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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Selective viral reexpression of β2* or α4* nAChRs in the VTA is sufficient to support intra-VTA and systemic nicotine self-administration, identifying subtypes necessary for nicotine reinforcement and showing the importance of nAChRs within the VTA.
“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
ACh provides complex regulation of reward and motivation behaviors through its actions on dopamine circuitry.
“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]
Nicotine in adolescence is poised to alter DA development because it acts directly on VTA DA neurons through their expression of nAChRs, modulating their firing rate in a population-specific manner in adult rodents.
“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]
Mice lacking α4, α6, and/or β2 nAChR subunits do not self-administer nicotine, and restoring these subunits in the ventral tegmental area of knockout mice restores nicotine self-administration.
“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
β2, α4, or α6 nAChR knockout mice fail to self-administer nicotine.
“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
The addictive effects of nicotine are mediated primarily through stimulation of nicotinic acetylcholine receptors in the VTA.
“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
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.
“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
Nicotine reinforcement and reward is mediated through nAChRs in the mesolimbic system.
“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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“Maskos et al., 2005 [21]: An elegant study showing that in knockout mice lacking the β2 subunit of the acetylcholine receptor, the rewarding properties of nicotine can be restored by selective re-expression in VTA neurons.”
BackgroundWalters, C. L., Brown, S., Changeux, J.-P., Martin, B., & Damaj, M. I. (2006) · Psychopharmacology · doi:10.1007/s00213-005-0295-x · Cited by 206 · see citing works
“However, when the β2 subunit is re-expressed in the VTA only in these mice, the nicotine-induced dopamine release and nicotine selfadministration are both recovered (Maskos et al. 2005).”
BackgroundSelf-citationDrenan, R. M., Grady, S. R., Whiteaker, P., McClure-Begley, T., McKinney, S., Miwa, J. M., Bupp, S., Heintz, N., McIntosh, J. M., Bencherif, M., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.009 · Cited by 197 · see citing works
“VTA b2* nAChRs are critical mediators of exploratory behavior in mice (Granon et al., 2003; Maskos et al., 2005 Schematic for baseline and nicotineinduced activation of DA neurons.”
Tapia, L., Kuryatov, A., & Lindstrom, J. M. (2006) · Molecular Pharmacology · doi:10.1124/mol.106.030445 · Cited by 196 · see citing works
“4 2* AChRs are sufficient for nicotine reward, tolerance, and sensitization (Tapper et al., 2004; Maskos et al., 2005).”
BackgroundNicotinic acetylcholine receptor β2 subunits in the medial prefrontal cortex control attention
Guillem, K., Bloem, B., Poorthuis, R. B., Loos, M., Smit, A. B., Maskos, U., Spijker, S., & Mansvelder, H. D. (2011) · Science · doi:10.1126/science.1207079 · Cited by 191 · see citing works
Cholinergic modulation of cognitive processing: insights drawn from computational models
Newman, E. L., Gupta, K., Climer, J. R., Monaghan, C. K., & Hasselmo, M. E. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00024 · Cited by 185 · see citing works
Nakamura, M., Oshima, A., Fujimoto, Y., Maruyama, N., Ishibashi, T., & Reeves, K. R. (2007) · Clinical Therapeutics · doi:10.1016/j.clinthera.2007.06.012 · Cited by 185 · see citing works
Nicotine reverses hypofrontality in animal models of addiction and schizophrenia
Koukouli, F., Rooy, M., Tziotis, D., Sailor, K. A., O’Neill, H. C., Levenga, J., Witte, M., Nilges, M., Changeux, J., Hoeffer, C. A., et al. (2017) · Nature Medicine · doi:10.1038/nm.4274 · Cited by 182 · see citing works
“To create the pLV-dsmPGK-β 2-IRES-tdTomato-WPRE vector, we used a previously described PTP-β 2-IRES-GFP-WPRE vector 45 and replaced the full IRES-GFP sequence with IRES-tdTomato available from Clotech (pLVX-IRES-tdTomato) by using the Gateway system.”
