Rodent Habenulo–Interpeduncular Pathway Expresses a Large Variety of Uncommon nAChR Subtypes, But Only the α3β4 and α3β3β4 Subtypes Mediate Acetylcholine Release
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Recent studies suggest that the neuronal nicotinic receptors (nAChRs) present in the habenulo–interpeduncular (Hb–IPn) system can modulate the reinforcing effect of addictive drugs and the anxiolytic effect of nicotine. Hb and IPn neurons express mRNAs for most nAChR subunits, thus making it difficult to establish the subunit composition of functional receptors. We used immunoprecipitation and immunopurification studies performed in rat and wild-type (+/+) and β2 knock-out (−/−) mice to establish that the Hb and IPn contain significant β2* and β4* populations of nAChR receptors (each of which is heterogeneous). The β4* nAChR are more highly expressed in the IPn. We also identified novel native subtypes (α2β2*, α4β3β2*, α3β3β4*, α6β3β4*). Our studies on IPn synaptosomes obtained from +/+ and α2, α4, α5, α6, α7, β2, β3, and β4−/−mice show that only the α3β4 and α3β3β4 subtypes facilitate acetylcholine (ACh) release. Ligand binding, immunoprecipitation, and Western blotting studies in β3−/−mice showed that, in the IPn of these mice, there is a concomitant reduction of ACh release and α3β4* receptors, whereas the receptor number remains the same in the Hb. We suggest that, in habenular cholinergic neurons, the β3 subunit may be important for transporting the α3β4* subtype from the medial habenula to the IPn. Overall, these studies highlight the presence of a wealth of uncommon nAChR subtypes in the Hb–IPn system and identify α3β4 and α3β3β4, transported from the Hb and highly enriched in the IPn, as the subtypes modulating ACh release in the IPn.
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α2 subunits are highly enriched in the IPN, similar to α5 subunits.
“Similar to α5 subunits, α2 subunits are highly enriched in the IPN (Grady et al. 2009).”
From Mechanisms of Nicotine Addiction (2021) · cites this paper as Grady et al. 2009
The Results (Subunit composition of nAChRs in rat interpeduncular nucleus; page unavailable) report α2 and α5 in the IPN, but classify both as present at moderate levels, not high levels. The Discussion (Native subtypes in the habenulo-interpeduncular system; page unavailable) says α2β2* receptors are restricted to the IPN relative to the habenula. That supports IPN localization, but not the claim that α2 and α5 are both highly enriched there. (LLM, conf=0.86)
Experimental — accuracy not yet measuredThe α5, α3, and β4 subunits are potential targets for treatments of nicotine withdrawal syndrome.
“and are potential targets for treatments of the nicotine withdrawal syndrome (Grady et al. 2009).”
From Nicotine Withdrawal (2015) · cites this paper as Grady et al. 2009
The Discussion (Pathophysiology of α3β4* nAChR subtypes; page unavailable) links α3β4-containing receptors to addictive-drug self-administration, providing some rationale for investigating them. It does not identify α5, α3, and β4 as treatment targets for nicotine withdrawal or assess withdrawal treatments. (LLM, conf=0.78)
Experimental — accuracy not yet measuredAntibody specificity was verified by quantitative immunoprecipitation or immunopurification using nAChRs from various CNS areas of wild-type and null mutant mice, which allowed selection of subunit-specific antibodies.
“Antibody specificity was checked by means of quantitative immunoprecipitation or immunopurification experiments using nAChRs from different areas of the CNS of wild-type α4, α5, α6, β2, β3, and β4 (+/+) and null mutant (−/−) mice, which allowed selection of antibodies specific for the subunit of interest, and assessing the immunoprecipitation capacity of each antibody.”
α3 and β4 nAChR subunits are expressed at high levels in the MHb/IPN axis.
