31 · see citing works
Fisher, M. L., LeMalefant, R., Zhou, L., Huang, G., & Turner, J. R. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.257 · Cited by 31 · see citing works
Nicotine enhances contextual fear memory reconsolidation in rats
Tian, S., Huang, F., Li, P., Zhen-bang, L. I., Zhou, S., Deng, H., & Yang, Y. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.10.058 · Cited by 31 · see citing works
Postweaning, forebrain-specific perturbation of the oxytocin system impairs fear conditioning
Pagani, J. H., Lee, H.-J., & Young, W. S. (2011) · Genes, Brain and Behavior · doi:10.1111/j.1601-183x.2011.00709.x · Cited by 30 · see citing works
Rinker, J. A., Hutchison, M. A., Chen, S. A., Thorsell, A., Heilig, M. A., & Riley, A. L. (2011) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2011.03.009 · Cited by 30 · see citing works
Adolescent nicotine exposure disrupts context conditioning in adulthood in rats
Spaeth, A. M., Barnet, R. C., Hunt, P. S., & Burk, J. A. (2010) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2010.07.011 · Cited by 29 · see citing works
Yamazaki, Y., Fujii, S., Jia, Y., & Sumikawa, K. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05160.x · Cited by 29 · see citing works
Nesil, T., Cao, J., Yang, Z., Chang, S. L., & Li, M. D. (2015) · Molecular Brain · doi:10.1186/s13041-015-0134-x · Cited by 27 · see citing works
Kimmey, B. A., Rupprecht, L. E., Hayes, M. R., & Schmidt, H. D. (2012) · Addiction Biology · doi:10.1111/adb.12014 · Cited by 29 · see citing works
Wilkinson, D. S., & Gould, T. J. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.010 · Cited by 26 · see citing works
Self-citationDissociation of tolerance and nicotine withdrawal-associated deficits in contextual fear
Gould, T. J., Wilkinson, D. S., Yildirim, E., Blendy, J. A., & Adoff, M. D. (2014) · Brain Research · doi:10.1016/j.brainres.2014.02.038 · Cited by 25 · see citing works
Self-citationBromoenol Lactone Attenuates Nicotine-Induced Breast Cancer Cell Proliferation and Migration
Cormier, L. E., Liu, S., Arnold, N., Bethany, B., Rollins, J. D., & Ndinguri, M. W. (2015) · PLoS ONE · doi:10.1371/journal.pone.0143277 · Cited by 24 · see citing works
Nicotine as a conditioned stimulus: Impact of attention-deficit/hyperactivity disorder medications.
Reichel, C. M., Linkugel, J. D., & Bevins, R. A. (2007) · Experimental and Clinical Psychopharmacology · doi:10.1037/1064-1297.15.5.501 · Cited by 24 · see citing works
Leach, P. T., Cordero, K. A., & Gould, T. J. (2013) · Behavioral Neuroscience · doi:10.1037/a0031913 · Cited by 23 · see citing works
Self-citationHolliday, E. D., Logue, S. F., Oliver, C. F., Bangasser, D. A., & Gould, T. J. (2019) · Addiction Biology · doi:10.1111/adb.12769 · Cited by 23 · see citing works
Self-citationNicotine-Derived Compounds as Therapeutic Tools Against Post-Traumatic Stress Disorder.