Regulation of synaptic transmission and plasticity by neuronal nicotinic acetylcholine receptors
McKay, B. E., Placzek, A. N., & Dani, J. A. (2007) · Biochemical Pharmacology · doi:10.1016/j.bcp.2007.07.001 · Cited by 181 · see citing works
Molecular Mechanisms Underlying Behaviors Related to Nicotine AddictionPreprint
Picciotto, M. R., & Kenny, P. J. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a012112 · Cited by 178 · see citing works
“Selective viral reexpression of b2 (Maskos et al. 2005; Pons et al. 2008) or a4 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…”
A C. elegans Model of Nicotine-Dependent Behavior: Regulation by TRP-Family Channels
Feng, Z., Li, W., Ward, A., Piggott, B. J., Larkspur, E. R., Sternberg, P. W., & Xu, X. Z. S. (2006) · Cell · doi:10.1016/j.cell.2006.09.035 · Cited by 173 · see citing works
“…is the only nAChR that has thus far been found to be essential and sufficient for mediating nicotine dependence in mice (Champtiaux and Changeux, 2004; Maskos et al., 2005; Tapper et al., 2004), we expressed this mouse nAChR as a transgene in the acr-16 mutant background under the acr-16 promoter.”
Cholinergic modulation of midbrain dopaminergic systems
Mena‐Segovia, J., Winn, P., & Bolam, J. P. (2008) · Brain Research Reviews · doi:10.1016/j.brainresrev.2008.02.003 · Cited by 170 · see citing works
“The development of new tools with which to manipulate cholinergic functions in the mesopontine tegmentum and midbrain will be of benefit in resolving this (Clark et al., 2007; Maskos et al., 2005).”
Nicotine aversion: Neurobiological mechanisms and relevance to tobacco dependence vulnerability
Fowler, C. D., & Kenny, P. J. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.09.008 · Cited by 167 · see citing works
Rollema, H., Shrikhande, A., Ward, K., Tingley III, F., Coe, J., O'Neill, B., Tseng, E., Wang, E., Mather, R., Hurst, R., et al. (2010) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2010.00682.x · Cited by 162 · see citing works
“This is consistent with nAChR-mediated dopamine release being predominantly mediated via activation and desensitization of a4b2-containing nAChRs located on dopaminergic and GABAergic neurons (Picciotto et al., 1998; 2008; Mansvelder and McGehee, 2002; Mansvelder et al., 2002; Laviolette and Van der Kooy, 2004; Maskos…”
BackgroundZhao-Shea, R., DeGroot, S. R., Liu, L., Vallaster, M., Pang, X.-Y., Su, Q., Gao, G., Rando, O. J., Martin, G. E., George, O., et al. (2015) · Nature Communications · doi:10.1038/ncomms7770 · Cited by 166 · see citing works
“…on nicotine dependence in animal models have focused on the traditional mesocorticolimbic “reward” circuitry of the central nervous system (CNS) 5–9 , a much more understudied circuit that may be critical for nicotine dependence--the habenulo-interpeduncular pathway 10–12 —has recently gained…”
McGranahan, T. M., Patzlaff, N. E., Grady, S. R., Heinemann, S. F., & Booker, T. K. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0937-11.2011 · Cited by 165 · see citing works
“Reintroduction of the missing subunit into the VTA of 2- or 4-null mutant mice rescued nicotine reward when expressed at high levels, indicating that VTA 4 2*-nAChRs are necessary for nicotine reward (Maskos et al., 2005; Pons et al., 2008).”
BackgroundDiversity of Dopaminergic Neural Circuits in Response to Drug Exposure
Juarez, B., & Han, M. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.32 · Cited by 165 · see citing works
“Reintroducing the β2-subunit into the VTA with specific lentiviruses in β2-KO mice restores nicotine’s reinforcing properties (Mameli-Engvall et al, 2006; Maskos et al, 2005; Tolu et al, 2012).”
