Endogenous Cholinergic Inputs and Local Circuit Mechanisms Govern the Phasic Mesolimbic Dopamine Response to Nicotine

PLoS Computational Biology

Volumn 9, Issue 8, 2013, Pages

  Graupner, Michael ^a,b   Maex, Reinoud ^a   Gutkin, Boris ^a,c  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b NEW YORK UNIVERSITY   (United States)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMINES; NEURONS; REINFORCEMENT; TIMING CIRCUITS;

ACETYLCHOLINE RECEPTOR; COMPUTATIONAL MODELLING; DISINHIBITION; DOPAMINE; GABAERGIC; IN-VITRO; IN-VIVO; NICOTINIC ACETYLCHOLINE; REINFORCING ACTION; VENTRAL TEGMENTAL AREAS;

NICOTINE;

ACETYLCHOLINE; ACETYLCHOLINESTERASE; DOPAMINE; NICOTINE; NICOTINIC RECEPTOR;

ARTICLE; CHOLINERGIC SYSTEM; DESENSITIZATION; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; ENZYME ACTIVITY; GABAERGIC SYSTEM; IN VITRO STUDY; IN VIVO STUDY; INTERNEURON; MESOLIMBIC DOPAMINERGIC SYSTEM; MOUSE; NONHUMAN; TOBACCO; VENTRAL TEGMENTUM;

EID: 84883332998     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003183     Document Type: Article

References (75)