Barreto, G., Yarkov, A., Avila-Rodriguez, M. F., Aliev, G., & Echeverría, V. (2015) · Current pharmaceutical design · doi:10.2174/1381612821666150710145250 · Cited by 20 · see citing works
Gitik, M., Holliday, E. D., Leung, M., Yuan, Q., Logue, S. F., Tikkanen, R., Goldman, D., & Gould, T. J. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.08.009 · Cited by 21 · see citing works
Self-citationKutlu, M. G., Tumolo, J. M., Holliday, E. D., Garrett, B., & Gould, T. J. (2016) · Learning & Memory · doi:10.1101/lm.042655.116 · Cited by 21 · see citing works
Self-citationWilkinson, D. S., & Gould, T. J. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.04.053 · Cited by 20 · see citing works
Self-citationKutlu, M. G., Connor, D. A., Tumolo, J. M., Cann, C., Garrett, B., & Gould, T. J. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.08.019 · Cited by 20 · see citing works
Self-citationShort- and Long-Lasting Consequences of<i>In Vivo</i>Nicotine Treatment on Hippocampal Excitability
Penton, R. E., Quick, M. W., & Lester, R. A. J. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4362-10.2011 · Cited by 19 · see citing works
Hall, F. S., Markou, A., Levin, E. D., & Uhl, G. R. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06415.x · Cited by 18 · see citing works
Kutlu, M. G., Holliday, E. D., & Gould, T. J. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.11.021 · Cited by 18 · see citing works
Self-citationKutlu, M. G., Oliver, C. F., Huang, P., Liu‐Chen, L., & Gould, T. J. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2016.06.032 · Cited by 16 · see citing works
Self-citationAshare, R. L., Valdez, J. N., Ruparel, K., Albelda, B., Hopson, R. D., Keefe, J. R., Loughead, J., & Lerman, C. E. (2013) · Psychopharmacology · doi:10.1007/s00213-013-3197-3 · Cited by 17 · see citing works
Time dependency of craving and response inhibition during nicotine abstinence
Tsaur, S., Strasser, A. A., Souprountchouk, V., Evans, G. C., & Ashare, R. L. (2014) · Addiction Research & Theory · doi:10.3109/16066359.2014.953940 · Cited by 17 · see citing works
The effects of acute nicotine on contextual safety discrimination
Kutlu, M. G., Oliver, C. F., & Gould, T. J. (2014) · Journal of Psychopharmacology · doi:10.1177/0269881114552743 · Cited by 16 · see citing works
Self-citationSimmons, S. J., & Gould, T. J. (2014) · Journal of Clinical Pharmacy and Therapeutics · doi:10.1111/jcpt.12171 · Cited by 16 · see citing works
Self-citationMetaxas, A., Al‐Hasani, R., Farshim, P. P., Tubby, K. C., Berwick, A., Ledent, C. A., Hourani, S. M. O., Kitchen, I., & Bailey, A. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.03.023 · Cited by 15 · see citing works
Parikh, V., Cole, R. D., Patel, P., Poole, R. L., & Gould, T. J. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.01.003 · Cited by 15 · see citing works
Self-citationTranslational Research on Nicotine Dependence
Falcone, M., Lee, B., Lerman, C. E., & Blendy, J. A. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_5005 · Cited by 15 · see citing works
Connor, D. A., & Gould, T. J. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.07.033 · Cited by 15 · see citing works
Self-citationCole, R. D., Wolsh, C. C., Zimmerman, M., Harrington, E. N., Gould, T. J., & Parikh, V. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.07.019 · Cited by 15 · see citing works
Self-citationKutlu, M. G., Zeid, D., Tumolo, J. M., & Gould, T. J. (2018) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2017.06.010 · Cited by 14 · see citing works
Self-citation
- Authors
- Davis, J. A., James, J. R., Siegel, S. J., & Gould, T. J.
- Affiliations
- Temple University (US)
- Virginia Commonwealth University (US)
- University of Pennsylvania (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2005-09-21
- Volume
- 25
- Issue
- 38
- Pages
- 8708-8713
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2697573
- OpenAlex
- W2088102722
- Cited by
- 146
- References
- 45
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 5 · 2023: 4 · 2022: 1 · 2021: 4 · 2020: 2 · 2019: 4 · 2018: 7 · 2017: 6 · 2016: 15 · 2015: 14 · 2014: 17 · 2013: 8 · 2012: 8
- FWCI
- 4.30
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Pennsylvania Department of Health
- Temple University
- National Institutes of Health (DA017949)
- U.S. Public Health Service (P5084718)
- National Institute on Drug Abuse (DA017949, R01DA017949, T32DA 07237, P5084718, T32DA007237)
- National Cancer Institute (P5084718)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Keywords
- nicotine, nicotine withdrawal, contextual fear conditioning, cued fear conditioning, chronic nicotine administration, acute nicotine administration, tolerance (pharmacology and immunology), nicotine dependence, C57BL/6 mice, plasma nicotine concentration, learning deficits
- MeSH terms
- Animals, Conditioning, Psychological, Fear, Male, Mice, Inbred C57BL, Nicotine, Substance Withdrawal Syndrome, Mice
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