BackgroundDopamine Signaling Differences in the Nucleus Accumbens and Dorsal Striatum Exploited by Nicotine
Zhang, T., Zhang, L., Liang, Y., Siapas, A. G., Zhou, F.-M., & Dani, J. A. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0261-09.2009 · Cited by 165 · see citing works
“This firing mode is expected to help mediate the phasic behavioral response to salient environmental stimuli as well as addictive drugs (Schultz et al., 1997; Maskos et al., 2005).”
BackgroundExley, R., Maubourguet, N., David, V., Eddine, R., Evrard, A., Pons, S., Marti, F., Threlfell, S., Cazala, P., McIntosh, J. M., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1103000108 · Cited by 159 · see citing works
“used a previously described mouse model of ICSA (8, 44).”
BackgroundMethodInfluentialPicciotto, M. R., Lewis, A. S., van Schalkwyk, G. I., & Mineur, Y. S. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.12.028 · Cited by 157 · see citing works
The role of the habenula in drug addiction
Velasquez, K. M., Molfese, D. L., & Salas, R. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00174 · Cited by 155 · see citing works
“In summary, the β2 subunit-containing nAChR expressed in the VTA/SNc and in many other areas is essential for reward-related dopamine release in the striatum and is important for nicotinic self-administration in mice (Picciotto et al., 1998; Maskos et al., 2005).”
BackgroundInfluentialCo-activation of VTA DA and GABA neurons mediates nicotine reinforcement
Tolu, S., Eddine, R., Marti, F., David, V, Graupner, M., Pons, S., Baudonnat, M., Husson, M., Besson, M., Reperant, C., et al. (2013) · Molecular Psychiatry · doi:10.1038/mp.2012.83 · Cited by 151 · see citing works
Mechanisms of Nicotine Addiction
Picciotto, M. R., & Kenny, P. J. (2021) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a039610 · Cited by 157 · see citing works
“Selective viral reexpression of β2 (Maskos et al. 2005; Pons et al. 2008) or α4 nAChRs in the VTA is sufficient to support both intra-VTA (Maskos et al.”
BackgroundInfluentialThe habenulo-interpeduncular pathway in nicotine aversion and withdrawal
Antolin-Fontes, B., Ables, J. L., Görlich, A., & Ibañez-Tallon, I. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.11.019 · Cited by 154 · see citing works
“…subunits in the MHbeIPN has been possible through the use of nAChR-mouse models, including null mice (Fowler et al., 2011; Kedmi et al., 2004; Maskos et al., 2005; Picciotto et al., 1998; Salas et al., 2004a, 2003a, 2004b, 2003b, 2009), gain-of-function mice (Broide et al., 2002; Fonck et…”
MethodIkemoto, S., Qin, M., & Liu, Z.-H. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4542-05.2006 · Cited by 151 · see citing works
“Indeed, a recent study showed that mice learn to run on a Y-maze for nicotine administration into the VTA (Maskos et al., 2005).”
BackgroundKenny, P. J., Chartoff, E. H., Roberto, M., Carlezon, W. A., & Markou, A. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.58 · Cited by 148 · see citing works
Cui, Y., Ostlund, S. B., James, A. S., Park, C. S., Ge, W., Roberts, K. W., Mittal, N., Murphy, N. P., Cepeda, C., Kieffer, B. L., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3622 · Cited by 147 · see citing works
Catassi, A., Servent, D., Paleari, L., Cesario, A., & Russo, P. (2008) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2008.04.002 · Cited by 146 · see citing works
“Finally, associated to this addictive effect, nicotine is also known to enhance cognitive performances [40], both properties involving mainly the b2 nAChR subunit present in the ventral tegmental area [41].”
