Phasic dopamine release drives rapid activation of striatal D2-receptors

Neuron

Volumn 84, Issue 1, 2014, Pages 164-176

  Marcott, Pamela F ^a   Mamaligas, Aphroditi A ^a   Ford, Christopher P ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE 2 RECEPTOR; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; GUANINE NUCLEOTIDE BINDING PROTEIN; DOPAMINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOPAMINE RELEASE; EXTRACELLULAR SPACE; INHIBITORY POSTSYNAPTIC CURRENT; MEDIUM SPINY NEURON; MOUSE; NERVE CELL; NONHUMAN; PROTEIN EXPRESSION; RECEPTOR AFFINITY; SIGNAL TRANSDUCTION; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION; WHOLE CELL PATCH CLAMP; ANIMAL; C57BL MOUSE; CORPUS STRIATUM; INHIBITORY POSTSYNAPTIC POTENTIAL; METABOLISM; ORGAN CULTURE TECHNIQUE; PHYSIOLOGY; SECRETION (PROCESS); TIME FACTOR; TRANSGENIC MOUSE;

ANIMALS; CORPUS STRIATUM; DOPAMINE; INHIBITORY POSTSYNAPTIC POTENTIALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; ORGAN CULTURE TECHNIQUES; RECEPTORS, DOPAMINE D2; TIME FACTORS;

EID: 84907970035     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.08.058     Document Type: Article

References (68)