“the α3 and β4 nAChR subunits are expressed at high levels in the MHb/IPN axis [222–224]”
From Mechanistic insights into nicotine withdrawal (2011) · cites this paper as [223]
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Cites
Lateral habenula as a source of negative reward signals in dopamine neurons
Matsumoto, M., & Hikosaka, O. (2007) · Nature · doi:10.1038/nature05860 · Cited by 1,292 · see citing works
Wada, E., Wada, K., Boulter, J., Deneris, E. S., Heinemann, S., Patrick, J., & Swanson, L. W. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902840212 · Cited by 1,044 · see citing works
Clarke, P. B. S., Schwartz, R., Paul, S. M., Cb, P., & Pert, A. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-05-01307.1985 · Cited by 1,037 · see citing works
The central cholinergic system studied by choline acetyltransferase immunohistochemistry in the cat
Kimura, H., McGeer, P. L., Peng, J. H., & McGeer, E. G. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.902000202 · Cited by 966 · see citing works
Efferent connections of the habenular nuclei in the rat
Herkenham, M. A., & Nauta, W. J. H. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901870103 · Cited by 855 · see citing works
Houser, C. R., Crawford, G. D., Barber, R. P., Salvaterra, P. M., & Vaughn, J. E. (1983) · Brain Research · doi:10.1016/0006-8993(83)91312-4 · Cited by 748 · see citing works
Nicotine binding and nicotinic receptor subunit RNA after chronic nicotine treatment
Marks, M., Pauly, Jr., Gross, S., Deneris, E., Hermans-Borgmeyer, I., Heinemann, S., & Collins, A. (1992) · The Journal of Neuroscience · doi:10.1523/jneurosci.12-07-02765.1992 · Cited by 551 · see citing works
Self-citationChamptiaux, N., Gotti, C., Cordero‐Erausquin, M., David, D. J. P., Przybylski, C., Léna, C., Clementi, F., Moretti, M., Rossi, F., Novère, N. G. L., et al. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-21-07820.2003 · Cited by 505 · see citing works
Self-citationZoli, M., Moretti, M., Zanardi, A., McIntosh, J. M., Clementi, F., & Gotti, C. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-20-08785.2002 · Cited by 407 · see citing works
Self-citationSalminen, O., Murphy, K. L., McIntosh, J. M., Drago, J., Marks, M. J., Collins, A. C., & Grady, S. R. (2004) · Molecular Pharmacology · doi:10.1124/mol.65.6.1526 · Cited by 401 · see citing works
Self-citationIdentification of Four Classes of Brain Nicotinic Receptors Using β2 Mutant Mice
Zoli, M., Léna, C., Picciotto, M. R., & Changeux, J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-12-04461.1998 · Cited by 401 · see citing works
Self-citationJi, H., & Shepard, P. D. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0958-07.2007 · Cited by 388 · see citing works
Identification of four classes of brain nicotinic receptors using beta2 mutant mice.
Zoli, M., Léna, C., Picciotto, M. R., & Changeux, J. (1998) · PubMed Central · doi:10.1523/jneurosci.18-12-04461.1996 · Cited by 387 · see citing works
Self-citationLe Novere, N., Zoli, M., & Changeux, J. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01206.x · Cited by 385 · see citing works
Self-citationConroy, W. G., & Berg, D. K. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.9.4424 · Cited by 297 · see citing works
Luo, S., Kulak, J. M., Cartier, G. E., Jacobsen, R. B., Yoshikami, D., Olivera, B. M., & McIntosh, J. M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-21-08571.1998 · Cited by 290 · see citing works
Lecourtier, L., & Kelly, P. H. (2007) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2007.01.004 · Cited by 283 · see citing works
Heterogeneity and complexity of native brain nicotinic receptors
Gotti, C., Moretti, M., Gaimarri, A., Zanardi, A., Clementi, F., & Zoli, M. (2007) · Biochemical Pharmacology · doi:10.1016/j.bcp.2007.05.023 · Cited by 282 · see citing works