BackgroundSmoking cessation in chronic obstructive pulmonary disease
Tashkin, D. P., & Murray, R. P. (2009) · Respiratory Medicine · doi:10.1016/j.rmed.2009.02.013 · Cited by 142 · see citing works
Microbiota‐gut‐brain axis as a regulator of reward processes
García‐Cabrerizo, R., Carbia, C., O’Riordan, K. J., Schellekens, H., & Cryan, J. F. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15284 · Cited by 147 · see citing works
“Nicotine causes release of DA in VTA activating nicotinic receptors (Maskos et al., 2005).”
BackgroundGlutamatergic synaptic plasticity in the mesocorticolimbic system in addiction
van Huijstee, A. N., & Mansvelder, H. D. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00466 · Cited by 144 · see citing works
“Nicotine increases DA levels by directly stimulating VTA DA neurons through α4β2-containing nicotinic receptors (Maskos et al., 2005).”
BackgroundInfluentialXiao, Y., Fan, H., Musachio, J. L., Wei, Z.-L., Chellappan, S. K., Kozikowski, A. P., & Kellar, K. J. (2006) · Molecular Pharmacology · doi:10.1124/mol.106.027318 · Cited by 141 · see citing works
“Several lines of evidence suggest that the 4 2 nAChR is the major brain nAChR subtype that mediates nicotine addiction (Flores et al., 1992; Picciotto et al., 1998; Marubio et al., 2003; Tapper et al., 2004; Maskos et al., 2005).”
BackgroundBerrendero, F., Robledo, P., Trigo, J. M., Martín-García, E., & Maldonado, R. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.02.006 · Cited by 140 · see citing works
Maskos, U. (2008) · British Journal of Pharmacology · doi:10.1038/bjp.2008.5 · Cited by 139 · see citing works
“However, in the mouse knockout for the high- affinity nicotinic–cholinergic receptor subunit b2 (Picciotto et al., 1995, 1998; Maskos et al., 2005; Maskos, 2007), burst firing is almost completely absent (Mameli-Engvall et al., 2006), but could be restored by the specific lentivirus- mediated…”
BackgroundInfluentialGenetics of nicotinic acetylcholine receptors: Relevance to nicotine addiction
Mineur, Y. S., & Picciotto, M. R. (2007) · Biochemical Pharmacology · doi:10.1016/j.bcp.2007.06.010 · Cited by 138 · see citing works
“The use of viral vectors to express nAChR subunits in specific cells/brain loci on the background of a constitutive knockout has been extremely powerful in identifying the anatomical basis for behavioral and neurochemical effects of nicotine [54,96].”
BackgroundInfluentialScherma, M., Panlilio, L. V., Fadda, P., Fattore, L., Gamaleddin, I., Foll, B. L., Justinová, Z., Mikics, É., Haller, J., Medalie, J., et al. (2008) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.108.142224 · Cited by 138 · see citing works
“, 2008), which are clearly implicated in the rewarding effects of nicotine (Picciotto et al., 1998; Maskos et al., 2005; Walters et al., 2006).”
BackgroundCholinergic modulation of mesolimbic dopamine function and reward
Mark, G. P., Shabani, S., Dobbs, L. K., & Hansen, S. T. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.04.052 · Cited by 137 · see citing works
Intrinsic dopamine and acetylcholine dynamics in the striatum of mice
Krok, A. C., Maltese, M., Mistry, P. N., Miao, X., Li, Y., & Tritsch, N. X. (2023) · Nature · doi:10.1038/s41586-023-05995-9 · Cited by 144 · see citing works
“9e,f), indicating that intrinsic fluctuations in striatal DA depend on the activity of midbrain DANs.”
