Dopamine excites nucleus accumbens neurons through the differential modulation of glutamate and GABA release

Journal of Neuroscience

Volumn 24, Issue 39, 2004, Pages 8621-8628

  Hjelmstad, Gregory O ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NONE   (United States)

Author keywords

Accumbens; Burst; Calcium; Depression; Dopamine; Presynaptic

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; 8 CHLORO 2,3,4,5 TETRAHYDRO 3 METHYL 5 PHENYL 1H 3 BENZAZEPIN 7 OL HYDROGEN MALEATE; CALCIUM CHANNEL BLOCKING AGENT; DOPAMINE; GLUTAMATE RECEPTOR ANTAGONIST; GLUTAMIC ACID; PICROTOXIN; SULPIRIDE;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC ACTIVITY; DRUG EFFECT; DRUG INHIBITION; EXCITATORY POSTSYNAPTIC POTENTIAL; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; NUCLEUS ACCUMBENS; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; STIMULUS RESPONSE; SYNAPTIC INHIBITION;

(R)-2,3,4,5-TETRAHYDRO-8-CHLORO-3-METHYL-5-PHENYL-1H-3-BENZAZEPIN-7-OL; ACTION POTENTIALS; ANIMALS; CALCIUM; DOPAMINE; DOPAMINE ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; MALE; MODELS, NEUROLOGICAL; NEURAL INHIBITION; NEURONS; NUCLEUS ACCUMBENS; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; SULPIRIDE; SYNAPSES;

EID: 4744360958     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3280-04.2004     Document Type: Article

References (47)