Self-citationβ3: A New Member of Nicotinic Acetylcholine Receptor Gene Family Is Expressed in Brain
Deneris, E. S., Boulter, J., Swanson, L. W., Patrick, J., & Heinemann, S. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)83343-9 · Cited by 225 · see citing works
Cui, C., Booker, T. K., Allen, R. S., Grady, S. R., Whiteaker, P., Marks, M. J., Salminen, O., Tritto, T., Butt, C. M., Allen, W. R., et al. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-35-11045.2003 · Cited by 213 · see citing works
Self-citationGroenewegen, H. J., Ahlenius, S., Haber, S. N., Kowall, N. W., & Nauta, W. J. H. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902490107 · Cited by 202 · see citing works
Mulle, C., Vidal, C., Benoit, P., & Changeux, J. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-08-02588.1991 · Cited by 200 · see citing works
Roles of Accessory Subunits in α4β2* Nicotinic Receptors
Kuryatov, A., Onksen, J., & Lindstrom, J. (2008) · Molecular Pharmacology · doi:10.1124/mol.108.046789 · Cited by 195 · see citing works
Dineley‐Miller, K., & Patrick, J. (1992) · Molecular Brain Research · doi:10.1016/0169-328x(92)90244-6 · Cited by 194 · see citing works
Araki, M., McGeer, P. L., & Kimura, H. (1988) · Brain Research · doi:10.1016/0006-8993(88)91410-2 · Cited by 163 · see citing works
Kim, U., & Chang, S.-Y. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20410 · Cited by 159 · see citing works
Grady, S. R., Meinerz, N. M., Cao, J., Reynolds, A. M., Picciotto, M. R., Changeux, J., McIntosh, J. M., Marks, M. J., & Collins, A. C. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00019.x · Cited by 156 · see citing works
Localization of nAChR subunit mRNAs in the brain of Macaca mulatta
Han, Z., Le Novère, N., Zoli, M., Hill, J. A., Champtiaux, N., & Changeux, J. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00262.x · Cited by 156 · see citing works
Self-citationHabenular and interpeduncularis nuclei: shared components in multiple-function networks.
Klemm, W. R. (2004) · PubMed · Cited by 153 · see citing works
α3β4 subunit-containing nicotinic receptors dominate function in rat medial habenula neurons
Quick, M. W., Ceballos, R. M., Kasten, M. R., McIntosh, J. M., & Lester, R. A. J. (1999) · Neuropharmacology · doi:10.1016/s0028-3908(99)00024-6 · Cited by 150 · see citing works
The Lateral Habenula:No Longer Neglected
Geisler, S., & Trimble, M. (2008) · CNS Spectrums · doi:10.1017/s1092852900016710 · Cited by 149 · see citing works
Involvement of the α3 Subunit in Central Nicotinic Binding Populations
Whiteaker, P., Peterson, C. G., Xu, W., McIntosh, J. M., Paylor, R. E., Beaudet, A. L., Collins, A. C., & Marks, M. J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-07-02522.2002 · Cited by 145 · see citing works
Self-citationContestabile, A., Villani, L., Fasolo, A., Franzoni, M. F., Gribaudo, L., Øktedalen, O., & Fonnum, F. (1987) · Neuroscience · doi:10.1016/0306-4522(87)90337-x · Cited by 136 · see citing works
Gotti, C., Moretti, M., Clementi, F., Riganti, L., McIntosh, J. M., Collins, A. C., Marks, M. J., & Whiteaker, P. (2005) · Molecular Pharmacology · doi:10.1124/mol.105.011940 · Cited by 133 · see citing works
Self-citationAltered Anxiety-Related Responses in Mutant Mice Lacking the β4 Subunit of the Nicotinic Receptor
Salas, R., Pieri, F., Fung, B., Dani, J. A., & De Biasi, M. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-15-06255.2003 · Cited by 128 · see citing works
Facilitation of glutamatergic neurotransmission by presynaptic nicotinic acetylcholine receptors
Girod, R., Barazangi, N., McGehee, D., & Role, L. W. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(00)00145-3 · Cited by 122 · see citing works
Dopamine neurones of the ventral tegmentum project to both medial and lateral habenula
Phillipson, O. T., & PYCOCK, C. (1982) · Experimental Brain Research · doi:10.1007/bf00235766 · Cited by 107 · see citing works
