NMDA receptor antagonism in the ventral tegmental area impairs acquisition of reward-related learning

Behavioural Brain Research

Volumn 197, Issue 2, 2009, Pages 442-449

  Zellner, Margaret R ^a   Kest, Karen ^b   Ranaldi, Robert ^a,b  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

AP 5; Conditioning; Food; Glutamate; Motivation; Reward

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ANIMAL EXPERIMENT; APPETITE; ARTICLE; FEEDING BEHAVIOR; LEARNING DISORDER; MALE; MOTIVATION; MOTOR ACTIVITY; NONHUMAN; PRIORITY JOURNAL; RAT; REINFORCEMENT; REWARD; STIMULATION; VENTRAL TEGMENTUM;

2-AMINO-5-PHOSPHONOVALERATE; ANALYSIS OF VARIANCE; ANIMALS; ASSOCIATION LEARNING; CHOICE BEHAVIOR; CONDITIONING, OPERANT; EXCITATORY AMINO ACID ANTAGONISTS; FEEDING BEHAVIOR; MALE; RATS; RATS, LONG-EVANS; RECEPTORS, N-METHYL-D-ASPARTATE; REINFORCEMENT SCHEDULE; REWARD; VENTRAL TEGMENTAL AREA;

EID: 58149333388     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2008.10.013     Document Type: Article

References (51)