1. Bamford NS, Zhang H, Schmitz Y, Wu NP, Cepeda C, Levine MS, Schmauss C, Zakharenko SS, Zablow L, Sulzer D (2004) Heterosynaptic dopamine neurotransmission selects sets of corticostriatal terminals. Neuron 42:653-663.
2. Cador M, Robbins TW, Everitt BJ (1989) Involvement of the amygdala in stimulus-reward associations: interaction with the ventral striatum. Neuroscience 30:77-86.
3. Chang HT, Kitai ST (1985) Projection neurons of the nucleus accumbens: an intracellular labeling study. Brain Res 347:112-116.
4. Cooper DC (2002) The significance of action potential bursting in the brain reward circuit. Neurochem Int 41:333-340.
5. Di Ciano P, Cardinal RN, Cowell RA, Little SJ, Everitt BJ (2001) Differential involvement of NMDA, AMPA/kainate, and dopamine receptors in the nucleus accumbens core in the acquisition and performance of Pavlovian approach behavior. J Neurosci 21:9471-9477.
6. Dittman JS, Regehr WG (1998) Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci 18:6147-6162.
7. Dittman JS, Kreitzer AC, Regehr WG (2000) Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J Neurosci 20:1374-1385.
8. Ghitza UE, Fabbricatore AT, Prokopenko V, Pawlak AP, West MO (2003) Persistent cue-evoked activity of accumbens neurons after prolonged abstinence from self-administered cocaine. J Neurosci 23:7239-7245.
9. Hefft S, Kraushaar U, Geiger JR, Jonas P (2002) Presynaptic short-term depression is maintained during regulation of transmitter release at a GABAergic synapse in rat hippocampus. J Physiol (Lond) 539:201-208.
10. 2 receptors increases spike firing of nucleus accumbens neurons via G-protein βγ subunits. J Neurosci 23:5079-5087.
11. Hutcheson DM, Parkinson JA, Robbins TW, Everitt BJ (2001) The effects of nucleus accumbens core and shell lesions on intravenous heroin self-administration and the acquisition of drug-seeking behaviour under a second-order schedule of heroin reinforcement. Psychopharmacology (Berl) 153:464-472.
12. Jung MW, Qin Y, McNaughton BL, Barnes CA (1998) Firing characteristics of deep layer neurons in prefrontal cortex in rats performing spatial working memory tasks. Cereb Cortex 8:437-450.
13. Kawaguchi Y, Wilson CJ, Augood SJ, Emson PC (1995) Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 18:527-535.
14. Kelley AE, Smith-Roe SL, Holahan MR (1997) Response-reinforcement learning is dependent on N-methyl-D-aspartate receptor activation in the nucleus accumbens core. Proc Natl Acad Sci USA 94:12174-12179.
15. Kim J, Alger BE (2001) Random response fluctuations lead to spurious paired-pulse facilitation. J Neurosci 21:9608-9618.
16. Koos T, Tepper JM (1999) Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 2:467-472.
17. Li Y, Kauer JA (2004) Repeated exposure to amphetamine disrupts dopaminergic modulation of excitatory synaptic plasticity and neurotransmission in nucleus accumbens. Synapse 51:1-10.
18. Markram H, Pikus D, Gupta A, Tsodyks M (1998) Potential for multiple mechanisms, phenomena and algorithms for synaptic plasticity at single synapses. Neuropharmacology 37:489-500.
19. McClure SM, Daw ND, Montague PR (2003) A computational substrate for incentive salience. Trends Neurosci 26:423-428.
20. Nicola SM, Malenka RC (1997) Dopamine depresses excitatory and inhibitory synaptic transmission by distinct mechanisms in the nucleus accumbens. J Neurosci 17:5697-5710.
21. Nicola SM, Malenka RC (1998) Modulation of synaptic transmission by dopamine and norepinephrine in ventral but not dorsal striatum. J Neurophysiol 79:1768-1776.
22. Nicola SM, Surmeier J, Malenka RC (2000) Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbens. Annu Rev Neurosci 23:185-215.
23. Nicola SM, Yun IA, Wakabayashi KT, Fields HL (2004a) Cue-evoked firing of nucleus accumbens neurons encodes motivational significance during a discriminative stimulus task. J Neurophysiol 91:1840-1865.
24. Nicola SM, Hopf FW, Hjelmstad GO (2004b) Contrast enhancement: a physiological effect of striatal dopamine? Cell Tissue Res, in press.
25. Parkinson JA, Olmstead MC, Burns LH, Robbins TW, Everitt BJ (1999) Dissociation in effects of lesions of the nucleus accumbens core and shell on appetitive pavlovian approach behavior and the potentiation of conditioned reinforcement and locomotor activity by D-amphetamine. J Neurosci 19:2401-2411.
26. Parkinson JA, Willoughby PJ, Robbins TW, Everitt BJ (2000) Disconnection of the anterior cingulate cortex and nucleus accumbens core impairs Pavlovian approach behavior: further evidence for limbic cortical-ventral striatopallidal systems. Behav Neurosci 114:42-63.
27. Parkinson JA, Dalley JW, Cardinal RN, Bamford A, Fehnert B, Lachenal G, Rudarakanchana N, Halkerston KM, Robbins TW, Everitt BJ (2002) Nucleus accumbens dopamine depletion impairs both acquisition and performance of appetitive Pavlovian approach behaviour: implications for mesoaccumbens dopamine function. Behav Brain Res 137:149-163.
28. Pennartz CM, Kitai ST (1991) Hippocampal inputs to identified neurons in an in vitro slice preparation of the rat nucleus accumbens: evidence for feed-forward inhibition. J Neurosci 11:2838-2847.
29. Pennartz CM, Dolleman-Van der Weel MJ, Kitai ST, Lopes da Silva FH (1992) Presynaptic dopamine D1 receptors attenuate excitatory and inhibitory limbic inputs to the shell region of the rat nucleus accumbens studied in vitro. J Neurophysiol 67:1325-1334.
30. Pennartz CM, Ameerun RF, Groenewegen HJ, Lopes da Silva FH (1993) Synaptic plasticity in an in vitro slice preparation of the rat nucleus accumbens. Eur J Neurosci 5:107-117.
31. Pennartz CM, Groenewegen HJ, Lopes da Silva FH (1994) The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Prog Neurobiol 42:719-761.
32. Roitman MF, Stuber GD, Phillips PE, Wightman RM, Carelli RM (2004) Dopamine operates as a subsecond modulator of food seeking. J Neurosci 24:1265-1271.
33. Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1-27.
34. Schultz W (2002) Getting formal with dopamine and reward. Neuron 36:241-263.
35. Schultz W, Tremblay L, Hollerman JR (2000) Reward processing in primate orbitofrontal cortex and basal ganglia. Cereb Cortex 10:272-284.
36. Selig DK, Nicoll RA, Malenka RC (1999) Hippocampal long-term potentiation preserves the fidelity of postsynaptic responses to presynaptic bursts. J Neurosci 19:1236-1246.
37. 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.
38. Smith-Roe SL, Kelley AE (2000) Coincident activation of NMDA and dopamine D, receptors within the nucleus accumbens core is required for appetitive instrumental learning. J Neurosci 20:7737-7742.
39. Stevens CF, Wesseling JF (1998) Activity-dependent modulation of the rate at which synaptic vesicles become available to undergo exocytosis. Neuron 21:415-424.
40. Taverna S, Van Dongen YC, Groenewegen HJ, Pennartz CM (2004) Direct physiological evidence for synaptic connectivity between medium-sized spiny neurons in rat nucleus accumbens in situ. J Neurophysiol 91:1111-1121.
41. Thomas MJ, Malenka RC, Bond A (2000) Modulation of long-term depression by dopamine in the mesolimbic system. J Neurosci 20:5581-5586.
42. Tsodyks MV, Markram H (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci USA 94:719-723.
43. Uchimura N, Cherubini E, North RA (1989) Inward rectification in rat nucleus accumbens neurons. J Neurophysiol 62:1280-1286.
44. Wang LY, Kaczmarek LK (1998) High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394:384-388.
45. Wigstrom H, Gustafsson B (1983) Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition. Nature 301:603-604.
46. Yun IA, Wakabayashi KT, Fields HL, Nicola SM (2004) The ventral tegmental area is required for the behavioral and nucleus accumbens neuronal firing responses to incentive cues. J Neurosci 24:2923-2933.
47. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.