1. Di Chiara G, (2000) Role of dopamine in the behavioural actions of nicotine related to addiction. Eur J Pharmacol 393: 295-314.
2. Nestler EJ, Aghajanian GK, (1997) Molecular and cellular basis of addiction. Science 278: 58-63.
3. Marti F, Arib O, Morel C, Dufresne V, Maskos U, et al. (2011) Smoke extracts and nicotine, but not tobacco extracts, potentiate firing and burst activity of ventral tegmental area dopaminergic neurons in mice. Neuropsychopharmacology 36: 2244-2257.
4. Pontieri FE, Tanda G, Orzi F, Di Chiara G, (1996) Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs. Nature 382: 255-257.
5. Di Chiara G, Imperato a, (1988) Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci U S A 85: 5274-5278.
6. Corrigall WA, Coen KM, Adamson KL, (1994) Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area. Brain Res 653: 278-284.
7. Changeux JP, Bertrand D, Corringer PJ, Dehaene S, Edelstein S, et al. (1998) Brain nicotinic receptors: structure and regulation, role in learning and reinforcement. Brain Res Brain Res Rev 26: 198-216.
8. Oakman SA, Faris PL, Kerr PE, Cozzari C, Hartman BK, (1995) Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J neurosci 15: 5859-5869.
9. Dani JA, Ji D, Zhou FM, (2001) Synaptic plasticity and nicotine addiction. Neuron 31: 349-352.
10. Giniatullin R, Nistri A, Yakel JL, (2005) Desensitization of nicotinic ACh receptors: shaping cholinergic signaling. Trends Neurosci 28: 371-378.
11. Henningfield JE, Stapleton JM, Benowitz NL, Grayson RF, London ED, (1993) Higher levels of nicotine in arterial than in venous blood after cigarette smoking. Drug Alcohol Depend 33: 23-29.
12. Pidoplichko VI, DeBiasi M, Williams JT, Dani JA, (1997) Nicotine activates and desensitizes midbrain dopamine neurons. Nature 390: 401-404.
13. Changeux JP, (2010) Nicotine addiction and nicotinic receptors: lessons from genetically modified mice. Nat Rev Neurosci 11: 389-401.
14. Taly A, Corringer PJ, Guedin D, Lestage P, Changeux JP, (2009) Nicotinic receptors: allosteric transitions and therapeutic targets in the nervous system. Nat Rev Drug Discov 8: 733-750.
15. Jones IW, Wonnacott S, (2004) Precise localization of (alpha)7 nicotinic acetylcholine receptors on glutamatergic axon terminals in the rat ventral tegmental area. J Neurosci 24: 11244-11252.
16. Picciotto MR, Zoli M, Rimondini R, Lena C, Marubio LM, et al. (1998) Acetylcholine receptors containing the (beta)2 subunit are involved in the reinforcing properties of nicotine. Nature 391: 173-177.
17. Mameli-Engvall M, Evrard A, Pons S, Maskos U, Svensson TH, et al. (2006) Hierarchical control of dopamine neuron-firing patterns by nicotinic receptors. Neuron 50: 911-921.
18. Mansvelder HD, Mcgehee DS, (2000) Long-Term Potentiation of Excitatory Inputs to Brain Reward Areas by Nicotine. Neuron 27: 349-357.
19. Mansvelder HD, Keath JR, Mcgehee DS, (2002) Synaptic Mechanisms Underlie Nicotine-Induced Excitability of Brain Reward Areas. Neuron 33: 905-919.
20. Tapper AR, McKinney SL, Nashmi R, Schwarz J, Deshpande P, et al. (2004) Nicotine activation of (alpha)4* receptors: sufficient for reward, tolerance, and sensitization. Science 306: 1029-1032.
21. Exley R, Maubourguet N, David V, Eddine R, Evrard A, et al. (2011) Distinct contributions of nicotinic acetylcholine receptor subunit (alpha)4 and subunit (alpha)6 to the reinforcing effects of nicotine. Proc Natl Acad Sci U S A 108: 7577-7582.
22. Katz B, Thesleff S, (1957) A study of the desensitization produced by acetylcholine at the motor end-plate. J Physiol 138: 63-80.
23. Shelley C, Cull-Candy SG, (2010) Desensitization and models of receptor-channel activation. J Physiol 588: 1395-1397.
24. Graupner M, Gutkin B, (2009) Modeling nicotinic neuromodulation from global functional and network levels to nAChR based mechanisms. Acta Pharmacol Sin 30: 681-693.
25. Fenster CP, Rains MF, Noerager B, Quick MW, Lester Ra, (1997) Influence of subunit composition on desensitization of neuronal acetylcholine receptors at low concentrations of nicotine. J Neurosci 17: 5747-5759.
26. Eaton JB, Peng J-H, Schroeder KM, George Aa, Fryer JD, et al. (2003) Characterization of human (alpha)4(beta)2-nicotinic acetylcholine receptors stably and heterologously expressed in native nicotinic receptor-null SH-EP1 human epithelial cells. Mol Pharmacol 64: 1283-1294.
