Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 18, 2009, Pages 7281-7288

  Zweifel, Larry S ^a,b   Parker, Jones G ^a,b   Lobb, Collin J ^a   Rainwater, Aundrea ^a,b   Wall, Valeriez ^a,b   Fadok, Jonathan P ^a,b   Darvas, Martin ^a,b   Kim, Min J ^a   Mizumori, Sheri J Y ^a   Paladini, Carlos A ^a   Phillips, Paul E M ^a   Palmiter, Richard D ^a,b  

^a Department of Biochemistry ^*  (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Cue dependent learning; Electrophysiology cyclic voltammetry; Mouse behavior

Indexed keywords

DOPAMINE; IONOTROPIC RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NR1 NMDA RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; ASSOCIATION; BEHAVIOR; CELL ACTIVITY; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; FEMALE; GENE INACTIVATION; LEARNING; MALE; MOLECULAR DYNAMICS; MOUSE; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; SYNAPTIC POTENTIAL; ANIMAL; ATTENTION; CYTOLOGY; DRINKING; FEAR; GENETICS; MAZE TEST; MESENCEPHALON; METABOLISM; MOUSE MUTANT; NERVE CELL; PHYSIOLOGY; REWARD;

ANIMALS; ATTENTION; BEHAVIOR; DOPAMINE; DRINKING; FEAR; LEARNING; MAZE LEARNING; MESENCEPHALON; MICE; MICE, KNOCKOUT; NEURONS; RECEPTORS, N-METHYL-D-ASPARTATE; REWARD;

EID: 66149139444     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0813415106     Document Type: Article

References (54)