Identification of a novel nicotinic binding site in mouse brain using [125I]‐epibatidine
Whiteaker, P., Jimenez, M., McIntosh, J. M., Collins, A. C., & Marks, M. J. (2000) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0703616 · Cited by 105 · see citing works
Self-citationContestabile, A., & Fonnum, F. (1983) · Brain Research · doi:10.1016/0006-8993(83)90989-7 · Cited by 101 · see citing works
Groot‐Kormelink, P. J., Luyten, W. H. M. L., Colquhoun, D., & Sivilotti, L. G. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.25.15317 · Cited by 100 · see citing works
Drenan, R. M., Nashmi, R., Imoukhuede, P., Just, H., McKinney, S., & Lester, H. A. (2008) · Molecular Pharmacology · doi:10.1124/mol.107.039180 · Cited by 100 · see citing works
Han, Z., Zoli, M., Cardona, A., Bourgeois, J., Changeux, J., & Novère, N. G. L. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10659 · Cited by 99 · see citing works
Self-citationInfluence of Neuronal Nicotinic Receptors over Nicotine Addiction and Withdrawal
De Biasi, M., & Salas, R. (2008) · Experimental Biology and Medicine · doi:10.3181/0712-mr-355 · Cited by 95 · see citing works
Clarke, P. B. S., Hamill, G. S., Nadi, N. S., Jacobowitz, D. M., & Pert, A. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902510311 · Cited by 94 · see citing works
Sa√±udo-Pe√±a, M. C., Force, M., Tsou, K., Miller, A. S., & Walker, J. M. (1998) · Synapse · doi:10.1002/(sici)1098-2396(199810)30:2 · Cited by 93 · see citing works
Sheffield, E. B., Quick, M. W., & Lester, R. A. J. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(00)00138-6 · Cited by 87 · see citing works
Chemical transmission in the rat interpeduncular nucleus in vitro.
Brown, D. A., Docherty, R. J., & Halliwell, J. V. (1983) · The Journal of Physiology · doi:10.1113/jphysiol.1983.sp014831 · Cited by 84 · see citing works
Shibata, H., Suzuki, T., & Matsushita, M. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902480210 · Cited by 82 · see citing works
Boorman, J. P., Groot‐Kormelink, P. J., & Sivilotti, L. G. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.00565.x · Cited by 77 · see citing works
Glick, S. D., Ramirez, R. L., Livi, J. M., & Maisonneuve, I. M. (2006) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2006.03.045 · Cited by 76 · see citing works
Gotti, C., Moretti, M., Zanardi, A., Gaimarri, A., Champtiaux, N., Changeux, J., Whiteaker, P., Marks, M. J., Clementi, F., & Zoli, M. (2005) · Molecular Pharmacology · doi:10.1124/mol.105.015925 · Cited by 71 · see citing works
Self-citationGotti, C., Moretti, M., Meinerz, N. M., Clementi, F., Gaimarri, A., Collins, A. C., & Marks, M. J. (2008) · Molecular Pharmacology · doi:10.1124/mol.108.045203 · Cited by 68 · see citing works
Self-citationEckenrode, T. C., Barr, G. A., Battisti, W. P., & Murray, M. (1987) · Brain Research · doi:10.1016/0006-8993(87)90095-3 · Cited by 64 · see citing works
Broadbent, S. D., Groot‐Kormelink, P. J., Krashia, P., Harkness, P. C., Millar, N. S., Beato, M., & Sivilotti, L. G. (2006) · Molecular Pharmacology · doi:10.1124/mol.106.026682 · Cited by 60 · see citing works
Taraschenko, O. D., Shulan, J. M., Maisonneuve, I. M., & Glick, S. D. (2007) · Synapse · doi:10.1002/syn.20396 · Cited by 53 · see citing works
Yeh, J. J., Yasuda, R. P., Dávila‐García, M. I., Xiao, Y., Ebert, S. N., Gupta, T., Kellar, K. J., & Wolfe, B. B. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.t01-1-00259.x · Cited by 52 · see citing works
Decreased anxiety-like behavior in beta3 nicotinic receptor subunit knockout mice
Booker, T. K., Butt, C. M., Wehner, J. M., Heinemann, S. F., & Collins, A. C. (2007) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2007.04.011 · Cited by 49 · see citing works
Heterogeneity of neuronal nicotinic acetylcholine receptors in thin slices of rat medial habenula.
