Blockade of muscarinic acetylcholine receptors in the ventral tegmental area prevents acquisition of food-rewarded operant responding in rats

Psychopharmacology

Volumn 186, Issue 1, 2006, Pages 113-121

  Sharf, Ruth ^a,b   McKelvey, Jennifer ^a   Ranaldi, Robert ^a  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Acetylcholine; Muscarinic; Nicotinic; Operant conditioning; Ventral tegmental area; VTA

Indexed keywords

MECAMYLAMINE; MUSCARINIC RECEPTOR; NICOTINIC RECEPTOR; SCOPOLAMINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; DRUG RECEPTOR BINDING; FEEDING BEHAVIOR; FEMALE; INSTRUMENTAL CONDITIONING; MALE; MICROINJECTION; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; RECEPTOR UPREGULATION; REWARD; TASK PERFORMANCE; VENTRAL TEGMENTUM;

ANIMALS; CONDITIONING, OPERANT; FOOD; MALE; MECAMYLAMINE; MUSCARINIC ANTAGONISTS; NICOTINIC ANTAGONISTS; RATS; RATS, LONG-EVANS; REWARD; SCOPOLAMINE; VENTRAL TEGMENTAL AREA;

EID: 33646347370     PISSN: 00333158     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00213-006-0352-0     Document Type: Article

References (61)

