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Nicotine reinforcement and cognition restored by targeted expression of nicotinic receptors
Abstract
Worldwide, 100 million people are expected to die this century from the consequences of nicotine addiction, but nicotine is also known to enhance cognitive performance. Identifying the molecular mechanisms involved in nicotine reinforcement and cognition is a priority and requires the development of new in vivo experimental paradigms. The ventral tegmental area (VTA) of the midbrain is thought to mediate the reinforcement properties of many drugs of abuse. Here we specifically re-expressed the beta2-subunit of the nicotinic acetylcholine receptor (nAChR) by stereotaxically injecting a lentiviral vector into the VTA of mice carrying beta2-subunit deletions. We demonstrate the efficient re-expression of electrophysiologically responsive, ligand-binding nicotinic acetylcholine receptors in dopamine-containing neurons of the VTA, together with the recovery of nicotine-elicited dopamine release and nicotine self-administration. We also quantified exploratory behaviours of the mice, and showed that beta2-subunit re-expression restored slow exploratory behaviour (a measure of cognitive function) to wild-type levels, but did not affect fast navigation behaviour. We thus demonstrate the sufficient role of the VTA in both nicotine reinforcement and endogenous cholinergic regulation of cognitive functions.
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In the citing paper
“Selective viral reexpression of β2 Ã (Maskos et al. 2005;Pons et al. 2008) or α4 Ã nAChRs in the VTA is sufficient to support both intra-VTA (Maskos et al. 2005) and systemic nicotine self-administration (Pons et al. 2008), identifying the nAChR subtypes necessary for nicotine reinforcement, as well as showing the importance of nAChRs within the VTA itself for this behavior.”
From Mechanisms of Nicotine Addiction (2021) · cites this paper as Maskos et al. 2005
In the citing paper
“ACh provides a complex regulation of reward and motivation behaviors through its actions on dopamine (DA) circuitry [68–72].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [72]
In the citing paper
“Nicotine in adolescence is thus poised to alter DA development, as it acts directly on VTA DA neurons through their expression of nAChRs, modulating their firing rate in a population-specific manner in adult rodents [72, 137–139].”
From Adolescent nicotine exposure and persistent neurocircuitry changes: unveiling lifelong psychiatric risks (2025) · cites this paper as [72]
In the citing paper
“Evidence for this idea stemmed from studies showing that mice lacking the ␣4, ␣6, and/or 2 nAChR subunits fail to self-administer nicotine, whereas re-expression of these subunits in the ventral tegmental area of knockout mice restored nicotine self-administration”
From Varenicline Is a Potent Partial Agonist at α6β2* Nicotinic Acetylcholine Receptors in Rat and Monkey Striatum (2012) · cites this paper as Maskos et al., 2005
In the citing paper
“extensive studies showing that 2, ␣4, or ␣6 nAChRs knockout mice fail to self-administer nicotine (Picciotto et al., 1998;Marubio et al., 2003;Maskos et al., 2005;Pons et al., 2008).”
From Varenicline Is a Potent Partial Agonist at α6β2* Nicotinic Acetylcholine Receptors in Rat and Monkey Striatum (2012) · cites this paper as Maskos et al., 2005
In the citing paper
“particularly because the addictive effects of nicotine are mediated primarily through stimulation of nAChRs in the VTA (Drenan et al., 2008; Maskos et al., 2005; McGranahan et al., 2011; Picciotto et al., 1998).”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Maskos et al., 2005
In the citing paper
“Mice learn to run on a Y-maze to self-administer nicotine into the VTA, an effect that can be diminished by systemic administration of dopamine antagonists”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as Maskos et al., 2005
In the citing paper
“Nicotine reinforcement and reward is mediated through nAChRs in the mesolimbic system (Maskos et al., 2005; McGranahan et al., 2011; Tolu et al., 2012)”
From Mood and anxiety regulation by nicotinic acetylcholine receptors: A potential pathway to modulate aggression and related behavioral states (2015) · cites this paper as Maskos et al., 2005
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A Choreography of Nicotinic Receptors Directs the Dopamine Neuron Routine
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Recent advances in gene manipulation and nicotinic acetylcholine receptor biology
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“…nicotine-induced increase in firing rate in dopaminergic neurons of the ventral tegmental area (VTA) (Picciotto et al., 1998; Chen et al., 2003; Mameli-Engvall et al., 2006), leading to dopamine release and nicotine addiction (Picciotto et al., 1998; Marubio et al., 2003; Maskos et al., 2005).”
BackgroundLotfipour, S., Mandelkern, M. A., & Brody, A. L. (2011) · Current Medical Imaging Formerly Current Medical Imaging Reviews · doi:10.2174/157340511795445676 · Cited by 9
“Furthermore, re-expression of β2-containing nicotinic receptors in the ventral tegmental area can rescue complex cognitive behaviors, including exploration, navigation, and transition probability [16].”