Connolly, J. G., Gibb, A. J., & Colquhoun, D. M. (1995) · The Journal of Physiology · doi:10.1113/jphysiol.1995.sp020650 · Cited by 48 · see citing works
Electrolytic lesions of the habenula attenuate brain stimulation reward
Morissette, M.-C., & Boye, S. M. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.08.021 · Cited by 43 · see citing works
Cholinergic and non-cholinergic forebrain projections to the interpenduncular nucleus
Albanese, A., Castagna, M., & Altavista, M. C. (1985) · Brain Research · doi:10.1016/0006-8993(85)90545-1 · Cited by 38 · see citing works
Fonnum, F., & Contestabile, A. (1984) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1984.tb12814.x · Cited by 37 · see citing works
Marks, M. J., Whiteaker, P., Grady, S. R., Picciotto, M. R., McIntosh, J. M., & Collins, A. C. (2002) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2002.00910.x · Cited by 32 · see citing works
Self-citationBoorman, J. P., Beato, M., Groot‐Kormelink, P. J., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m211719200 · Cited by 29 · see citing works
Induction of Fos-immunostaining by nicotine and nicotinic receptor antagonists in rat brain
Seppä, T., Salminen, O., Moed, M., & Ahtee, L. (2001) · Neuropharmacology · doi:10.1016/s0028-3908(01)00093-4 · Cited by 29 · see citing works
Demonstration of functional α4-containing nicotinic receptors in the medial habenula
Fonck, C., Nashmi, R., Salas, R., Zhou, C., Huang, Q., Biasi, M. D., Lester, R. A. J., & Lester, H. A. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.08.021 · Cited by 26 · see citing works
High resolution spatial mapping of nicotine action using pharmacologic magnetic resonance imaging
Choi, J., Mandeville, J. B., Chen, Y. I., Kim, Y. R., & Jenkins, B. G. (2006) · Synapse · doi:10.1002/syn.20284 · Cited by 23 · see citing works
The interpeduncular nucleus regulates nicotineʼs effects on free-field activity
Hentall, I. D., & Gollapudi, L. A. (1995) · Neuroreport · doi:10.1097/00001756-199512150-00008 · Cited by 19 · see citing works
Li, T., Gao, W., & Rao, Z. (1998) · Brain Research · doi:10.1016/s0006-8993(97)01183-9 · Cited by 14 · see citing works
Adams, M. R., Nikkel, A. L., Donnelly‐Roberts, D. L., et al. (2004) · Molecular Brain Research · doi:10.1016/j.molbrainres.2004.06.019 · Cited by 8 · see citing works
Editorial--Modeling Negative Symptoms: What's Missing?
Shepard, D. S. (2005) · Schizophrenia Bulletin · doi:10.1093/schbul/sbj084 · Cited by 4 · see citing works
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Sorted by citations
Habenular α5 nicotinic receptor subunit signalling controls nicotine intake
Fowler, C. D., Lu, Q., Johnson, P. M., Marks, M. J., & Kenny, P. J. (2011) · Nature · doi:10.1038/nature09797 · Cited by 663 · see citing works
Self-citation<scp>N</scp> icotine and the adolescent brain
Yuan, M., Cross, S. J., Loughlin, S. E., & Leslie, F. M. (2015) · The Journal of Physiology · doi:10.1113/jp270492 · Cited by 582 · see citing works
Structural and functional diversity of native brain neuronal nicotinic receptors
Gotti, C., Clementi, F., Fornari, A., Gaimarri, A., Guiducci, S., Manfredi, I., Moretti, M., Pedrazzi, P., Pucci, L., & Zoli, M. (2009) · Biochemical Pharmacology · doi:10.1016/j.bcp.2009.05.024 · Cited by 469 · see citing works
Self-citationReward, addiction, withdrawal to nicotine
De Biasi, M., & Dani, J. A. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113734 · Cited by 366 · see citing works
“In the mouse, the α5, α2, and β4 nAChR subunits are expressed at high levels in either MHb and/or IPN (De Biasi & Salas 2008, Grady et al. 2009), and no mRNA encoding for nAChR subunits can be detected in the LHb by in situ hybridization techniques.”
