Nicotine withdrawal‐induced deficits in trace fear conditioning in C57BL / 6 mice – a role for high‐affinity β2 subunit‐containing nicotinic acetylcholine receptors
Open accessAbstract
Nicotine alters cognitive processes that include working memory and long-term memory. Trace fear conditioning may involve working memory during acquisition while also allowing the assessment of long-term memory. The present study used trace fear conditioning in C57BL/6 mice to investigate the effects of acute nicotine, chronic nicotine and withdrawal of chronic nicotine on processes active during acquisition and recall 24 h later and to examine the nicotinic acetylcholine receptor subtypes (nAChRs) involved in withdrawal deficits in trace fear conditioning. During training, acute nicotine (0.09 mg/kg) enhanced, but chronic nicotine (6.3 mg/kg/day, 13 days) and withdrawal of chronic nicotine (6.3 mg/kg/day, 12 days) had no significant effect on, acquisition of trace conditioning. At recall, acute treatment enhanced conditioning while chronic nicotine had no effect and withdrawal of chronic nicotine resulted in deficits. Antagonist-precipitated withdrawal was used to characterize the nAChRs involved in the withdrawal deficits. The low-affinity nAChR antagonist MLA (1.5, 3 or 9 mg/kg) had no effect on trace fear conditioning, but the high-affinity nAChR antagonist DHbetaE (3 mg/kg) precipitated deficits in trace fear conditioning if administered at training or training and testing, but not if administered at testing alone. The beta2 nAChR subunit is involved in the withdrawal effects as withdrawal of chronic nicotine produced deficits in trace fear conditioning in wildtype but not in beta2-knockout mice. Thus, nicotine alters processes involved in both acquisition and long-term memory of trace fear conditioning, and high-affinity beta2 subunit-containing nAChRs are critically involved in the effects of nicotine withdrawal on trace fear conditioning.
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The DHβE-precipitated trace fear conditioning deficit implicates high-affinity nAChRs containing α4 and β2/β4 subunits.
“implicating high-affinity receptors such as those containing the α4, and the β2/β4 nAChR subunits”
From Mechanistic insights into nicotine withdrawal (2011) · cites this paper as [201]
Systemic NMDA receptor antagonists inhibit acquisition of contextual fear conditioning, and this effect is ameliorated by nicotine acting at α4β2-containing nAChRs.
“Also, systemic administration of NMDA receptor antagonists inhibits acquisition of contextual fear conditioning [200]. This effect is ameliorated by co-administration of systemic nicotine acting at α4β2-containing nAChRs, as indicated by antagonism with DHβE [200].”
From Mechanistic insights into nicotine withdrawal (2011) · cites this paper as [200]
Spontaneous withdrawal from chronic nicotine causes deficits in acquisition of trace fear conditioning.
“Raybuck and Gould [201] demonstrated that spontaneous withdrawal from chronic nicotine leads to deficits in the acquisition of trace fear conditioning.”
From Mechanistic insights into nicotine withdrawal (2011) · cites this paper as [201]
Withdrawal precipitated by DHβE, but not MLA, produces a trace fear conditioning deficit similar to spontaneous withdrawal.
“Withdrawal precipitated by DHβE, but not methyllycaconitine (MLA), led to a similar deficit”
From Mechanistic insights into nicotine withdrawal (2011) · cites this paper as [201]
β2-null mice do not show a trace fear conditioning deficit after spontaneous nicotine withdrawal.
“β2-null mice were not observed to have a deficit in trace fear conditioning upon spontaneous nicotine withdrawal [201].”
From Mechanistic insights into nicotine withdrawal (2011) · cites this paper as [201]
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Weike, A. I., Schupp, H. T., & Hamm, A. O. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.3.685 · Cited by 31 · see citing works
Trivedi, M. A., & Coover, G. D. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.11.029 · Cited by 24 · see citing works
Effects of Smoking and Smoking Deprivation on the Articulatory Loop of Working Memory
Blake, J. J., & Smith, A. P. (1997) · Human Psychopharmacology Clinical and Experimental · doi:10.1002/(sici)1099-1077(199705/06)12:3 · Cited by 23 · see citing works
An opponent process theory of habitual behavior with special reference to smoking.
Jw, T. (1977) · PubMed · Cited by 15 · see citing works
Seo, D.-O., Pang, M.-H., Shin, M.-S., Kim, H.-T., & Choi, J.-S. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.04.011 · Cited by 14 · see citing works
Regulating the regulators: The role of nicotinic acetylcholine receptors in human epilepsy
Hogg, R. C., & Bertrand, D. (2003) · Drug News & Perspectives · doi:10.1358/dnp.2003.16.5.829313 · Cited by 14 · see citing works
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- Cohen BH 2001 Explaining Psychological Stastistics New York Wiley
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Cognitive function during nicotine withdrawal: Implications for nicotine dependence treatment
Ashare, R. L., Falcone, M., & Lerman, C. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.034 · Cited by 170 · see citing works
Bridging the interval: Theory and neurobiology of trace conditioning
Raybuck, J. D., & Lattal, K. M. (2014) · Behavioural Processes · doi:10.1016/j.beproc.2013.08.016 · Cited by 114 · see citing works
Self-citationNicotine modulation of fear memories and anxiety: Implications for learning and anxiety disorders
Kutlu, M. G., & Gould, T. J. (2015) · Biochemical Pharmacology · doi:10.1016/j.bcp.2015.07.029 · Cited by 97 · 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-citationMechanistic 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
Nicotine 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-citationGould, 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
“…prior work has shown that a7nAChRs are not involved in the effects of nicotine on contextual fear conditioning or nicotine withdrawal-associated deficits in hippocampus-dependent learning (André et al., 2011; Davis and Gould, 2006, 2007a, 2009; Portugal et al., 2008; Raybuck and Gould, 2009).”
InfluentialSelf-citation
- Authors
- Raybuck, J. D., & Gould, T. J.
- Affiliations
- Temple University (US)
- Corresponding author
- Gould, T. J.
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2009-01
- Volume
- 29
- Issue
- 2
- Pages
- 377-387
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- PMC
- PMC2746945
- OpenAlex
- W1983587045
- Cited by
- 53
- References
- 106
- Citations by year
- 2023: 1 · 2022: 3 · 2021: 1 · 2020: 3 · 2019: 1 · 2018: 1 · 2017: 3 · 2016: 9 · 2015: 5 · 2014: 8 · 2013: 7 · 2012: 4
- FWCI
- 1.47
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Institute on Drug Abuse (DA017949, R01DA017949, T32DA 07237, P50DA84718, T32DA007237)
- National Cancer Institute
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Keywords
- nicotine withdrawal, trace fear conditioning, nicotinic acetylcholine receptors, beta2 subunit, long-term memory, working memory, chronic nicotine
- MeSH terms
- Animals, Avoidance Learning, Conditioning, Psychological, Disease Models, Animal, Drug Administration Schedule, Fear, Male, Memory, Short-Term, Mice, Inbred C57BL, Nicotine, Receptors, Nicotinic, Substance Withdrawal Syndrome, Tobacco Use Disorder, Mice, Knockout, Nicotinic Agonists, Nicotinic Antagonists, Mice
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