InfluentialMukhin, A. G., Kimes, A. S., Chefer, S. I., Matochik, J. A., Contoreggi, C. S., Horti, A. G., Vaupel, D. B., Pavlova, O., & Stein, E. A. (2008) · Journal of Nuclear Medicine · doi:10.2967/jnumed.108.050716 · Cited by 135 · see citing works
“This idea is supported by several lines of evidence: these receptors have the highest affinity for nicotine (4); the density of these receptors is greater in smokers and chronically nicotine-treated animals than in nonsmokers (5,6) and saline-treated animals (7,8), respectively, and the density of these receptors in e…”
BackgroundNicotine inhibits the VTA-to-amygdala dopamine pathway to promote anxiety
Nguyen, C., Mondoloni, S., Le Borgne, T., Centeno, I., Come, M., Jehl, J., Solié, C., Reynolds, L. M., Durand-de Cuttoli, R., Tolu, S., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.06.013 · Cited by 136 · see citing works
Tsai, S.-T., Cho, H., Cheng, H., Kim, C.-H., Hsueh, K.-C., Billing, C. B., & Williams, K. E. (2007) · Clinical Therapeutics · doi:10.1016/j.clinthera.2007.06.011 · Cited by 134 · see citing works
The Insula: A Brain Stimulation Target for the Treatment of Addiction
Ibrahim, C., Rubin-Kahana, D. S., Pushparaj, A., Musiol, M., Blumberger, D. M., Daskalakis, Z. J., Zangen, A., & Le Foll, B. (2019) · Frontiers in Pharmacology · doi:10.3389/fphar.2019.00720 · Cited by 133 · see citing works
The medial habenula: still neglected
Viswanath, H., Carter, A. Q., Baldwin, P. R., Molfese, D. L., & Salas, R. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00931 · Cited by 133 · see citing works
“…nAChRs in the VTA, striatum, cortex, and hippocampus have been the focus of nicotinic research to the known role these structures play in nicotine addiction and to the high levels of nAChR expression in these areas (Picciotto et al., 1998; Franceschini et al., 2002; Maskos et al., 2005).”
BackgroundFowler, C. D., Arends, M. A., & Kenny, P. J. (2008) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e32830c360e · Cited by 131 · see citing works
“In contrast, nonrescued b2 knockout mice did not display a preference for either the nicotinepaired or nonpaired arm of the Y-maze (Maskos et al., 2005).”
BackgroundMethodInfluentialDopamine, behavior, and addiction
Wise, R. A., & Jordan, C. J. (2021) · Journal of Biomedical Science · doi:10.1186/s12929-021-00779-7 · Cited by 138 · see citing works
Hendrickson, L. M., Guildford, M. J., & Tapper, A. R. (2013) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2013.00029 · Cited by 132 · see citing works
Tuesta, L. M., Fowler, C. D., & Kenny, P. J. (2011) · Biochemical Pharmacology · doi:10.1016/j.bcp.2011.06.026 · Cited by 129 · see citing works
“Hence, the β2 KO earned far less nicotine than wildtype mice and appeared resistant to the reinforcing properties of the drug [87, 88].”
BackgroundDrenan, R. M., Grady, S. R., Steele, A. D., McKinney, S., Patzlaff, N. E., McIntosh, J. M., Marks, M. J., Miwa, J. M., & Lester, H. A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2056-10.2010 · Cited by 127 · see citing works
“2 subunits are strictly required for nAChR function in midbrain DA neurons (Picciotto et al., 1998; Maskos et al., 2005); 4 subunits are expressed in nearly all DA neurons, and loss of 4 subunits eliminates 80% of surface nAChRs in these cells (Azam et al.”
Role of nicotinic acetylcholine receptors in regulating dopamine neuron activity
Faure, P., Tolu, S., Valverde, S., & Naudé, J. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.05.040 · Cited by 125 · see citing works
Nicotine consumption is regulated by a human polymorphism in dopamine neurons
Morel, C., Fattore, L., Pons, S., Hay, Y. A., Marti, F., Lambolez, B., De Biasi, M., Lathrop, M., Fratta, W., Maskos, U., et al. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.158 · Cited by 123 · see citing works
Neurobiological Mechanisms of Nicotine Reward and Aversion
Wills, L. P., Ables, J. L., Braunscheidel, K. M., Caligiuri, S. P. B., Elayouby, K. S., Fillinger, C., Ishikawa, M., Moen, J. K., & Kenny, P. J. (2022) · Pharmacological Reviews · doi:10.1124/pharmrev.121.000299 · Cited by 126 · see citing works
“Chrnb2 re-expression in the VTA also restored the reinforcing and locomotor-stimulating properties of nicotine in b2 knockout mice (Maskos et al., 2005).”
