Dopamine Neurons Mediate a Fast Excitatory Signal via Their Glutamatergic Synapses

Journal of Neuroscience

Volumn 24, Issue 4, 2004, Pages 972-981

  Chuhma, Nao ^a,b   Zhang, Hui ^a   Masson, Justine ^a,b,d   Zhuang, Xiaoxi ^c   Sulzer, David ^a,b   Hen, René ^a   Rayport, Stephen ^a,b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d Lab Biol Physiopathol Cranio F   (France)

Author keywords

Accumbens; Addiction; Dopamine; Glutamate; Incentive salience; Schizophrenia; Slice; Ventral tegmental area; Yellow fluorescent protein

Indexed keywords

DOPAMINE 2 RECEPTOR STIMULATING AGENT; GLUTAMIC ACID; QUINPIROLE; YELLOW FLUORESCENT PROTEIN;

ADDICTION; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; FLUORESCENCE; MESENCEPHALON; MONOSYNAPTIC REFLEX; MOUSE; NERVE CELL STIMULATION; NERVE PROJECTION; NEUROTRANSMISSION; NONHUMAN; NUCLEUS ACCUMBENS; POLYSYNAPTIC REFLEX; PRIORITY JOURNAL; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; SYNAPSE; TRANSGENIC MOUSE; VENTRAL TEGMENTUM;

ANIMALS; BACTERIAL PROTEINS; DOPAMINE; DOPAMINE AGONISTS; FEMALE; GENES, REPORTER; GLUTAMIC ACID; HETEROZYGOTE; LUMINESCENT PROTEINS; MALE; MICE; MICE, TRANSGENIC; MOTIVATION; NEURAL INHIBITION; NEURONS; NUCLEUS ACCUMBENS; PATCH-CLAMP TECHNIQUES; RECEPTORS, DOPAMINE D2; SYNAPSES; SYNAPTIC TRANSMISSION; VENTRAL TEGMENTAL AREA;

EID: 0742287910     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4317-03.2004     Document Type: Article

References (54)

