Nicotine enhances contextual fear conditioning in C57BL/6J mice at 1 and 7 days post-training
Abstract
Nicotine has been demonstrated to enhance learning processes. The present experiments extend these results to examine the effects of nicotine on acquisition and consolidation of contextual and cued fear conditioning, and the duration of nicotine's enhancement of conditioned fear. C57BL/6 mice were trained with two pairings of an auditory CS and a foot shock US. Multiple doses of nicotine were given before or immediately after training and on testing day (0.0, 0.050, 0.125, 0.250, and 0.375 mg/kg, i.p). Freezing to both the context and auditory CS was measured 24h after training and again 1 week after training. Mice did not receive nicotine for the 1-week retest. Nicotine (0.125 and 0.250 mg/kg) given on both training and testing days enhanced freezing to the context at 24h. In addition, elevated freezing to the context was seen 1 week post-training in mice previously treated with 0.125 and 0.250 mg/kg nicotine. Thus, nicotine-treated mice did show elevated levels of freezing when retested 1 week later, even though no nicotine was administered at the 1-week retest. Mice that received nicotine on training day or testing day only and mice that received nicotine with mecamylamine, a nicotinic receptor antagonist, were not different from saline-treated mice. In addition, post-training administration of nicotine did not enhance fear conditioning. The present results indicate that nicotine enhancement of contextual fear conditioning depends on administration of nicotine on training and test days but results in a long-lasting enhancement of memories of contextual fear conditioning that remains in the absence of nicotine.
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Acute nicotine exposure enhances fear conditioning in mice.
“For example, acute nicotine exposure enhances fear conditioning in mice (Gould and Higgins 2003).”
From The long-term cognitive consequences of adolescent exposure to recreational drugs of abuse (2018) · cites this paper as Gould and Higgins 2003
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Self-citationDavis, J. A., & Gould, T. J. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0047-y · Cited by 78 · see citing works
Self-citationNicotine enhances trace cued fear conditioning but not delay cued fear conditioning in C57BL/6 mice
Gould, T. J., Feiro, O., & Moore, D. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.04.009 · Cited by 78 · see citing works
Self-citationHolliday, E. D., & Gould, T. J. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.04.003 · Cited by 75 · see citing works
Self-citationDavis, J. A., & Gould, T. J. (2007) · Psychopharmacology · doi:10.1007/s00213-006-0624-8 · Cited by 72 · see citing works
Self-citationBesson, M., & Forget, B. (2016) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2016.00160 · Cited by 73 · see citing works
Portugal, G. S., & Gould, T. J. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.05.006 · Cited by 71 · see citing works
Self-citationKenney, J. W., Adoff, M. D., Wilkinson, D. S., & Gould, T. J. (2011) · Psychopharmacology · doi:10.1007/s00213-011-2283-7 · Cited by 67 · see citing works
Self-citationCellular, molecular, and genetic substrates underlying the impact of nicotine on learning
Gould, T. J., & Leach, P. T. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.08.004 · Cited by 68 · see citing works
Self-citationPortugal, G. S., Kenney, J. W., & Gould, T. J. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2007.05.002 · Cited by 66 · see citing works
Self-citationNicotine’s effect on cognition, a friend or foe?
Wang, Q., Du, W., Wang, H., Geng, P., Sun, Y., Zhang, J., Wang, W., & Jin, X. (2023) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2023.110723 · Cited by 66 · see citing works
Kenney, J. W., Raybuck, J. D., & Gould, T. J. (2012) · Hippocampus · doi:10.1002/hipo.22003 · Cited by 65 · see citing works
Self-citationNicotine enhances both foreground and background contextual fear conditioning
Davis, J. A., Porter, J., & Gould, T. J. (2006) · Neuroscience Letters · doi:10.1016/j.neulet.2005.10.026 · Cited by 65 · see citing works
Self-citationNicotine addiction and psychiatric disorders
Kutlu, M. G., Parikh, V., & Gould, T. J. (2015) · International Review of Neurobiology · doi:10.1016/bs.irn.2015.08.004 · Cited by 65 · see citing works
Self-citationNicotinic modulation of hippocampal cell signaling and associated effects on learning and memory
Kutlu, M. G., & Gould, T. J. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.12.008 · Cited by 62 · see citing works
Self-citationVarenicline ameliorates nicotine withdrawal-induced learning deficits in C57BL/6 mice.