1. Aberman JE, Ward SJ, Salamone JD (1998) Effects of dopamine antagonists and accumbens dopamine depletions on time-constrained progressive-ratio performance. Pharmacol Biochem Behav 61:341-348
2. Baldwin AE, Sadeghian K, Kelley AE (2002) Appetitive instrumental learning requires coincident activation of NMDA and dopamine D1 receptors within the medial prefrontal cortex. J Neurosci 22:1063-1071
3. Bechara A, van der Kooy D (1989) The tegmental pedunculopontine nucleus: a brain-stem output of the limbic system critical for the conditioned place preferences produced by morphine and amphetamine. J Neurosci 9:3400-3409
4. Bechara A, van der Kooy D (1992) A single brainstem substrate mediates the motivational effects of both opiates and food in non-deprived rats but not in deprived rats. Behav Neuro 106:351-363
5. Bechara A, Harrington F, Nader K, van der Kooy D (1992) Neurobiology of motivation: double dissociation of two motivational mechanisms mediating opiate reward in drug-naïve versus drug-dependent animals. Behav Neurosci 106:798-807
6. Beninger RJ, Ranaldi R (1993) Microinjections of flupenthixol into the caudate-putamen but not the nucleus accumbens, amygdala or frontal cortex of rats produce intra-session declines in food-rewarded operant responding. Behav Brain Res 55:203-212
7. Beninger RJ, D'Amico CM, Ranaldi R (1993) Microinjections of flupenthixol into the caudate putamen of rats produce intrasession declines in food-rewarded operant responding. Pharmacol Biochem Behav 45:343-350
8. Berridge KC (1995) Food reward: brain substrates of wanting and liking. Neurosci Biobehav Rev 20:1-25
9. Berridge KC, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28:309-369
10. Blackburn JR, Phillips AG (1989) Dopamine and preparatory behavior: II. a neurochemical analysis. Behav Neurosci 103:15-23
11. Blaha CD, Allen LF, Das S, Inglis WL, Latimer MP, Vincent SR, Winn P (1996) Modulation of dopamine efflux in the nucleus accumbens after cholinergic stimulation of the ventral tegmental area in intact, pedunculopontine tegmental nucleus-lesioned, and laterodorsal tegmental nucleus-lesioned rats. J Neurosci 16:714-722
12. Bonci A, Malenka RC (1999) Properties and plasticity of excitatory synapses on dopaminergic and GABAergic cells in the ventral tegmental area. J Neurosci 19:3723-3730
13. Bradberry CW, Roth RH (1989) Cocaine increases extracellular dopamine in rat nucleus accumbens and ventral tegmental area as shown by in vivo microdialysis. Neurosci Lett 103:97-102
14. Charara A, Smith Y, Parent A (1996) Glutamatergic inputs from the pedunculopontine nucleus to midbrain dopaminergic neurons in primates: Phaseolus vulgaris-leucoagglutinin anterograde labeling combined with postembedding glutamate and GABA immunohistochemistry. J Comp Neurol 364:254-266
15. Chen NH, Reith ME (1994) Effects of locally applied cocaine, lidocaine, and various uptake blockers on monoamine transmission in the ventral tegmental area of freely moving rats: a microdialysis study on monoamine interrelationships. J Neurochem 63:1701-1713
16. Clarke PB, Pert A (1985) Autoradiographic evidence for nicotine receptors on nigrostriatal and mesolimbic dopaminergic neurons. Brain Res 348(2):355-358
17. Gratton A, Wise RA (1994) Drug- and behavior-associated changes in dopamine-related electrochemical signals during intravenous cocaine self-administration in rats. J Neurosci 14:4130-4146
18. Gronier B, Rasmussen K (1998) Activation of midbrain presumed dopaminergic neurones by muscarinic cholinergic receptors: an in vivo electrophysiological study in the rat. Br J Pharmacol 124:455-465
19. Harris GC, Wimmer M, Byrne R, Aston-Jones G (2004) Glutamate-associated plasticity in the ventral tegmental area is necessary for conditioning environmental stimuli with morphine. Neurosci 129:841-847
20. Hernandez L, Hoebel BG (1988) Food reward and cocaine increase extracellular dopamine in the nucleus accumbens as measured by microdialysis. Life Sci 42:1705-1712
21. Hopkins DA, Holstege G (1978) Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat. Exp Brain Res 32(4):529-547
22. Ikemoto K, Satoh K, Kitahama K, Geffard M, Maeda T (1996) Electron-microscopic study of dopaminergic structures in the medial subdivision of the monkey nucleus accumbens. Exp Brain Res 111:41-50
23. Ikemoto S, Panksepp J (1999) The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretations with special reference to reward-seeking. Brain Res Brain Res Rev 31:6-41
24. Kiyatkin EA, Gratton A (1994) Electrochemical monitoring of extracellular dopamine in nucleus accumbens of rats lever-pressing for food. Brain Res 652:225-234
25. Kofman O, Yeomans JS (1988) Cholinergic antagonists in ventral tegmentum elevate thresholds for lateral hypothalamic and brainstem self-stimulation. Pharmacol Biochem Behav 31:547-559
26. Kurumiya S, Nakajima S (1988) Dopamine D1 receptors in the nucleus accumbens: involvement in the reinforcing effect of tegmental stimulation. Brain Res 448:1-6
27. Lacey MG, Calabresi P, North RA (1990) Muscarine depolarizes rat substantia nigra zona compacta and ventral tegmental neurons in vitro through M1-like receptors. J Pharmacol Exp Ther 253:395-400
28. Lepore M, Franklin KB (1996) N-methyl-D-aspartate lesions of the pedunculopontine nucleus block acquisition and impair maintenance of responding reinforced with brain stimulation. Neurosci 71(1):147-155
