Co-activation of VTA DA and GABA neurons mediates nicotine reinforcement (original) (raw)

• WHO. World Health Organization Report on the Global Tobacco Epidemic, available from: http://www.who.int/tobacco/mpower/2009/en/, 2009.
• Changeux JP . Nicotine addiction and nicotinic receptors: lessons from genetically modified mice. Nat Rev Neurosci 2010; 11: 389–401.
  Article CAS Google Scholar
• Taly A, Corringer PJ, Guedin D, Lestage P, Changeux JP . Nicotinic receptors: allosteric transitions and therapeutic targets in the nervous system. Nat Rev Drug Discov 2009; 8: 733–750.
  Article CAS Google Scholar
• Marti F, Arib O, Morel C, Dufresne V, Maskos U, Corringer PJ et al. Smoke extracts and nicotine, but not tobacco extracts, potentiate firing and burst activity of ventral tegmental area dopaminergic neurons in mice. Neuropsychopharmacology 2011; 36: 2244–2257.
  Article CAS Google Scholar
• Changeux JP, Edelstein SJ . Nicotinic Acetylcholine Receptors: From Molecular Biology to Cognition. Odile Jacob: New York, 2005.
  Google Scholar
• Pontieri FE, Tanda G, Orzi F, Chiara GD . Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs. Nature 1996; 382: 255–257.
  Article CAS Google Scholar
• Picciotto MR, Zoli M, Rimondini R, Lena C, Marubio LM, Pich EM et al. Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine. Nature 1998; 391: 173–177.
  Article CAS Google Scholar
• Klink R, de Kerchove d’Exaerde A, Zoli M, Changeux JP . Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J Neurosci 2001; 21: 1452–1463.
  Article CAS Google Scholar
• Mansvelder HD, McGehee DS . Cellular and synaptic mechanisms of nicotine addiction. J Neurobiol 2002; 53: 606–617.
  Article CAS Google Scholar
• Laviolette SR, van der Kooy D . The neurobiology of nicotine addiction: bridging the gap from molecules to behaviour. Nat Rev Neurosci 2004; 5: 55–65.
  Article CAS Google Scholar
• Mansvelder HD, Keath JR, McGehee DS . Synaptic mechanisms underlie nicotine-induced excitability of brain reward areas. Neuron 2002; 33: 905–919.
  Article CAS Google Scholar
• Mansvelder HD, McGehee DS . Long-term potentiation of excitatory inputs to brain reward areas by nicotine. Neuron 2000; 27: 349–357.
  Article CAS Google Scholar
• Luscher C, Malenka RC . Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 2011; 69: 650–663.
  Article Google Scholar
• Sulzer D . How addictive drugs disrupt presynaptic dopamine neurotransmission. Neuron 2011; 69: 628–649.
  Article CAS Google Scholar
• Mameli-Engvall M, Evrard A, Pons S, Maskos U, Svensson TH, Changeux JP et al. Hierarchical control of dopamine neuron-firing patterns by nicotinic receptors. Neuron 2006; 50: 911–921.
  Article CAS Google Scholar
• Dani JA, Bertrand D . Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu Rev Pharmacol Toxicol 2007; 47: 699–729.
  Article CAS Google Scholar
• Olivo-Marin JC . Extraction of spots in biological images using multiscale products. Pattern Recogn 2002; 35: 1989–1996.
  Article Google Scholar
• Tolu S, Avale ME, Nakatani H, Pons S, Parnaudeau S, Tronche F et al. A versatile system for the neuronal subtype specific expression of lentiviral vectors. FASEB J 2010; 24: 723–730.
  Article CAS Google Scholar
• Maskos U, Molles BE, Pons S, Besson M, Guiard BP, Guilloux JP et al. Nicotine reinforcement and cognition restored by targeted expression of nicotinic receptors. Nature 2005; 436: 103–107.
  Article CAS Google Scholar
• David V, Cazala P . A comparative study of self-administration of morphine into the amygdala and the ventral tegmental area in mice. Behav Brain Res 1994; 65: 205–211.
  Article CAS Google Scholar
• David V, Durkin TP, Cazala P . Differential effects of the dopamine D2/D3 receptor antagonist sulpiride on self-administration of morphine into the ventral tegmental area or the nucleus accumbens. Psychopharmacology (Berl) 2002; 160: 307–317.
  Article CAS Google Scholar
• David V, Segu L, Buhot MC, Ichaye M, Cazala P . Rewarding effects elicited by cocaine microinjections into the ventral tegmental area of C57BL/6 mice: involvement of dopamine D1 and serotonin1B receptors. Psychopharmacology (Berl) 2004; 174: 367–375.
  Article CAS Google Scholar
• David V, Gold LH, Koob GF, Cazala P . Anxiogenic-like effects limit rewarding effects of cocaine in balb/cbyj mice. Neuropsychopharmacology 2001; 24: 300–318.
  Article CAS Google Scholar
• David V, Besson M, Changeux JP, Granon S, Cazala P . Reinforcing effects of nicotine microinjections into the ventral tegmental area of mice: dependence on cholinergic nicotinic and dopaminergic D1 receptors. Neuropharmacology 2006; 50: 1030–1040.
