Hippocampal nAChRs mediate nicotine withdrawal-related learning deficits
Open accessAbstract
Nicotine modulation of learning may contribute to its abuse liability. The role of hippocampal nicotinic acetylcholine receptors (nAChRs) in the effects of acute, chronic and withdrawal from chronic nicotine on learning was assessed via intrahippocampal drug infusion in mice. Acute dorsal hippocampal nicotine infusion enhanced contextual fear conditioning. Conversely, chronic intrahippocampal infusion of a matched dose had no effect, and withdrawal from chronic infusion impaired learning. Thus, hippocampal functional adaptation, evidenced by learning deficits during abstinence, occurs with the transition from acute to chronic nicotine exposure. To investigate which hippocampal nAChRs mediate these adaptations, C57BL/6, beta2 nAChR subunit knockout (KO), and wildtype (WT) mice treated chronically with systemic nicotine received intrahippocampal dihydro-beta-erythroidine (a high affinity nAChR antagonist). Intrahippocampal dihydro-beta-erythroidine precipitated learning deficits in all but the KO mice. Therefore, the action of nicotine at hippocampal beta2 nAChRs mediates adaptations in hippocampal function that underlie withdrawal deficits in contextual fear conditioning.
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β2* nAChRs are implicated in memory-associated deficits during nicotine withdrawal.
“The work also implicated β2* nAChRs in the manifestation of memory-associated deficits during nicotine withdrawal.”
From Nicotine Withdrawal (2015) · cites this paper as Davis and Gould 2009
Infusing a nAChR antagonist (dihydro-β-erythroidine) into the hippocampus of chronically nicotine-treated wild-type mice produces similar deficits in contextual fear learning.
“Similar deficits of contextual fear learning were observed when a nAChR antagonist (dihydro-β-erythroidine) was infused into the hippocampus of WT mice chronically treated with nicotine (Davis and Gould 2009).”
From Nicotine Withdrawal (2015) · cites this paper as Davis and Gould 2009
The withdrawal-induced contextual learning deficit is mediated by direct nicotine effects in the hippocampus.
“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 and Gould, 2009
The hippocampus is necessary and sufficient for nicotine withdrawal-related disruption of contextual fear conditioning.
“These experiments demonstrate that the hippocampus is necessary and sufficient for nicotine withdrawal-related disruption of contextual fear conditioning.”
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 and Gould, 2009
Infusion of DHβE into the hippocampus of mice treated systemically with chronic nicotine precipitates withdrawal deficits in contextual fear conditioning.
“Furthermore, infusion of DHβE (an α4β2 nAChR antagonist) into the hippocampus of mice treated systemically with chronic nicotine precipitated withdrawal deficits in contextual fear conditioning (Davis and Gould, 2009).”
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 and Gould, 2009
Withdrawal deficits in learning are mediated by β2* nAChRs but not α7 nAChRs.
“These withdrawal deficits in learning are mediated by nicotinic acetylcholinergic receptors (nAChRs) containing the β2 subunits (β2* nAChR) but not by those containing the α7 subunit (α7 nAChR) (Davis and Gould, 2009; Portugal 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 and Gould, 2009
Withdrawal from chronic nicotine infusion into the hippocampus, but not cortex or thalamus, produces deficits in contextual fear conditioning.
“However, withdrawal from chronic nicotine infusion into the hippocampus, but not cortex or thalamus, produced deficits in contextual fear conditioning (Davis and Gould, 2009).”
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 and Gould, 2009
Chronic nicotine acts directly in the hippocampus to cause withdrawal symptoms after treatment ends.
“direct drug infusion studies have confirmed that chronic nicotine is acting directly in the hippocampus to produce the withdrawal symptoms when treatment ceases (Davis and Gould, 2009).”
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 and Gould, 2009
Direct nicotine effects in the hippocampus mediate withdrawal-related deficits in contextual learning.
“our prior data demonstrating that direct nicotine effects in the hippocampus mediate withdrawal-related deficits in contextual learning (Davis and Gould, 2009)”
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 and Gould, 2009
Hippocampal β2* nAChRs are involved in nicotine withdrawal learning deficits.
“hippocampal β2* nAChRs are involved in nicotine withdrawal learning deficits (Davis and Gould, 2009; Portugal et al., 2008; Raybuck and Gould, 2009).”
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 and Gould, 2009
The present results and prior work suggest that these effects are mediated by β2* nAChRs.
“The present results and prior work (Davis and Gould, 2009; Portugal et al., 2008; Raybuck and Gould, 2009) suggest that these effects are mediated by β2* nAChRs.”