29. McGregor A, Roberts DCS (1993) Dopaminergic antagonism within the nucleus accumbens or the amygdala produces differential effects on intravenous cocaine self-administration under fixed and progressive ratio schedules of reinforcement. Brain Res 624:245-252
30. Nader K, Bechara A, Roberts DCS, van der Kooy D (1994) Neuroleptics block high - but not low - dose heroin place preferences: further evidence for a two-system model of motivation. Behav Neurosci 108:1128-1138
31. Nisell M, Nomikos GG, Svensson TH (1994) Infusion of nicotine in the ventral tegmental area or the nucleus accumbens of the rat differentially affects accumbal dopamine release. Pharmacol Toxicol 75:348-352
32. 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
33. Olmstead MC, Franklin KBJ (1993) Effects of pedunculopontine tegmental nucleus lesions on morphine-induced conditioned place preference and analgesia in the formalin test. Neurosci 57:411-418
34. Olmstead MC, Franklin KBJ (1994) Lesions of the pedunculopontine tegmental nucleus block drug-induced reinforcement but not amphetamine-induced locomotion. Brain Res 638:29-35
35. Omelchenko N, Sesack SR (2005) Laterodorsal tegmental projections to identified cell populations in the rat ventral tegmental area. J Comp Neurol 483:217-235
36. Overton PG, Richards CD, Berry MS, Clark D (1999) Long-term potentiation at excitatory amino acid synapses on midbrain dopamine neurons. Neuroreport 10:221-226
37. Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. 2nd edn. Academic, New York
38. Pettit HO, Justice JB Jr (1989) Dopamine in the nucleus accumbens during cocaine self-administration as studied by in vivo microdialysis. Pharmacol Biochem Behav 34:899-904
39. Phillipson OT (1979) Afferent projections to the ventral tegmental area of Tsai and interfascicular nucleus: a horseradish peroxidase study in the rat. J Comp Neurol 187(1):117-143
40. Pratt WE, Kelley AE (2004) Nucleus accumbens acetylcholine regulates appetitive learning and motivation for food via activation of muscarinic receptors. Behav Neurosci 118:730-739
41. Quinlan MG, Sharf R, Lee DY, Wise RA, Ranaldi R (2004) Blockade of substantia nigra dopamine D1 receptors reduces intravenous cocaine reward in rats. Psychopharmacology 175:53-59
42. Rada PV, Mark GP, Yeomans JS, Hoebel BG (2000) Acetylcholine release in ventral tegmental area by hypothalamic self-stimulation, eating, and drinking. Pharmacol Biochem Behav 65:375-379
43. Ranaldi R, Wise RA (2001) Blockade of D1 dopamine receptors in the ventral tegmental area decreases cocaine reward: possible role for dendritically released dopamine. J Neurosci 21:5841-5846
44. Ranaldi R, Pocock D, Zereik R, Wise RA (1999) Dopamine fluctuations in the nucleus accumbens during maintenance, extinction, and reinstatement of intravenous D-amphetamine self-administration. J Neurosci 19:4102-4109
45. Redgrave P, Horrell RI (1976) Potentiation of central reward by localised perfusion of acetylcholine and 5-hydroxytryptamine. Nature 262:305-307
46. Richardson NR, Gratton A (1996) Behavior-relevant changes in nucleus accumbens dopamine transmission elicited by food reinforcement: an electrochemical study in rat. J Neurosci 16:8160-8169
47. Schultz W (1997) A neural substrate of prediction and reward. Science 275:1593-1599
48. 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
49. Sharf R, Ranaldi R (2006) Blockade of muscarinic acetylcholine receptors in the ventral tegmental area disrupts food-related learning in rats. Psychopharmacology 184(1):87-94
50. Sharf R, Lee DY, Ranaldi R (2005) Microinjections of SCH 23390 in the ventral tegmental area reduce operant responding under a progressive ratio schedule of food reinforcement in rats. Brain Res 1033:179-185
51. Smith Y, Bolam JP (1991) Convergence of synaptic inputs from the striatum and the globus pallidus onto identified nigrocollicular cells in the rat: a double anterograde labelling study. Neurosci 44:45-73
52. Smith-Roe SL, Kelley AE (2000) Coincident activation of NMDA and dopamine D1 receptors within the nucleus accumbens core is required for appetitive instrumental learning. J Neurosci 20:7737-7742
53. Smith Y, Charara A, Parent A (1996) Synaptic innervation of midbrain dopaminergic neurons by glutamate-enriched terminals in the squirrel monkey. J Comp Neurol 364:231-253
54. Stewart J (1984) Reinstatement of heroin and cocaine self-administration behavior in the rat by intracerebral application of morphine in the ventral tegmental area. Pharmacol Biochem Behav 20:917-923
55. Wise RA (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5:483-494
56. Wise RA, Bozarth MA (1987) A psychomotor stimulant theory of addiction. Psychol Rev 94:469-492
57. Wise RA, Hoffman DC (1992) Localization of drug reward mechanisms by intracranial injections. Synapse 10:247-263
58. Wise RA, Rompré P-P (1989) Brain dopamine and reward. Annu Rev Psychol 40:191-225
59. Yeomans J, Baptista M (1997) Both nicotinic and muscarinic receptors in ventral tegmental area contribute to brain-stimulation reward. Pharmacol Biochem Behav 57:915-921
60. Yeomans JS, Kofman O, McFarlane V (1985) Cholinergic involvement in lateral hypothalamic rewarding brain stimulation. Brain Res 329:19-26
61. Yeomans JS, Mathur A, Tampakeras M (1993) Rewarding brain stimulation: role of tegmental cholinergic neurons that activate dopamine neurons. Behav Neurosci 107:1077