Raybuck, J. D., Portugal, G. S., Lerman, C., & Gould, T. J. (2008) · Behavioral Neuroscience · doi:10.1037/a0012601 · Cited by 62 · see citing works
Self-citationSubstance abuse, memory, and post-traumatic stress disorder
Tipps, M. E., Raybuck, J. D., & Lattal, K. M. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.12.002 · Cited by 62 · see citing works
Nicotine and Hippocampus-Dependent Learning: Implications for Addiction
Gould, T. J. (2006) · Molecular Neurobiology · doi:10.1385/mn:34:2:93 · Cited by 61 · see citing works
Self-citationGulick, D., & Gould, T. J. (2007) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.2007.00458.x · Cited by 60 · see citing works
Self-citationPortugal, G. S., Wilkinson, D. S., Kenney, J. W., Sullivan, C., & Gould, T. J. (2012) · Behavior Genetics · doi:10.1007/s10519-011-9489-7 · Cited by 58 · see citing works
Self-citationKeller, J. J., Keller, A. B., Bowers, B. J., & Wehner, J. M. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.03.004 · Cited by 57 · see citing works
Gould, T. J., Portugal, G. S., André, J. M., Tadman, M. P., Marks, M. J., Kenney, J. W., Yildirim, E., & Adoff, M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2012.01.003 · Cited by 56 · see citing works
“During training and testing, each mouse was judged as either freezing or active once every 10 s (Gould and Higgins, 2003).”
Self-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-citationExposure to Kynurenic Acid During Adolescence Produces Memory Deficits in Adulthood
Akagbosu, C., Evans, G. C., Gulick, D., Suckow, R. F., & Bucci, D. J. (2010) · Schizophrenia Bulletin · doi:10.1093/schbul/sbq151 · Cited by 50 · see citing works
Associative 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
Phillips, J. M., Ehrlichman, R. S., & Siegel, S. J. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.11.003 · Cited by 47 · 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-citationNicotine 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-citationKenney, J. W., Florian, C., Portugal, G. S., Abel, T. G., & Gould, T. J. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.153 · Cited by 42 · 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-citationAtomoxetine and nicotine enhance prepulse inhibition of acoustic startle in C57BL/6 mice
Gould, T. J., Rukstalis, M. R., & Lewis, M. C. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.11.073 · Cited by 40 · see citing works
Self-citationHuang, Y.-Y., Kandel, E. R., & Levine, A. A. (2008) · Learning & Memory · doi:10.1101/lm.975308 · Cited by 40 · see citing works
Holliday, 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-citationThe role of working memory and declarative memory in trace conditioning
Connor, D. A., & Gould, T. J. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.07.009 · Cited by 39 · see citing works
Self-citationVarenicline ameliorates ethanol-induced deficits in learning in C57BL/6 mice
Gulick, D., & Gould, T. J. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.03.002 · Cited by 37 · 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-citationDeAngeli, N. E., Todd, T. P., Chang, S. E., Yeh, H. H., Yeh, P. W. L., & Bucci, D. J. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00451 · Cited by 35 · see citing works
Feiro, O., & Gould, T. J. (2004) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2004.11.005 · Cited by 34 · see citing works
Self-citationGould, T. J., & Lewis, M. C. (2005) · Learning & Memory · doi:10.1101/lm.89105 · Cited by 33 · see citing works
Self-citationRaybuck, J. D., & Gould, T. J. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.5.1119 · Cited by 33 · see citing works
Self-citationAndré, J. M., Leach, P. T., & Gould, T. J. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.12.004 · Cited by 32 · see citing works
Self-citationNicotine 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
Kenney, J. W., Poole, R. L., Adoff, M. D., Logue, S. F., & Gould, T. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039939 · Cited by 30 · see citing works
Self-citationBatterman, K. V., & Bucci, D. J. (2011) · Schizophrenia Research · doi:10.1016/j.schres.2011.08.014 · Cited by 30 · see citing works