27. Gerzanich V, Peng X, Wang F, Wells G, Anand R, et al. (1995) Comparative pharmacology of epibatidine: a potent agonist for neuronal nicotinic acetylcholine receptors. Mol Pharmacol 48: 774-782.
28. Buisson B, Bertrand D, (2001) Chronic exposure to nicotine upregulates the human (alpha)4(beta)2 nicotinic acetylcholine receptor function. J Neurosci 21: 1819-1829.
29. Papke RL, (2006) Estimation of both the potency and efficacy of (alpha)7 nAChR agonists from single-concentration responses. Life Sci 78: 2812-2819.
30. Peng X, Katz M, Gerzanich V, Anand R, Lindstrom J, (1994) Human (alpha)7 acetylcholine receptor: cloning of the (alpha)7 subunit from the SH-SY5Y cell line and determination of pharmacological properties of native receptors and functional (alpha)7 homomers expressed in Xenopus oocytes. Mol Pharmacol 45: 546-554.
31. Rose JE, Mukhin AG, Lokitz SJ, Turkington TG, Herskovic J, et al. (2010) Kinetics of brain nicotine accumulation in dependent and nondependent smokers assessed with PET and cigarettes containing 11C-nicotine. Proc Natl Acad Sci U S A 107: 5190-5195.
32. Paradiso KG, Steinbach JH, (2003) Nicotine is highly effective at producing desensitization of rat (alpha)4(beta)2 neuronal nicotinic receptors. J Physiol 553: 857-871.
33. Klink R, de Kerchove d'Exaerde A, Zoli M, Changeux JP, (2001) Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J Neurosci 21: 1452-1463.
34. Picciotto MR, Addy NA, Mineur YS, Brunzell DH, (2008) It is not "either/or": activation and desensitization of nicotinic acetylcholine receptors both contribute to behaviors related to nicotine addiction and mood. Prog Neurobiol 84: 329-342.
35. Garzón M, Vaughan Ra, Uhl GR, Kuhar MJ, Pickel VM, (1999) Cholinergic axon terminals in the ventral tegmental area target a subpopulation of neurons expressing low levels of the dopamine transporter. J Comp Neurol 410: 197-210.
36. Nashmi R, Xiao C, Deshpande P, McKinney S, Grady SR, et al. (2007) 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 27: 8202-8218.
37. Tolu S, Eddine R, Marti F, David V, Graupner M, et al. (2013) Co-activation of VTA DA and GABA neurons mediates nicotine reinforcement. Mol Psychiatry 18: 382-393.
38. Johnson SW, North RA, (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12: 483-488.
39. Lüscher C, Ungless MA, (2006) The mechanistic classification of addictive drugs. PLoS Med 3: e437.
40. Ikemoto S, Kohl RR, McBride WJ, (1997) GABA(A) receptor blockade in the anterior ventral tegmental area increases extracellular levels of dopamine in the nucleus accumbens of rats. J Neurochem 69: 137-143.
41. David V, Durkin TP, Cazala P, (1997) Self-administration of the GABAA antagonist bicuculline into the ventral tegmental area in mice: dependence on D2 dopaminergic mechanisms. Psychopharmacology (Berl) 130: 85-90.
42. Sher E, Chen Y, Sharples TJ, Broad LM, Benedetti G, et al. (2004) Physiological roles of neuronal nicotinic receptor subtypes: new insights on the nicotinic modulation of neurotransmitter release, synaptic transmission and plasticity. Curr Top Med Chem 4: 283-297.
43. Johnson SW, North RA, (1992) Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J Physiol 450: 455-468.
44. Lacey MG, Mercuri NB, North RA, (1989) Two cell types in rat substantia nigra zona compacta distinguished by membrane properties and the actions of dopamine and opioids. J Neurosci 9: 1233-1241.
45. Jhou TC, Fields HL, Baxter MG, Saper CB, Holland PC, (2009) The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses. Neuron 61: 786-800.
46. Kalivas PW, Churchill L, Klitenick MA, (1993) GABA and enkephalin projection from the nucleus accumbens and ventral pallidum to the ventral tegmental area. Neuroscience 57: 1047-1060.
47. Erhardt S, Schwieler L, Engberg G, (2002) Excitatory and inhibitory responses of dopamine neurons in the ventral tegmental area to nicotine. Synapse 43: 227-237.
48. Wooltorton JR, Pidoplichko VI, Broide RS, Dani JA, (2003) Differential desensitization and distribution of nicotinic acetylcholine receptor subtypes in midbrain dopamine areas. J Neurosci 23: 3176-3185.
49. Grenhoff J, Tung CS, Svensson TH, (1988) The excitatory amino acid antagonist kynurenate induces pacemaker-like firing of dopamine neurons in rat ventral tegmental area in vivo. Acta Physiol Scand 134: 567-568.
50. Chergui K, Charlety PJ, Akaoka H, Saunier CF, Brunet JL, et al. (1993) Tonic activation of NMDA receptors causes spontaneous burst discharge of rat midbrain dopamine neurons in vivo. Eur J Neurosci 5: 137-144.