1. +-evoked dopamine release in the neostriatum. Brain Res Dev Brain Res 78:123-130.
2. Benoit-Marand M, Jaber M, Gonon F (2000) Release and elimination of dopamine in vivo in mice lacking the dopamine transporter: functional consequences. Eur J Neurosci 12:2985-2992.
3. Benoit-Marand M, Borrelli E, Gonon F (2001) Inhibition of dopamine release via presynaptic D2 receptors: time course and functional characteristics in vivo. J Neurosci 21:9134-9141.
4. Berg-Johnsen J, Langmoen IA (1992) Temperature sensitivity of thin unmyelinated fibers in rat hippocampal cortex. Brain Res 576:319-321.
5. Berry MS, Pentreath VW (1976) Criteria for distinguishing between monosynaptic and polysynaptic transmission. Brain Res 105:1-20.
6. Budygin EA, John CE, Mateo Y, Jones SR (2002) Lack of cocaine effect on dopamine clearance in the core and shell of the nucleus accumbens of dopamine transporter knock-out mice. J Neurosci 22:RC222(1-4).
7. Chang HT, Wilson CJ, Kitai ST (1981) Single neostriatal efferent axons in the globus pallidus: a light and electron microscopic study. Science 213:915-918.
8. Chuhma N, Zhang H, Sulzer D, Rayport S (2003) The intact mesoaccumbens dopamine projection in the brain slice: dopamine release and origin of the excitatory polysynaptic components. Soc Neurosci Abstr 29:461.20.
9. Coulter CL, Happe HK, Murrin LC (1996) Postnatal development of the dopamine transporter: a quantitative autoradiographic study. Brain Res Dev Brain Res 92:172-181.
10. Cragg SJ, Greenfield SA (1997) Differential autoreceptor control of somatodendritic and axon terminal dopamine release in substantia nigra, ventral tegmental area, and striatum. J Neurosci 17:5738-5746.
11. Fiorillo CD, Tobler PN, Schultz W (2003) Discrete coding of reward probability and uncertainty by dopamine neurons. Science 299:1898-1902.
12. Fremeau Jr RT, Burman J, Qureshi T, Tran CH, Proctor J, Johnson J, Zhang H, Sulzer D, Copenhagen DR, Storm-Mathisen J, Reimer RJ, Chaudhry FA, Edwards RH (2002) The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc Natl Acad Sci USA 99:14488-14493.
13. Giros B, Jaber M, Jones SR, Wightman RM, Caron MG (1996) Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 379:606-612.
14. Gonon F (1997) Prolonged and extrasynaptic excitatory action of dopamine mediated by D1 receptors in the rat striatum in vivo. J Neurosci 17:5972-5978.
15. Goto Y, O'Donnell P (2001) Network synchrony in the nucleus accumbens in vivo. J Neurosci 21:4498-4504.
16. Gras C, Herzog E, Bellenchi GC, Bernard V, Ravassard P, Pohl M, Gasnier B, Giros B, El Mestikawy S (2002) A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J Neurosci 22:5442-5451.
17. Ingham CA, Hood SH, Taggart P, Arbuthnott GW (1998) Plasticity of synapses in the rat neostriatum after unilateral lesion of the nigrostriatal dopaminergic pathway. J Neurosci 18:4732-4743.
18. Jones SR, Garris PA, Kilts CD, Wightman RM (1995) Comparison of dopamine uptake in the basolateral amygdaloid nucleus, caudate-putamen, and nucleus accumbens of the rat. J Neurochem 64:2581-2589.
19. Joyce MP, Rayport S (2000) Mesoaccumbens dopamine neuron synapses reconstructed in vitro are glutamatergic. Neuroscience 99:445-456.
20. Kandel ER, Frazier WT, Waziri R, Coggeshall RE (1967) Direct and common connections among identified neurons in Aplysia. J Neurophysiol 30:1352-1376.
21. Kaneko T (2000) Enzymes responsible for glutamate synthesis and degradation. In: Handbook of chemical neuroanatomy, Vol 18: glutamate (Ottersen OP, Storm-Mathisen J, eds), pp 203-230. Amsterdam: Elsevier.
22. Kaneko T, Akiyama H, Nagatsu I, Mizuno N (1990) Immunohistochemical demonstration of glutaminase in catecholaminergic and serotoninergic neurons of rat brain. Brain Res 507:151-154.
23. Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908-4923.
24. Lacey MG, Mercuri NB, North RA (1987) Dopamine acts on D2 receptors to increase potassium conductance in neurones of the rat substantia nigra zona compacta. J Physiol (Lond) 392:397-416.
25. Lavin A, Grace AA (2001) Stimulation of D1-type dopamine receptors enhances excitability in prefrontal cortical pyramidal neurons in a state-dependent manner. Neuroscience 104:335-346.
26. 3H] dihydrotetrabenazine. Neurosci Lett 117:1-7.