1. Goto Y, Grace AA (2005) Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nat Neurosci 8:805-812.
2. Grace AA, et al. (2007) Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci 30:220-227.
3. Frank MJ (2005) Dynamic dopamine modulation in the basal ganglia: A neurocompu- tational account of cognitive deficits in medicated and nonmedicated Parkinsonism. J Cogn Neurosci 17:51-72.
4. Wang M, Vijayraghavan S, Goldman-Rakic PS (2004) Selective D2 receptor actions on the functional circuitry of working memory. Science 303:853-856.
5. Shen W, et al. (2008) Dichotomous dopaminergic control of striatal synaptic plasticity Science 321:848-851.
6. Bayer HM, Lau B, Glimcher PW (2007), Statistics of midbrain dopamine neuron spike trains in the awake primate. J Neurophysiol 98:1428-1439.
7. Roitman MF, et al. (2004) Dopamine operates as a subsecond modulator of food seeking. J Neurosci 24:1265-1271.
8. Schultz W, Apicella P, Ljungberg T (1993) Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J Neurosci 13:900-913.
9. Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1-27.
10. Wise RA(2006) Role of brain dopamine in food reward and reinforcement. Philos Trans R Soc Lond B Biol Sci 361:1149 -1158.
11. Lisman JE. Grace AA (2005) The hippocampal-VTA loop: Controlling the entry of information into long-term memory. Neuron 46:703-713.
12. Cagniard B, et al. (2006) Mice with chronically elevated dopamine exhibit enhanced motivation, butnotlearning, for a food reward. Neuropsychopharmacology31:1362-1370.
13. Cagniard B, etal. (2006) Dopamine scales performance in the absence of new learning. Neuron 51:541-547.
14. Hnasko TS, Sotak BN, PalmiterRD (2005) Morphine reward in dopamine-deficient mice. Nature 438:854-857.
15. Hnasko TS, Sotak BN, Palmiter RD (2007) Cocaine-conditioned place preference by dopamine-deficient mice is mediated by serotonin. J Neurosci 27:12484-12488.
16. Robinson S, et al. (2004) Distinguishing whether dopamine regulates liking, wanting, and/or learning about rewards. Behav Neurosci 119:5-15.
17. Berridge KC (2007) The debate over dopamine's role in reward: The case for incentive salience. Psychopharmacology 191:391-431.
18. Komendantov AO, et al. (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. JNeurophysiol 91:346-357.
19. Overton P, Clark D (1992) Iontophoreticallyadministered drugsacting atthe N-methyl- D-aspartate receptor modulate burst firing in A9 dopamine neurons in the rat. Synapse 10:131-140.
20. Overton PG, Clark D (1997) Burst firing in midbrain dopaminergic neurons. Brain Res Brain Res Rev 25:312-334.
21. Engblom D, et al. (2008) Glutamate receptors on dopamine neurons control the persistence of cocaine seeking. Neuron 59:497-508.
22. Zweifel LS, et al. (2008) Role of NMDA receptors in dopamine neurons for plasticity and addictive behaviors. Neuron 59:486-496.
23. Lammel S, et al. (2008) Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 57:760-773.
24. Margolis EB, etal. (2006) The ventral tegmental area revisited: Is there an electrophysiological marker for dopaminergic neurons? J Physiol 577:907-924.
25. Robinson S, et al. (2004) Firing properties of dopamine neurons in freely moving dopamine-deficient mice: Effects of dopamine receptor activation and anesthesia. Proc Natl Acad Sci USA 101:13329-13334.
26. Grace AA, Bunney BS (1984) The control of firing pattern in nigral dopamine neurons: Burst firing. J Neurosci 4:2877-2890.
27. Pan WX, Hyland BI (2005) Pedunculopontine tegmental nucleus controls conditioned responses of midbrain dopamine neurons in behaving rats. JNeurosci 25:4725-4732.
28. Floresco SB, et al. Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat Neurosci 6:968-973.
29. Lokwan SJ, et al. (1999) Stimulation of the pedunculopontine tegmental nucleus in the rat produces burst firing in A9 dopaminergic neurons. Neuroscience 92:245-254.
30. Phillips PE, et al. (2003) Real-time measurements of phasic changes in extracellular dopamine concentration in freely moving rats by fast-scan cyclic voltammetry. Methods Mol Med 79:443-464.
31. Palmiter RD (2007) Is dopamine a physiologically relevantmediator of feeding behavior? Trends Neurosci 30:375-381.
32. Denenberg VH, Kim DS, Palmiter RD (2004) The role of dopamine in learning, memory, and performance of a water escape task. Behav Brain Res 148:73-78.
33. Zhou QY, Palmiter RD (1995) Dopamine-deficient mice are severely hypoactive, adipsic,and aphagic. Cell 83:1197-1209.
34. Sawa A, Snyder SH (2002) Schizophrenia: Diverse approaches to a complex disease.Science 296:692-695.
35. Krishnan V, etal. (2007) Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131:391-404.
36. Ralph RJ, et al. (2001) Prepulse inhibition deficits and perseverative motor patterns in dopamine transporter knock-out mice: Differential effects of D1 and D2 receptor antagonists. JNeurosci 21:305-313.
37. El-Ghundi M, et al. (1999) Spatial learning deficit in dopamine D(1) receptor knockout mice. Eur JPharmacol 383:95-106.
38. Morris RG, et al. (2003) Elements of a neurobiological theory of the hippocampus: The role of activity-dependent synaptic plasticity in memory. Philos Trans R Soc London B Biol Sci 358:773-786.
39. Robinson S, et al. (2007) Viral restoration of dopamine signaling to the dorsal striatum restores instrumental conditioning to dopamine-deficient mice. Psychopharmacology 191:567-578.
40. Mirenowicz J, Schultz W (1996) Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 379:449-451.
41. Guarraci FA, Kapp BS (1999) An electrophysiological characterization of ventral teg- mental area dopaminergic neurons during differential pavlovian fear conditioning in the awake rabbit. Behav Brain Res 99:169-179.
42. Trulson ME, Preussler DW (1984) Dopamine-containing ventral tegmental area neurons in freely moving cats: Activity during the sleep-waking cycle and effects of stress.Exp Neurol 83:367-377.
43. UnglessMA, Magill PJ, Bolam JP (2004) Uniform inhibition ofdopamine neuronsin the ventral tegmental area by aversive stimuli. Science 303:2040-2042.
44. Koch M (1999) The neurobiology of startle. Prog Neurobiol 59:107-128.
45. Chen BT, et al. (2005) Cocaine but not natural reward self-administration nor passive cocaine infusion produces persistent LTP in the VTA. Neuron 59:288-297.
46. Stuber GD, et al. (2008) Reward-Predictive Cues Enhance Excitatory Synaptic Strength onto Midbrain Dopamine Neurons. Science 321:1690-1692.
47. Saal D, et al. (2003) Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37:577-582.
48. Dan Y, Poo MM (2006) Spike timing-dependentplasticity: From synapse to perception. Physiol Rev 86:1033-1048.
49. Palmiter RD (2008) Dopamine signaling in the dorsal striatum is essential for motivated behaviors: Lessons from dopamine-deficient mice. Ann NY Acad Sci 1129:35-46.
50. Krahe R, Gabbiani F (2004) Burst firing in sensory systems. Nat Rev Neurosci 5:13-23.
51. Choi WY, Balsam PD, Horvitz JC (2005) Extended habit training reduces dopamine mediation of appetitive response expression. JNeurosci 25:6729-6733.
52. Horvitz JC, et al. (2007) A ''good parent'' function of dopamine: Transient modulation of learning and performance during early stages of training. Ann NY Acad Sci 1104:270-288.
53. Salamone JD, et al. (2003) Nucleus accumbens dopamine and the regulation of effort in food-seeking behavior: Implications for studies of natural motivation, psychiatry, and drug abuse. JPharmacol Exp Ther 305:1-8.
54. Paxinos G, Franklin K (2001) The Mouse Brain in Stereotaxic Coordinates (Academic, New York), 2nd Ed.