BackgroundAlburges, M. E., Hoonakker, A. J., & Hanson, G. R. (2007) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.06.063 · Cited by 9
“…that: (i) it contains high concentrations of nicotinic acetylcholine receptors (Klink et al., 2001), such as alpha 4 and 7 and beta 2 subunits (Maskos et al., 2005; Klink et al., 2001; Wu et al., 2004), that have been linked to the addicting properties of nicotine-containing products (Maskos…”
BackgroundInfluentialThe Neurobiology of Nicotine Addiction: Clinical and Public Policy Implications
Gardner, P. D., Tapper, A. R., King, J. A., DiFranza, J. R., & Ziedonis, D. M. (2009) · Journal of Drug Issues · doi:10.1177/002204260903900211 · Cited by 9
“Furthermore, re-expression of β2 nAChRs in the VTA via viral-mediated gene delivery restores nicotine self-administration, drug-induced dopaminergic neuron activation, and DA elevation in nucleus accumbens (Maskos et al., 2005).”
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“The α4β2* subtype of the nicotinic acetylcholine receptor (nAChR) has been implicated in mediating the reinforcing effects of nicotine (Maskos et al. 2005).”
TC299423, a Novel Agonist for Nicotinic Acetylcholine Receptors
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“…among the most nicotinesensitive subtypes in the brain, responding to agonist concentrations in the 0.2–0.5 µM range (Matta et al., 2007; Kuryatov and Lindstrom, 2011), and play a crucial role in nicotine reward and reinforcement (Picciotto et al., 1998; Maskos et al., 2005; Walters et al., 2006).”
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“Moreover,studieshaveshown that VTA dopaminergic neuron can be directly activated by addictive drugs 26 – 28 or indirectly regulated by glutamatergic neurons 29 , GABAergic neurons 30,31 , and glial cells 32 , respectively.”
Elucidating the reinforcing effects of nicotine: a tribute to Nadia Chaudhri
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“2012); similar findings were noted with intra-VTA nicotine self-administration (Maskos et al. 2005).”
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“Despite its potential noxious effects, nicotine intake is reinforced via the dopaminergic system (Corrigall et al., 1992; Di Chiara, 2000; Maskos et al. 2005; Tolu et al. 2013; Faure et al. 2014).”
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“Furthermore, knockouts of β2-containing nAChRs were shown to completely shut down the activity of these receptors, with its complete restoration by local re-expression (Guillem et al., 2011; Maskos et al., 2005; Avale et al., 2008).”
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“Particularly, the high-affinity α4β2 subunit-containing nAChRs desensitizing relatively slowly (≃ sec) and located postsynaptically on VTA DA and GABA neurons have been shown to have the most prominent role in nicotine-induced DAergic bursting activity and self-administration, as suggested by mouse knock-out experimen…”
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“Then we took advantage of the compatibility between the two sites XbaI and NheI to directly replace the cDNA coding for the β 2 subunit, cloned between XhoI and NheI in the ptrip β 2-ires-eGFP [79], by the α 7 cDNA.”
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SMOKING CESSATION – WHAT’S NEW?
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“The reinforcing effects of nicotine primarily stem from its binding to β2-containing nicotinic acetylcholine receptors (nAChRs) [10], particularly those with α4β2 subunits, which exhibit the highest affinity for nicotine [11].”
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“To create the pLV-PGK-mCherry-WPRE vector, a two-step strategy was used to substitute the eGFP sequence in the pre-existing pTRIP-PGK-eGFP LV (Maskos et al., 2005).”
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“Whereas β2-subunit gene knockout mice show no increase in self-administration and their mesencephalic dopaminergic neurons were unresponsiveness to nicotine, reinserting the subunit gene in the VTA restored responsiveness to nicotine [Maskos et al., 2005].”
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“…to have the most prominent role in nicotine-induced DAergic bursting activity and self-administration, as suggested by mouse knock-out experiments (Maskos et al., 2005; Changeux, 2010; Faure et al., 2014) and recent direct optogenetic modulation of these somatic receptors (Durand-de Cuttoli et…”
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Metadata
- Authors
- Maskos, U., Molles, B. E., Pons, S., Besson, M., Guiard, B. P., Guilloux, J.-P., Evrard, A., Cazala, P., Cormier, A., Mameli-Engvall, M., Dufour, N., Cloëz-Tayarani, I., Bemelmans, A.-P., Mallet, J., Gardier, A. M., David, V., Faure, P., Granon, S., & Changeux, J.-P.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Université Paris-Sud (FR)
- Corresponding author
- Changeux, J.-P.
- ORCID
- Venue
- Nature
- Published
- 2005-07
- Volume
- 436
- Issue
- 7047
- Pages
- 103-107
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2141456252
- Cited by
- 566
- References
- 32
- Citations by year
- 2026: 7 · 2025: 19 · 2024: 7 · 2023: 18 · 2022: 10 · 2021: 18 · 2020: 21 · 2019: 17 · 2018: 21 · 2017: 17 · 2016: 15 · 2015: 26 · 2014: 32 · 2013: 34 · 2012: 32
- FWCI
- 18.32
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Smoking Behavior and Cessation
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- nicotine, nicotinic acetylcholine receptors, beta2 subunit, ventral tegmental area, dopaminergic neurons, nicotine self-administration, nicotine reinforcement, nicotine dependence, cognitive function, exploratory behavior, lentiviral vectors, cholinergic modulation, dopamine release
- MeSH terms
- Animals, Cognition, Dopamine, Exploratory Behavior, Locomotion, Morphine, Neurons, Nicotine, Receptors, Nicotinic, Gene Expression, Ventral Tegmental Area, Receptors, Adrenergic, beta-2, Mice
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