51. Komendantov AO, Komendantova OG, Johnson SW, Canavier CC, (2004) A modeling study suggests complementary roles for GABAA and NMDA receptors and the SK channel in regulating the firing pattern in midbrain dopamine neurons. J Neurophysiol 91: 346-357.
52. Gao M, Jin Y, Yang K, Zhang D, Lukas RJ, et al. (2010) Mechanisms involved in systemic nicotine-induced glutamatergic synaptic plasticity on dopamine neurons in the ventral tegmental area. J Neurosci 30: 13814-13825.
53. Wu M, Hrycyshyn AW, Brudzynski SM, (1996) Subpallidal outputs to the nucleus accumbens and the ventral tegmental area: anatomical and electrophysiological studies. Brain Res 740: 151-161.
54. Carr DB, Sesack SR, (2000) Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J Neurosci 20: 3864-3873.
55. Fagen ZM, Mansvelder HD, Keath JR, McGehee DS, (2003) Short- and long-term modulation of synaptic inputs to brain reward areas by nicotine. Ann N Y Acad Sci 1003: 185-195.
56. Dayan P, Niv Y, (2008) Reinforcement learning: the good, the bad and the ugly. Curr Opin Neurobiol 18: 185-196.
57. Reynolds JN, Wickens JR, (2002) Dopamine-dependent plasticity of corticostriatal synapses. Neural Netw 15: 507-521.
58. Yu AJ, Dayan P, (2005) Uncertainty, neuromodulation, and attention. Neuron 46: 681-692.
59. Lichtenstein E, (1982) The smoking problem: a behavioral perspective. J Consult Clin Psychol 50: 804-819.
60. Di Chiara G, (1999) Drug addiction as dopamine-dependent associative learning disorder. Eur J Pharmacol 375: 13-30.
61. Wilson HR, Cowan JD, (1972) Excitatory and inhibitory interactions in localized populations of model neurons. Biophys J 12: 1-24.
62. Grace AA, Onn SP, (1989) Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J Neurosci 9: 3463-3481.
63. Champtiaux N, Gotti C, Cordero-Erausquin M, David DJ, Przybylski C, et al. (2003) Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice. J neurosci 23: 7820-7829.
64. Changeux JP, Devillers-Thiéry a, Chemouilli P, (1984) Acetylcholine receptor: an allosteric protein. Science 225: 1335-1345.
65. Dani Ja, Heinemann S, (1996) Molecular and cellular aspects of nicotine abuse. Neuron 16: 905-908.
66. Chavez-Noriega LE, Crona JH, Washburn MS, Urrutia A, Elliott KJ, et al. (1997) Pharmacological characterization of recombinant human neuronal nicotinic acetylcholine receptors h(alpha)2(beta)2, h(alpha)2(beta)4, h(alpha)3(beta)2, h(alpha)3(beta)4, h(alpha)4(beta)2, h(alpha)4(beta)4 and h(alpha)7 expressed in Xenopus oocytes. J Pharmacol Exp Ther 280: 346-356.
67. Grady SR, Drenan RM, Breining SR, Yohannes D, Wageman CR, et al. (2010) Structural differences determine the relative selectivity of nicotinic compounds for native (alpha)4(beta)2*-, (alpha)6(beta)2*-, (alpha)3(beta)4*- and (alpha)7-nicotine acetylcholine receptors. Neuropharmacology 58: 1054-1066.
68. Christie MJ, Bridge S, James LB, Beart PM, (1985) Excitotoxin lesions suggest an aspartatergic projection from rat medial prefrontal cortex to ventral tegmental area. Brain Res 333: 169-172.
69. Sesack SR, Pickel VM, (1992) Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J Comp Neurol 320: 145-160.
70. Tong ZY, Overton PG, Clark D, (1996) Stimulation of the prefrontal cortex in the rat induces patterns of activity in midbrain dopaminergic neurons which resemble natural burst events. Synapse 22: 195-208.
71. Steffensen SC, Svingos AL, Pickel VM, Henriksen SJ, (1998) Electrophysiological characterization of GABAergic neurons in the ventral tegmental area. J Neurosci 18: 8003-8015.
72. Clements JR, Grant S, (1990) Glutamate-like immunoreactivity in neurons of the laterodorsal tegmental and pedunculopontine nuclei in the rat. Neurosci Lett 120: 70-73.
73. Cornwall J, Cooper JD, Phillipson OT, (1990) Afferent and efferent connections of the laterodorsal tegmental nucleus in the rat. Brain Res Bull 25: 271-284.
74. Forster GL, Blaha CD, (2000) Laterodorsal tegmental stimulation elicits dopamine efflux in the rat nucleus accumbens by activation of acetylcholine and glutamate receptors in the ventral tegmental area. Eur J Neurosci 12: 3596-3604.
75. Gerzanich V, Anand R, Lindstrom J, (1994) Homomers of (alpha)8 and (alpha)7 subunits of nicotinic receptors exhibit similar channel but contrasting binding site properties. Mol Pharmacol 45: 212-220.