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 and Gould, 2009
Infusions of the high-affinity nAChR antagonist DhβE into the dorsal hippocampus precipitated withdrawal deficits in contextual and trace fear learning.
“infusions of the high-affinity nAChR antagonist DhβE into the dorsal hippocampus precipitated withdrawal deficits in both contextual (Davis & Gould, 2009) and trace fear learning (Raybuck & Gould, 2009).”
From Nicotine addiction and psychiatric disorders (2015) · cites this paper as Davis & Gould, 2009
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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
Portugal, 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-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-citationAcetylcholine release and inhibitory interneuron activity in hippocampal CA1
McQuiston, A. R. (2014) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2014.00020 · Cited by 55 · see citing works
Miwa, J. M., Lester, H. A., & Walz, A. (2012) · Physiology · doi:10.1152/physiol.00002.2012 · Cited by 52 · see citing works
Nicotinic 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-citationUnraveling the neurobiology of nicotine dependence using genetically engineered mice
Stoker, A. K., & Markou, A. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.02.013 · Cited by 35 · see citing works
Wilkinson, 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-citationThe modulatory role of nicotine on cognitive and non-cognitive functions
Zarrindast, M., & Khakpai, F. (2018) · Brain Research · doi:10.1016/j.brainres.2018.12.002 · Cited by 32 · see citing works
Renda, A., & Nashmi, R. (2014) · BMC Neuroscience · doi:10.1186/1471-2202-15-89 · Cited by 31 · see citing works
Saravia, 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
Divergent Functional Effects of Sazetidine-A and Varenicline During Nicotine Withdrawal
Turner, J. R., Wilkinson, D. S., Poole, R. L., Gould, T. J., Carlson, G. C., & Blendy, J. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.105 · Cited by 29 · see citing works
Self-citationBell, L. A., Bell, K. A., & McQuiston, A. R. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00115 · Cited by 29 · see citing works
Treadmill exercise ameliorates nicotine withdrawal-induced symptoms
Park, S.-S., Shin, M., Park, H.-S., Kim, T.-W., Kim, C., & Lim, B. (2019) · Journal of Exercise Rehabilitation · doi:10.12965/jer.1938228.114 · Cited by 27 · 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-citationMennecke, A., Gossler, A., Hammen, T., Dörfler, A., Stadlbauer, A., Rösch, J., Kornhuber, J., Bleich, S., Doelken, M. T., & Thürauf, N. (2014) · Journal of Neural Transmission · doi:10.1007/s00702-014-1190-6 · Cited by 24 · see citing works
Wilkinson, D. S., & Gould, T. J. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.04.053 · Cited by 20 · see citing works
Self-citationThe efficiency of functional brain networks does not differ between smokers and non-smokers
Breckel, T. P. K., Thiel, C. M., & Gießing, C. (2013) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2013.07.005 · Cited by 20 · 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
Ahmadi‐Soleimani, S. M., Amiry, G. Y., Khordad, E., Masoudi, M., & Beheshti, F. (2023) · Life Sciences · doi:10.1016/j.lfs.2023.122100 · Cited by 17 · see citing works
Nicotine Addiction: Mechanisms and Consequences
Rosenthal, D. G., Weitzman, M. L., & Benowitz, N. L. (2011) · International Journal of Mental Health · doi:10.2753/imh0020-7411400102 · Cited by 17 · see citing works
Laikowski, M. M., Reisdorfer, F., & Moura, S. (2018) · Current Medicinal Chemistry · doi:10.2174/0929867325666180410105135 · Cited by 17 · see citing works
Biała, G., Polak, P., Michalak, A., Kruk-Słomka, M., & Budzyńska, B. (2014) · Pharmacological Reports · doi:10.1016/j.pharep.2014.02.003 · Cited by 17 · see citing works
Upton, M. K., & Lotfipour, S. (2015) · Biochemical Pharmacology · doi:10.1016/j.bcp.2015.06.015 · Cited by 16 · see citing works
Simmons, S. J., & Gould, T. J. (2014) · Journal of Clinical Pharmacy and Therapeutics · doi:10.1111/jcpt.12171 · Cited by 16 · see citing works