BackgroundO’Connor, E. C., Parker, D., Rollema, H., & Mead, A. N. (2010) · Psychopharmacology · doi:10.1007/s00213-009-1739-5 · Cited by 118 · see citing works
“These findings are also consistent with reports demonstrating that the disruption of nicotine self-administration induced by deletion of the β2 subunit can be reversed by virally mediated re-expression of the β2 subunit in the ventral tegmental area (Maskos et al. 2005).”
Mazzaferro, S., Benallegue, N., Carbone, A. L., Gasparri, F., Vijayan, R., Biggin, P. C., Moroni, M., & Bermúdez, I. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.262014 · Cited by 119 · see citing works
Liu, L., Zhao-Shea, R., McIntosh, J. M., Gardner, P. D., & Tapper, A. R. (2012) · Molecular Pharmacology · doi:10.1124/mol.111.076661 · Cited by 121 · see citing works
Xiao, C., Zhou, C., Jiang, J., & Cui, Y. (2019) · Acta Pharmacologica Sinica · doi:10.1038/s41401-019-0299-4 · Cited by 120 · see citing works
Habenular TCF7L2 links nicotine addiction to diabetes
Duncan, A., Heyer, M. P., Ishikawa, M., Caligiuri, S. P. B., Liu, X.-A., Chen, Z., Micioni Di Bonaventura, M. V., Elayouby, K. S., Ables, J. L., Howe, W. M., et al. (2019) · Nature · doi:10.1038/s41586-019-1653-x · Cited by 119 · see citing works
Molecules and circuits involved in nicotine addiction: The many faces of smoking
Picciotto, M. R., & Mineur, Y. S. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.04.028 · Cited by 117 · see citing works
“Interestingly, these studies show that b2* nAChR expression in VTA is sufficient for neuronal firing and nicotine reinforcement (Maskos et al., 2005), but that these nAChRs must be expressed in both DA and GABA neurons of the VTA for nicotine to induce burst firing of DA neurons and to support…”
BackgroundMethodInfluentialSchindler, A. G., Messinger, D. I., Smith, J. S., Shankar, H., Gustin, R. M., Schattauer, S. S., Lemos, J. C., Chavkin, N. W., Hagan, C. E., Neumaier, J. F., et al. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3220-12.2012 · Cited by 119 · see citing works
Prefrontal nicotinic receptors control novel social interaction between mice
Avale, M. E., Chabout, J., Pons, S., Serreau, P., De Chaumont, F., Olivo‐Marin, J., Bourgeois, J., Maskos, U., Changeux, J., & Granon, S. (2011) · The FASEB Journal · doi:10.1096/fj.10-178558 · Cited by 114 · see citing works
“Taken together with our previous efficient recovery obtained in more elementary and self-generated choices of action behavior (22, 23), our present results highlight the contribution of the 2 subunit in the PrL area of the mouse to flexible behaviors.”
BackgroundMethodResultInfluentialSelf-citationZhao-Shea, R., Liu, L., Soll, L. G., Improgo, M. R., Meyers, E. E., McIntosh, J. M., Grady, S. R., Marks, M. J., Gardner, P. D., & Tapper, A. R. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.240 · Cited by 113 · see citing works
“Knockout mice that do not express β 2, α 4, or α 6* nAChRs fail to self-administer nicotine but nicotine intake can be rescued via re-expressing these subunits into the VTA, highlighting the importance of this brain structure in nicotine reinforcement (Maskos et al , 2005; Pons et al , 2008).”
- 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 › Physiology › 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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