27. Meador-Woodruff JH, Mansour A, Bunzow JR, Van Tol HH, Watson Jr SJ, Civelli O (1989) Distribution of D2 dopamine receptor mRNA in rat brain. Proc Natl Acad Sci USA 86:7625-7628.
28. Mereu G, Costa E, Armstrong DM, Vicini S (1991) Glutamate receptor subtypes mediate excitatory synaptic currents of dopamine neurons in midbrain slices. J Neorosci 11:1359-1366.
29. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG (1998) Dopamine receptors: from structure to function. Physiol Rev 78:189-225.
30. Mogenson GJ, Yang CR, Yim CY (1988) Influence of dopamine on limbic inputs to the nucleus accumbens. Ann NY Acad Sci 537:86-100.
31. O'Donnell P (2003) Dopamine gating of forebrain neural ensembles. Eur J Neurosci 17:429-435.
32. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates, Ed 2. San Diego: Academic.
33. Phillips PE, Hancock PJ, Stamford JA (2002) Time window of autoreceptor-mediated inhibition of limbic and striatal dopamine release. Synapse 44:15-22.
34. Plaitakis A, Shashidharan P (2000) Glutamate transport and metabolism in dopaminergic neurons of substantia nigra: implications for the pathogenesis of Parkinson's disease. J Neurol 247 [Suppl 2]:II/25-II/35.
35. Plenz D, Kitai ST (1996) Organotypic cortex-striatum-mesencephalon cultures: the nigrostriatal pathway. Neurosci Lett 209:177-180.
36. Restani P, Corsini E, Galimberti P, Galli CL (1990) Postnatal ontogenesis of dopaminergic and serotoninergic systems in rat caudate nucleus. Pharmacol Res 22:343-350.
37. Rodriguez M, Gonzalez-Hernandez T (1999) Electrophysiological and morphological evidence for a GABAergic nigrostriatal pathway. J Neurosci 19:4682-4694.
38. Ryan LJ, Young SJ, Groves PM (1986) Substantia nigra stimulation evoked antidromic responses in rat neostriatum. Exp Brain Res 63:449-460.
39. Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1-27.
40. Seamans JK, Yang CR (2004) The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol, in press.
41. Sesack SR, Aoki C, Pickel VM (1994) Ultrastructural localization of D2 receptor-like immunoreactivity in midbrain dopamine neurons and their striatal targets. J Neurosci 14:88-106.
42. Siggins GR (1978) Electrophysiological role of dopamine in the striatum: excitatory or inhibitory? In: Psychopharmacology: a generation of progress (Lipton MA, DiMascio A, Killam KF, eds), pp 143-157. New York: Raven.
43. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, Costantini F (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1:4.
44. Steffensen SC, Svingos AL, Pickel VM, Henriksen SJ (1998) Electrophysiological characterization of GABAergic neurons in the ventral tegmental area. J Neurosci 18:8003-8015.
45. Sulzer D, Joyce MP, Lin L, Geldwert D, Haber SN, Hattori T, Rayport S (1998) Dopamine neurons make glutamatergic synapses in vitro. J Neurosci 18:4588-4602.
46. Tarazi FI, Baldessarini RJ (2000) Comparative postnatal development of dopamine D(1), D(2) and D(4) receptors in rat forebrain. Int J Dev Neurosci 18:29-37.
47. Usuda I, Tanaka K, Chiba T (1998) Efferent projections of the nucleus accumbens in the rat with special reference to subdivision of the nucleus: biotinylated dextran amine study. Brain Res 797:73-93.
48. Wilson CJ (1998) Basal ganglia. In: The synaptic organization of the brain (Shepherd GM, ed), pp 329-375. New York: Oxford UP.
49. Wilson CJ, Groves PM (1981) Spontaneous firing patterns of identified spiny neurons in the rat neostriatum. Brain Res 220:67-80.
50. Wilson CJ, Kawaguchi Y (1996) The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci 16:2397-2410.
51. Wilson CJ, Chang HT, Kitai ST (1982) Origins of postsynaptic potentials evoked in identified rat neostriatal neurons by stimulation in substantia nigra. Exp Brain Res 45:157-167.
52. Yung KKL, Bolam JP, Smith AD, Hersch SM, Ciliax BI, Levey AI (1995) Immunocytochemical localization of D1 and D2 dopamine receptors in the basal ganglia of the rat: light and electron microscopy. Neuroscience 65:709-730.
53. Zhou FM, Wilson CJ, Dani JA (2002) Cholinergic interneuron characteristics and nicotinic properties in the striatum. J Neurobiol 53:590-605.
54. Zhuang X, Masson J, Gingrich JA, Rayport S, Hen R (2004) Targeted gene expression in dopaminergic and serotonergic neurons of the mouse brain. J Neurosci Methods, in press.