  Article CAS Google Scholar
• Mason PA, Milner PM, Miousse R . Preference paradigm: provides better self-stimulation reward discrimination than a rate-dependent paradigm. Behav Neural Biol 1985; 44: 521–529.
  Article CAS Google Scholar
• David V, Matifas A, Gavello-Baudy S, Decorte L, Kieffer BL, Cazala P . Brain regional Fos expression elicited by the activation of mu- but not delta-opioid receptors of the ventral tegmental area: evidence for an implication of the ventral thalamus in opiate reward. Neuropsychopharmacology 2008; 33: 1746–1759.
  Article CAS Google Scholar
• Maskos U . Emerging concepts: novel integration of in vivo approaches to localise the function of nicotinic receptors. J Neurochem 2007; 100: 596–602.
  Article CAS Google Scholar
• Wise R . Brain reward circuitry: insights from unsensed incentives. Neuron 2002; 36: 229–240.
  Article CAS Google Scholar
• Maskos U . The cholinergic mesopontine tegmentum is a relatively neglected nicotinic master modulator of the dopaminergic system: relevance to drugs of abuse and pathology. Br J Pharmacol 2008; 153 (Suppl 1): S438–S445.
  CAS PubMed PubMed Central Google Scholar
• Maskos U . Role of endogenous acetylcholine in the control of the dopaminergic system via nicotinic receptors. J Neurochem 2010; 114: 641–646.
  Article CAS Google Scholar
• Petersen DR, Norris KJ, Thompson JA . A comparative study of the disposition of nicotine and its metabolites in three inbred strains of mice. Drug Metab Dispos 1984; 12: 725–731.
  CAS PubMed Google Scholar
• Graupner M, Gutkin BS . Modeling nicotinic neuromodulation from global functional and network levels to nAChR based mechanisms. Acta Pharmacol Sin 2009; 30: 681–693.
  Article CAS Google Scholar
• Graupner M, Gutkin BS In: Gutkin BS, Ahmed SH (eds). Computational Neuroscience of Drug Addiction, Computational Neuroscience Series. Springer Verlag: Berlin, 2011, pp 111–144.
  Google Scholar
• Dobi A, Margolis EB, Wang H-L, Harvey BK, Morales M . Glutamatergic and nonglutamatergic neurons of the ventral tegmental area establish local synaptic contacts with dopaminergic and nondopaminergic neurons. J Neurosci 2010; 30: 218–229.
  Article CAS Google Scholar
• Graupner M, Gutkin BS . Tonic acetylcholine governs the phasic mesolimbic dopamine response to nicotine. PLoS Comp Biol 2012 (under consideration).
• Turiault M, Parnaudeau S, Milet A, Parlato R, Rouzeau JD, Lazar M et al. Analysis of dopamine transporter gene expression pattern—generation of DAT-iCre transgenic mice. FEBS J 2007; 274: 3568–3577.
  Article CAS Google Scholar
• Fuchs EC, Doheny H, Faulkner H, Caputi A, Traub RD, Bibbig A et al. Genetically altered AMPA-type glutamate receptor kinetics in interneurons disrupt long-range synchrony of gamma oscillation. Proc Natl Acad Sci USA 2001; 98: 3571–3576.
  Article CAS Google Scholar
• Fields HL, Hjelmstad GO, Margolis EB, Nicola SM . Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu Rev Neurosci 2007; 30: 289–316.
  Article CAS Google Scholar
• Bromberg-Martin ES, Matsumoto M, Hikosaka O . Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 2010; 68: 815–834.
  Article CAS Google Scholar
• Valjent E, Pages C, Herve D, Girault JA, Caboche J . Addictive and non-addictive drugs induce distinct and specific patterns of ERK activation in mouse brain. Eur J Neurosci 2004; 19: 1826–1836.
  Article Google Scholar
• Girault JA, Valjent E, Caboche J, Herve D . ERK2: a logical AND gate critical for drug-induced plasticity? Curr Opin Pharmacol 2007; 7: 77–85.
  Article CAS Google Scholar
• Grace AA . Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 1991; 41: 1–24.
  Article CAS Google Scholar
• Schultz W . Multiple dopamine functions at different time courses. Annu Rev Neurosci 2007; 30: 259–288.
  Article CAS Google Scholar
• Gonon FG . Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry. Neuroscience 1988; 24: 19–28.
  Article CAS Google Scholar
• Chergui K, Svenningsson P, Nomikos GG, Gonon F, Fredholm BB, Svennson TH . Increased expression of NGFI-A mRNA in the rat striatum following burst stimulation of the medial forebrain bundle. Eur J Neurosci 1997; 9: 2370–2382.
  Article CAS Google Scholar
• Tsai HC, Zhang F, Adamantidis A, Stuber GD, Bonci A, de Lecea L et al. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 2009; 324: 1080–1084.
  Article CAS Google Scholar
• Corrigall WA . Nicotine self-administration in animals as a dependence model. Nicotine Tob Res 1999; 1: 11–20.