Self-citationAbreu‐Villaça, Y., Correa‐Santos, M., Dutra-Tavares, A. C., Paes‐Branco, D., Nunes‐Freitas, A. L., Manhães, A. C., Filgueiras, C. C., & Ribeiro‐Carvalho, A. (2016) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2016.06.002 · 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-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-citationYildirim, E., Connor, D. A., & Gould, T. J. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000111 · 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
Leach, P. T., Holliday, E. D., Kutlu, M. G., & Gould, T. J. (2014) · Nicotine & Tobacco Research · doi:10.1093/ntr/ntu229 · Cited by 12 · see citing works
Self-citationSystems genetic analysis of nicotine withdrawal deficits in hippocampus‐dependent learning
Goldberg, L. R., Kutlu, M. G., Zeid, D., Seemiller, L. R., & Gould, T. J. (2021) · Genes Brain & Behavior · doi:10.1111/gbb.12734 · Cited by 9 · see citing works
Self-citationVarani, A. P., Antonelli, M. C., & Balerio, G. N. (2013) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2013.02.016 · Cited by 7 · see citing works
Translational Research in Nicotine AddictionPreprint
Fisher, M. L., Pauly, J. R., Froeliger, B., & Turner, J. R. (2020) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a039776 · Cited by 6 · see citing works
Lee, C., Quito, J., Poteat, T., Mourikes, V. E., Flaws, J. A., & Mahoney, M. M. (2025) · Toxics · doi:10.3390/toxics13110918 · Cited by 5 · see citing works
Müderrisoğlu, A., Babaoğlu, E., Korkmaz, E. T., Kalkışım, S., Karabulut, E., Emri, S., & Babaoglu, M. O. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.812715 · Cited by 5 · see citing works
Devi, S., Goyal, S., Rathor, B. S., Kumar, P., & Singla, S. (2023) · International Journal of Science and Research Archive · doi:10.30574/ijsra.2023.9.1.0352 · Cited by 5 · see citing works
The Effects of Nicotine on Learning and Memory
Gould, T. J. (2014) · The Receptors · doi:10.1007/978-1-4939-1167-7_11 · Cited by 5 · see citing works
Self-citationPreclinical Models of Nicotine Withdrawal
Shoaib, M., & Hall, F. S. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802574-1.00003-x · Cited by 2 · see citing works
Neurobiology and Mechanisms of Nicotine Addiction
Gogineni, H. P., Sachs, D. P. L., & Brunzell, D. H. (2023) · Respiratory medicine · doi:10.1007/978-3-031-24914-3_3 · Cited by 2 · see citing works
Pharmakologische und nicht-pharmakologische Effekte auf die Kognition
Both, C. (2013) · Univ. Duesseldorf: Duesseldorfer Dokumenten- und Publikationsserver
Contribution of Translational Genetic Research to Our Understanding of Nicotine Dependence
Hall, F. S., Arime, Y., Saber, Y., & Sora, I. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802574-1.00007-7
Kutlu, M. G., Holliday, E. L., & Gould, T. J. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802574-1.00004-1
Self-citationEmergent Cognitive Impairment During Early Nicotine Withdrawal ∗
Schuster, R. M., & Evins, A. E. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-802574-1.00015-6
Esteves, I. D. M. (2016) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.17.2016.tde-26082016-110343
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- Authors
- Davis, J. A., & Gould, T. J.
- Affiliations
- Temple University (US)
- Corresponding author
- Gould, Thomas J.
- Venue
- European Neuropsychopharmacology
- Publisher
- Elsevier BV
- Published
- 2009-08
- Volume
- 19
- Issue
- 8
- Pages
- 551-561
- ISSN
- 0924-977X (ISSN-L)
- PMC
- PMC2777542
- OpenAlex
- W2009923575
- Cited by
- 60
- References
- 76
- Citations by year
- 2025: 1 · 2023: 3 · 2022: 1 · 2021: 1 · 2020: 1 · 2019: 1 · 2018: 2 · 2017: 3 · 2016: 9 · 2015: 7 · 2014: 9 · 2013: 8 · 2012: 5
- FWCI
- 1.88
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- European Neuropsychopharmacology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute on Drug Abuse (F31DA021949, DA017949, R01DA017949, DA024787, DA021949, R01DA024787)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- nicotinic acetylcholine receptors, beta2 nAChR, hippocampus, nicotine withdrawal, learning deficits, contextual fear conditioning, chronic nicotine exposure, dihydro-beta-erythroidine, functional adaptation
- MeSH terms
- Animals, Cerebral Cortex, Conditioning, Operant, Dihydro-beta-Erythroidine, Fear, Hippocampus, Learning Disabilities, Male, Mice, Inbred C57BL, Microinjections, Nicotine, Receptors, Nicotinic, Substance Withdrawal Syndrome, Thalamus, Mice, Knockout, Nicotinic Agonists, Mice
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