1. Wise R.A., and Rompré P.-P. Brain dopamine and reward. Annu Rev Psychol 40 (1989) 191-225
2. Berridge K.C., and Robinson T.E. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?. Brain Res Rev 28 (1998) 309-369
3. Wise R.A. Dopamine, learning and motivation. Nat Rev Neurosci 5 (2004) 483-494
4. Schultz W. Responses of midbrain dopamine neurons to behavioral trigger stimuli in the monkey. J Neurophysiol 56 (1986) 1439-1461
5. Romo R., and Schultz W. Dopamine neurons of the monkey midbrain: contingencies of responses to active touch during self-initiated arm movements. J Neurophysiol 63 (1990) 592-606
6. Schultz W., Apicella P., and Ljungberg T. Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J Neurosci 13 (1993) 900-913
7. Mirenowicz J., and Schultz W. Importance of unpredictability for reward responses in primate dopamine neurons. J Neurophysiol 72 (1994) 1024-1027
8. Fiorillo C.D., Tobler P.N., and Schultz W. Discrete coding of reward probability and uncertainty by dopamine neurons. Science 299 (2003) 1856-1902
9. Satoh T., Nakai S., Sato T., and Kimura M. Correlated coding of motivation and outcome of decision by dopamine neurons. J Neurosci 23 (2003) 9913-9923
10. Stewart J. 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 (1984) 917-923
11. Ranaldi R., Pocock D., Zereik R., and Wise R.A. Dopamine fluctuations in the nucleus accumbens during maintenance, extinction, and reinstatement of intravenous d-amphetamine self-administration. J Neurosci 19 (1999) 4102-4109
12. Gratton A., and Wise R.A. Drug- and behavior-associated changes in dopamine-related electrochemical signals during intravenous cocaine self-administration in rats. J Neurosci 14 (1994) 4130-4146
13. Kiyatkin E.A., and Gratton A. Electrochemical monitoring of extracellular dopamine in nucleus accumbens of rats lever-pressing for food. Brain Res 652 (1994) 225-234
14. Richardson N.R., and Gratton A. Behavior-relevant changes in nucleus accumbens dopamine transmission elicited by food reinforcement: an electrochemical study in rat. J Neurosci 16 (1996) 8160-8169
15. Sesack S.R., and Pickel V.M. Prefrontal cortical efferents in the rat synapse on unlableled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J Comp Neurol 320 (1992) 145-160
16. Smith Y., Charara A., and Parent A. Synaptic innervation of midbrain dopaminergic neurons by glutamate-enriched terminals in the squirrel monkey. J Comp Neurol 364 (1996) 231-253
17. Harris G.C., Wimmer M., Byrne R., and Aston-Jones G. Glutamate-associated plasticity in the ventral tegmental area is necessary for conditioning environmental stimuli with morphine. Neuroscience 129 (2004) 841-847
18. Harris G.C., and Aston-Jones G. Critical role for ventral tegmental glutamate in preference for a cocaine-conditioned environment. Neuropsychopharmacology 28 (2003) 73-76
19. Martinez Jr. J.L., and Derrick B.E. Long-term potentiation and learning. Annu Rev Psychol 47 (1996) 173-203
20. Kandel E.R. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294 (2001) 1030-1038
21. Overton P.G., Richards C.D., Berry M.S., and Clark D. Long-term potentiation at excitatory amino acid synapses on midbrain dopamine neurons. Neuroreport 10 (1999) 221-226
22. Bonci A., and Malenka R.C. Properties and plasticity of excitatory synapses on dopaminergic and GABAergic cells in the ventral tegmental area. J Neurosci 19 (1999) 3723-3730
23. Muller D., Joly M., and Lynch G. Contributions of quisqualate and NMDA receptors to the induction and expression of LTP. Science 242 (1988) 1694-1697
24. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (1986), Academic, New York
25. Adams C.D. Variations in the sensitivity of instrumental responding to reinforcer devaluation. Q J Exp Psychol 34 (1982) 77-98
26. Dickinson A., Balleine B.W., Watt A., Gonzalez F., and Boakes R.A. Motivational control after extended instrumental training. Anim Learn Behav 23 (1995) 197-206
27. Beninger R.J. The role of dopamine in locomotor activity and learning. Brain Res Rev 6 (1983) 173-196
28. Kelley A.E. Ventral striatal control of appetitive motivation: role in ingestive behavior and reward-related learning. Neurosci Biobehav Rev 27 (2004) 765-776
29. Arbuthnott G.W., and Wickens J. Space, time and dopamine. Trends Neurosci 30 (2007) 62-69
30. Miller J.D., Sanghera M.K., and German D.C. Mesencephalic dopaminergic unit activity in the behaviorally conditioned rat. Life Science 29 (1981) 1255-1263
31. Kosobud A.E., Harris G.C., and Chapin J.K. Behavioral associations of neuronal activity in the ventral tegmental area of the rat. J Neurosci 14 (1994) 7117-7129
32. Hyland B.I., Reynolds J.N., Hay J., Perk C.G., and Miller R. Firing modes of midbrain dopamine cells in the freely moving rat. Neuroscience 114 (2002) 475-492
33. Pan W.X., Schmidt R., Wickens J.R., and Hyland B.I. Dopamine cells respond to predicted events during classical conditioning: evidence for eligibility traces in the reward-learning network. J Neurosci 25 (2005) 6235-6242
34. Bugelski R. Extinction with and without sub-goal reinforcement. J Comp Psychol 26 (1938) 121-133
35. Stein L. Secondary reinforcement established with subcortical stimulation. Science 127 (1958) 466-467
36. Wang T., O'Connor W.T., Ungerstedt U., and French E.D. N-methyl-d-aspartic acid biphasically regulates the biochemical and electrophysiological response of A10 dopamine neurons in the ventral tegmental area: in vivo microdialysis and in vitro electrophysiological studies. Brain Res 666 (1994) 255-262
37. Beninger R.J., D'Amico C.M., and Ranaldi R. Microinjections of flupenthixol into the caudate putamen of rats produce intrasession declines in food-rewarded operant responding. Pharmacol Biochem Behav 45 (1993) 343-350
38. Yun I.A., Nicola S.M., and Fields H.L. Contrasting effects of dopamine and glutamate receptor antagonist injection in the nucleus accumbens suggest a neural mechanism underlying cue-evoked goal-directed behavior. Eur J Neurosci 20 (2004) 249-263
39. Yun I.A., Wakabayashi K.T., Fields H.L., and Nicola S.M. The ventral tegmental area is required for the behavioral and nucleus accumbens neuronal firing responses to incentive cues. J Neurosci 24 (2004) 2923-2933
40. Nakajima S. Suppression of operant responding in the rat by dopamine D1 receptor blockade with SCH 23390. Physiol Psychol 14 (1986) 111-114
41. Smith-Roe S.L., and Kelley A.E. Coincident activation of NMDA and dopamine D1 receptors within the nucleus accumbens core is required for appetitive instrumental learning. J Neurosci 20 (2000) 7737-7742
42. Baldwin A.E., Sadeghian K., and Kelley A.E. Appetitive instrumental learning requires coincident activation of NMDA and dopamine D1 receptors within the medial prefrontal cortex. J Neurosci 22 (2002) 1063-1071
43. Cervo L., and Samanin R. Effects of dopaminergic and glutamatergic receptor antagonists on the acquisition and expression of cocaine conditioning place preference. Brain Res 673 (1995) 242-250
44. Kelley A.E., Smith-Roe S.L., and Holahan M.R. Response-reinforcement learning is dependent on N-methyl-d-aspartate receptor activation in the nucleus accumbens core. Proc Natl Acad Sci U S A 94 (1997) 12174-12179
45. Sharf R., McKelvey J., and Ranaldi R. Blockade of muscarinic acetylcholine receptors in the ventral tegmental area prevents acquisition of food-rewarded operant responding in rats. Psychopharmacology 186 (2006) 113-121
46. Sharf R., and Ranaldi R. Blockade of muscarinic acetylcholine receptors in the ventral tegmental area disrupts food-related learning in rats. Psychopharmacology 184 (2006) 87-94
47. Decker MW, McGaugh JL. The role of interactions between the cholinergic system and other neuromodulatory systems in learning and memory. Synapse 1991;7:151-68.
48. Beninger R.J., Wirsching B.A., Jhamandas K., and Boegman R.J. Animal studies of brain acetylcholine and memory. Arch Gerontol Geriatr Suppl. 1 (1989) 71-90
49. Boddeke H.W.G.M., and Boeijinga P.H. Muscarinic acetylcholine receptors and long-term potentiation of synaptic transmission. In: Stone T.W. (Ed). CNS neurotransmitters and modulators: acetylcholine (1995), CRC Press Inc., Boca Raton 171-183
50. Goldberg S.R. Comparable behavior maintained under fixed-ratio and second-order schedules of food presentation, cocaine injection or d-amphetamine injection in the squirrel monkey. J Pharmacol Exp Ther 186 (1973) 18-30
51. Kelleher R.T., and Goldberg S.R. Fixed-interval responding under second-order schedules of food presentation or cocaine injection. J Exp Anal Behav 28 (1977) 221-231