  Article CAS Google Scholar
• Rose JE, Corrigall WA . Nicotine self-administration in animals and humans: similarities and differences. Psychopharmacology (Berl) 1997; 130: 28–40.
  Article CAS Google Scholar
• Wessler I, Kirkpatrick CJ . Acetylcholine beyond neurons: the non-neuronal cholinergic system in humans. Br J Pharmacol 2008; 154: 1558–1571.
  Article CAS Google Scholar
• Nair-Roberts RG, Chatelain-Badie SD, Benson E, White-Cooper H, Bolam JP, Ungless MA . Stereological estimates of dopaminergic, GABAergic and glutamatergic neurons in the ventral tegmental area, substantia nigra and retrorubral field in the rat. Neuroscience 2008; 152: 1024–1031.
  Article CAS Google Scholar
• Nashmi R, Xiao C, Deshpande P, McKinney S, Grady SR, Whiteaker P et al. Chronic nicotine cell specifically upregulates functional alpha 4* nicotinic receptors: basis for both tolerance in midbrain and enhanced long-term potentiation in perforant path. J Neurosci 2007; 27: 8202–8218.
  Article CAS Google Scholar
• Schultz W . Getting formal with dopamine and reward. Neuron 2002; 36: 241–263.
  Article CAS Google Scholar
• Zweifel LS, Parker JG, Lobb CJ, Rainwater A, Wall VZ, Fadok JP et al. Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior. Proc Natl Acad Sci USA 2009; 106: 7281–7288.
  Article CAS Google Scholar
• Overton PG, Clark D . Burst firing in midbrain dopaminergic neurons. Brain Res 1997; 25: 312–334.
  Article CAS Google Scholar
• Tepper JM, Lee CR In: Tepper JM, Abercrombie ED, Bolam JP (eds). Progress in Brain Research Vol. 160. Elsevier: Amsterdam, pp 189–208##2007.
  Google Scholar
• Deister CA, Teagarden MA, Wilson CJ, Paladini CA . An intrinsic neuronal oscillator underlies dopaminergic neuron bursting. J Neurosci 2009; 29: 15888–15897.
  Article CAS Google Scholar
• Canavier CC, Landry RS . An increase in AMPA and a decrease in SK conductance increase burst firing by different mechanisms in a model of a dopamine neuron in vivo. J Neurophysiol 2006; 96: 2549–2563.
  Article CAS Google Scholar
• Kitai ST, Shepard PD, Callaway JC, Scroggs R . Afferent modulation of dopamine neuron firing patterns. Curr Opin Neurobiol 1999; 9: 690–697.
  Article CAS Google Scholar
• Exley R, Maubourguet N, David V, Eddine R, Evrard A, Pons S et al. Distinct contributions of nicotinic acetylcholine receptor subunit {alpha}4 and subunit {alpha}6 to the reinforcing effects of nicotine. Proc Natl Acad Sci USA 2011; 108: 7577–7582.
  Article CAS Google Scholar
• Floresco SB, West AR, Ash B, Moore H, Grace AA . Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat Neurosci 2003; 6: 968–973.
  Article CAS Google Scholar
• Grace AA, Floresco SB, Goto Y, Lodge DJ . Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci 2007; 30: 220–227.
  Article CAS Google Scholar
• Lodge DJ, Grace AA . The laterodorsal tegmentum is essential for burst firing of ventral tegmental area dopamine neurons. Proc Natl Acad Sci USA 2006; 103: 5167–5172.
  Article CAS Google Scholar
• Omelchenko N, Sesack SR . Ultrastructural analysis of local collaterals of rat ventral tegmental area neurons: GABA phenotype and synapses onto dopamine and GABA cells. Synapse 2009; 63: 895–906.
  Article CAS Google Scholar
• Hong S, Hikosaka O . The globus pallidus sends reward-related signals to the lateral habenula. Neuron 2008; 60: 720–729.
  Article CAS Google Scholar
• Lobb CJ, Wilson CJ, Paladini CA . A dynamic role for GABA receptors on the firing pattern of midbrain dopaminergic neurons. J Neurophysiol 2010; 104: 403–413.
  Article CAS Google Scholar
• Grace AA, Bunney BS . Opposing effects of striatonigral feedback pathways on midbrain dopamine cell activity. Brain Res 1985; 333: 271–284.
  Article CAS Google Scholar
• Oster MA, Faure P, Gutkin BS . Society for Neuroscience Annual Meeting. San Diego, CA, 2010.
  Google Scholar
• Graupner M, Gutkin BS . Society for Neuroscience Annual Meeting. Chicago, IL, 2009.
  Google Scholar
• Miwa JM, Freedman R, Lester HA . Neural systems governed by nicotinic acetylcholine receptors: emerging hypotheses. Neuron 2011; 70: 20–33.
  Article CAS Google Scholar
• Dalley JW, Everitt BJ, Robbins TW . Impulsivity, compulsivity, and top–down cognitive control. Neuron 2011; 69: 680–694.
  Article CAS Google Scholar