Gulick, D., & Gould, T. J. (2009) · Neuropharmacology · doi:10.1016/j.neuropharm.2009.05.007 · 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-citationSharp, B. M. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.13970 · Cited by 25 · see citing works
Gould, T. J., Wilkinson, D. S., Yildirim, E., Poole, R. L., Leach, P. T., & Simmons, S. J. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.01.009 · Cited by 24 · see citing works
Self-citationAndré, J. M., Cordero, K. A., & Gould, T. J. (2012) · Behavioral Neuroscience · doi:10.1037/a0027048 · Cited by 24 · see citing works
Self-citationGulick, D., & Gould, T. J. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.45 · 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-citationGitik, 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-citationHall, 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-citationThe 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-citationMineur, Y. S., Ernstsen, C., Islam, A., Maibom, K. L., & Picciotto, M. R. (2020) · Genes Brain & Behavior · doi:10.1111/gbb.12677 · Cited by 14 · see citing works
Kutlu, 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-citationPoole, R. L., Braak, D. C., & Gould, T. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.03.045 · Cited by 13 · see citing works
Self-citationYildirim, E., Connor, D. A., & Gould, T. J. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000111 · Cited by 13 · see citing works
Self-citationSeemiller, L. R., Logue, S. F., & Gould, T. J. (2022) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2022.173429 · Cited by 13 · see citing works
Self-citationBorkar, C. D., Sagarkar, S., Sakharkar, A. J., Subhedar, N. K., & Kokare, D. M. (2017) · Addiction Biology · doi:10.1111/adb.12579 · Cited by 13 · see citing works
Lewis, M. (2003) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(03)00213-2 · Cited by 12 · see citing works
Vago, D. R., & Kesner, R. P. (2006) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2006.11.001 · Cited by 11 · see citing works
Holliday, E. D., & Gould, T. J. (2016) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntw176 · Cited by 10 · see citing works
Self-citationRehman, N. U., Esmaeilpour, K., Joushi, S., Abbas, M., al‐Rashida, M., Rauf, K., & Masoumi‐Ardakani, Y. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110783 · Cited by 10 · see citing works
Keady, J. V., Hessing, M. C., Songrady, J. C., McLaurin, K. A., & Turner, J. R. (2024) · Biology of Sex Differences · doi:10.1186/s13293-024-00656-6 · Cited by 9 · see citing works
Kim, B., & Im, H. (2024) · Behavioral and Brain Functions · doi:10.1186/s12993-024-00227-0 · Cited by 9 · see citing works
Honeycutt, S. C., Paladino, M. S., Camadine, R. D., Mukherjee, A., & Loney, G. C. (2022) · Addiction Biology · doi:10.1111/adb.13170 · Cited by 9 · see citing works
Kirshenbaum, A. P., Johnson, M. W., Schwarz, S. L., & Jackson, E. R. (2009) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2009.06.018 · Cited by 9 · see citing works
Connor, D. A., Kutlu, M. G., & Gould, T. J. (2017) · Journal of Psychopharmacology · doi:10.1177/0269881117695861 · Cited by 8 · see citing works
Self-citation
- Authors
- Gould, T. J., & Stephen Higgins, J.
- Affiliations
- Temple University (US)
- Corresponding author
- Gould, Thomas J.
- ORCID
- Gould, Thomas J.
- Venue
- Neurobiology of Learning and Memory
- Publisher
- Elsevier BV
- Published
- 2003-09
- Volume
- 80
- Issue
- 2
- Pages
- 147-157
- ISSN
- 1074-7427 (ISSN-L)
- OpenAlex
- W2074624311
- Cited by
- 123
- References
- 90
- Citations by year
- 2024: 4 · 2023: 1 · 2022: 3 · 2020: 6 · 2019: 2 · 2018: 10 · 2017: 4 · 2016: 13 · 2015: 8 · 2014: 8 · 2013: 5 · 2012: 7
- FWCI
- 3.36
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neurobiology of Learning and Memory (publishedVersion)
- PubMed (publishedVersion)
- 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, contextual fear conditioning, cued fear conditioning, memory consolidation, long-term memory, mecamylamine, nicotinic acetylcholine receptors, freezing behavior, C57BL/6 mice
- MeSH terms
- Age Factors, Animals, Conditioning, Psychological, Fear, Ganglionic Stimulants, Male, Mice, Inbred C57BL, Nicotine, Teaching, Mice
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