BackgroundFrahm, S., Ślimak, M. A., Ferrarese, L., Santos-Torres, J., Antolin-Fontes, B., Auer, S., Filkin, S., Pons, S., Fontaine, J.-F., Tsetlin, V., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.013 · Cited by 283 · see citing works
Diversity of native nicotinic receptor subtypes in mammalian brain
Zoli, M., Pistillo, F., & Gotti, C. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.11.003 · Cited by 277 · see citing works
Self-citationGotti, C., Guiducci, S., Tedesco, V., Corbioli, S., Zanetti, L., Moretti, M., Zanardi, A., Rimondini, R., Mugnaini, M., Clementi, F., et al. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5095-09.2010 · Cited by 226 · see citing works
Self-citationMcLaughlin, I., Dani, J. A., & De Biasi, M. (2015) · Current Topics in Behavioral Neurosciences · doi:10.1007/978-3-319-13482-6_4 · Cited by 173 · see citing works
“They are each densely expressed in the MHb and/or IPN (Salas et al. 2003b, 2004) and are potential targets for treatments of the nicotine withdrawal syndrome (Grady et al. 2009).”
BackgroundTranscriptional and spatial resolution of cell types in the mammalian habenula
Hashikawa, Y., Hashikawa, K., Rossi, M. A., Basiri, M. L., Liu, Y., Johnston, N. L., Ahmad, O. R., & Stuber, G. D. (2020) · Neuron · doi:10.1016/j.neuron.2020.03.011 · 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
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
The 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
Zhao-Shea, R., Liu, L., Pang, X., Gardner, P. D., & Tapper, A. R. (2013) · Current Biology · doi:10.1016/j.cub.2013.09.041 · Cited by 129 · see citing works
An essential role of acetylcholine-glutamate synergy at habenular synapses in nicotine dependence
Frahm, S., Antolin-Fontes, B., Görlich, A., Zander, J.-F., Ahnert-Hilger, G., & Ibañez-Tallon, I. (2015) · eLife · doi:10.7554/elife.11396 · Cited by 98 · see citing works
Different physiological and behavioural effects of e-cigarette vapour and cigarette smoke in mice
Ponzoni, L., Moretti, M., Sala, M., Fasoli, F., Mucchietto, V, Lucini, V, Cannazza, G., Gallesi, G., Castellana, C., Clementi, F., et al. (2015) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2015.06.010 · Cited by 91 · see citing works
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Wolfman, S. L., Gill, D. F., Bogdanic, F., Long, K., Al-Hasani, R., McCall, J. G., Bruchas, M. R., & McGehee, D. S. (2018) · Nature Communications · doi:10.1038/s41467-018-04654-2 · Cited by 81 · see citing works
Jackson, K. J., Sanjakdar, S. S., Muldoon, P. P., McIntosh, J. M., & Damaj, M. I. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.01.017 · Cited by 69 · see citing works
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- Authors
- Grady, S. R., Moretti, M., Zoli, M., Marks, M. J., Zanardi, A., Pucci, L., Clementi, F., & Gotti, C.
- Affiliations
- University of Colorado Boulder (US)
- University of Milan (IT)
- University of Modena and Reggio Emilia (IT)
- Corresponding author
- Gotti, Cecilia
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2009-02-18
- Volume
- 29
- Issue
- 7
- Pages
- 2272-2282
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2680386
- OpenAlex
- W2146586474
- Cited by
- 222
- References
- 70
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 7 · 2023: 11 · 2022: 7 · 2021: 9 · 2020: 13 · 2019: 11 · 2018: 15 · 2017: 11 · 2016: 11 · 2015: 23 · 2014: 23 · 2013: 20 · 2012: 15
- FWCI
- 7.24
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- IRIS UNIMORE (University of Modena and Reggio Emilia) (submittedVersion, cc-by)
- Funders
- Compagnia di San Paolo
- Fondazione Cariplo
- National Institutes of Health
- National Institute on Drug Abuse (DA 015663, P30DA015663, R01DA003194, DA003194)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Keywords
- neuronal nicotinic acetylcholine receptors, medial habenula, interpeduncular nucleus, beta3 subunit, beta2 subunit, acetylcholine release, synaptosomes, drug reinforcement
- MeSH terms
- Acetylcholine, Animals, Male, Mesencephalon, Neural Pathways, Synaptic Transmission, Receptors, Nicotinic, Tegmentum Mesencephali, Rats, Sprague-Dawley, Presynaptic Terminals, Mice, Knockout, Habenula, Protein Subunits, Mice, Rats
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