1. Albin R.L., Young A.B., Penney J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989, 12:366-375.
2. Arbuthnott G.W., Wickens J. Space, time and dopamine. Trends Neurosci. 2007, 30:62-69.
3. Baik J.H., Picetti R., Saiardi A., Thiriet G., Dierich A., Depaulis A., Le Meur M., Borrelli E. Parkinsonian-like locomotor impairment in mice lacking dopamine D2 receptors. Nature 1995, 377:424-428.
4. Beckstead M.J., Grandy D.K., Wickman K., Williams J.T. Vesicular dopamine release elicits an inhibitory postsynaptic current in midbrain dopamine neurons. Neuron 2004, 42:939-946.
5. Berke J.D., Hyman S.E. Addiction, dopamine, and the molecular mechanisms of memory. Neuron 2000, 25:515-532.
6. Bromberg-Martin E.S., Hikosaka O. Midbrain dopamine neurons signal preference for advance information about upcoming rewards. Neuron 2009, 63:119-126.
7. Castro L.R., Brito M., Guiot E., Polito M., Korn C.W., Hervé D., Girault J.A., Paupardin-Tritsch D., Vincent P. Striatal neurones have a specific ability to respond to phasic dopamine release. J.Physiol. 2013, 591:3197-3214.
8. Chen R., Tilley M.R., Wei H., Zhou F., Zhou F.M., Ching S., Quan N., Stephens R.L., Hill E.R., Nottoli T., et al. Abolished cocaine reward in mice with a cocaine-insensitive dopamine transporter. Proc. Natl. Acad. Sci. USA 2006, 103:9333-9338.
9. Chergui K., Suaud-Chagny M.F., Gonon F. Nonlinear relationship between impulse flow, dopamine release and dopamine elimination in the rat brain invivo. Neuroscience 1994, 62:641-645.
10. Courtney N.A., Ford C.P. The timing of dopamine- and noradrenaline-mediated transmission reflects underlying differences in the extent of spillover and pooling. J.Neurosci. 2014, 34:7645-7656.
11. Cragg S.J., Rice M.E. DAncing past the DAT at a DA synapse. Trends Neurosci. 2004, 27:270-277.
12. Cragg S., Rice M.E., Greenfield S.A. Heterogeneity of electrically evoked dopamine release and reuptake in substantia nigra, ventral tegmental area, and striatum. J.Neurophysiol. 1997, 77:863-873.
13. De Lean A., Stadel J.M., Lefkowitz R.J. A ternary complex model explains the agonist-specific binding properties of the adenylate cyclase-coupled beta-adrenergic receptor. J.Biol. Chem. 1980, 255:7108-7117.
14. DeLong M.R. Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 1990, 13:281-285.
15. Floresco S.B., West A.R., Ash B., Moore H., Grace A.A. Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat. Neurosci. 2003, 6:968-973.
16. Ford C.P., Phillips P.E., Williams J.T. The time course of dopamine transmission in the ventral tegmental area. J.Neurosci. 2009, 29:13344-13352.
17. Ford C.P., Gantz S.C., Phillips P.E., Williams J.T. Control of extracellular dopamine at dendrite and axon terminals. J.Neurosci. 2010, 30:6975-6983.
18. Gantz S.C., Bunzow J.R., Williams J.T. Spontaneous inhibitory synaptic currents mediated by a G protein-coupled receptor. Neuron 2013, 78:807-812.
19. Garris P.A., Ciolkowski E.L., Pastore P., Wightman R.M. Efflux of dopamine from the synaptic cleft in the nucleus accumbens of the rat brain. J.Neurosci. 1994, 14:6084-6093.
20. Gerfen C.R., Surmeier D.J. Modulation of striatal projection systems by dopamine. Annu. Rev. Neurosci. 2011, 34:441-466.
21. Goto Y., Grace A.A. Limbic and cortical information processing in the nucleus accumbens. Trends Neurosci. 2008, 31:552-558.
22. Grace A.A., Bunney B.S. The control of firing pattern in nigral dopamine neurons: single spike firing. J.Neurosci. 1984, 4:2866-2876.
23. Grace A.A., Bunney B.S. The control of firing pattern in nigral dopamine neurons: burst firing. J.Neurosci. 1984, 4:2877-2890.
24. Grace A.A., Floresco S.B., Goto Y., Lodge D.J. Regulation of firing of dopaminergic neurons and control of goal-directed behaviors. Trends Neurosci. 2007, 30:220-227.
25. Graybiel A.M. Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci. 1990, 13:244-254.
26. Hoffman A.F., Gerhardt G.A. Differences in pharmacological properties of dopamine release between the substantia nigra and striatum: an invivo electrochemical study. J.Pharmacol. Exp. Ther. 1999, 289:455-463.
27. Howe M.W., Tierney P.L., Sandberg S.G., Phillips P.E., Graybiel A.M. Prolonged dopamine signalling in striatum signals proximity and value of distant rewards. Nature 2013, 500:575-579.
28. Howes O.D., Kapur S. The dopamine hypothesis of schizophrenia: version III-the final common pathway. Schizophr. Bull. 2009, 35:549-562.
29. Jones S.R., Gainetdinov R.R., Jaber M., Giros B., Wightman R.M., Caron M.G. Profound neuronal plasticity in response to inactivation of the dopamine transporter. Proc. Natl. Acad. Sci. USA 1998, 95:4029-4034.
30. Karschin C., Dissmann E., Stühmer W., Karschin A. IRK(1-3) and GIRK(1-4) inwardly rectifying K+ channel mRNAs are differentially expressed in the adult rat brain. J.Neurosci. 1996, 16:3559-3570.
31. Kawagoe K.T., Garris P.A., Wiedemann D.J., Wightman R.M. Regulation of transient dopamine concentration gradients in the microenvironment surrounding nerve terminals in the rat striatum. Neuroscience 1992, 51:55-64.
32. Kawaguchi Y., Wilson C.J., Augood S.J., Emson P.C. Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci. 1995, 18:527-535.
33. Keefe K.A., Zigmond M.J., Abercrombie E.D. Invivo regulation of extracellular dopamine in the neostriatum: influence of impulse activity and local excitatory amino acids. J.Neural Transm. 1993, 91:223-240.
34. Kenakin T. The classification of seven transmembrane receptors in recombinant expression systems. Pharmacol. Rev. 1996, 48:413-463.
35. Kenakin T. New concepts in pharmacological efficacy at 7TM receptors: IUPHAR review 2. Br. J. Pharmacol. 2013, 168:554-575.
36. Kita T., Kita H., Kitai S.T. Passive electrical membrane properties of rat neostriatal neurons in an invitro slice preparation. Brain Res. 1984, 300:129-139.
37. Kobayashi T., Ikeda K., Ichikawa T., Abe S., Togashi S., Kumanishi T. Molecular cloning of a mouse G-protein-activated K+ channel (mGIRK1) and distinct distributions of three GIRK (GIRK1, 2 and 3) mRNAs in mouse brain. Biochem. Biophys. Res. Commun. 1995, 208:1166-1173.
38. Kravitz A.V., Freeze B.S., Parker P.R., Kay K., Thwin M.T., Deisseroth K., Kreitzer A.C. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 2010, 466:622-626.
39. Kreitzer A.C. Physiology and pharmacology of striatal neurons. Annu. Rev. Neurosci. 2009, 32:127-147.
40. Lesage F., Guillemare E., Fink M., Duprat F., Heurteaux C., Fosset M., Romey G., Barhanin J., Lazdunski M. Molecular properties of neuronal G-protein-activated inwardly rectifying K+ channels. J.Biol. Chem. 1995, 270:28660-28667.
41. Liao Y.J., Jan Y.N., Jan L.Y. Heteromultimerization of G-protein-gated inwardly rectifying K+ channel proteins GIRK1 and GIRK2 and their altered expression in weaver brain. J.Neurosci. 1996, 16:7137-7150.
42. Lovinger D.M. Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacology 2010, 58:951-961.
43. Lüscher C., Slesinger P.A. Emerging roles for G protein-gated inwardly rectifying potassium (GIRK) channels in health and disease. Nat. Rev. Neurosci. 2010, 11:301-315.
44. Matsuda W., Furuta T., Nakamura K.C., Hioki H., Fujiyama F., Arai R., Kaneko T. Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum. J.Neurosci. 2009, 29:444-453.
45. Meisenzahl E.M., Schmitt G.J., Scheuerecker J., Möller H.J. The role of dopamine for the pathophysiology of schizophrenia. Int. Rev. Psychiatry 2007, 19:337-345.
46. Nicola S.M., Malenka R.C. Modulation of synaptic transmission by dopamine and norepinephrine in ventral but not dorsal striatum. J.Neurophysiol. 1998, 79:1768-1776.
47. Ostrom R.S., Post S.R., Insel P.A. Stoichiometry and compartmentation in G protein-coupled receptor signaling: implications for therapeutic interventions involving G(s). J.Pharmacol. Exp. Ther. 2000, 294:407-412.
48. Ostrom R.S., Gregorian C., Drenan R.M., Xiang Y., Regan J.W., Insel P.A. Receptor number and caveolar co-localization determine receptor coupling efficiency to adenylyl cyclase. J.Biol. Chem. 2001, 276:42063-42069.
49. Phillips P.E., Stuber G.D., Heien M.L., Wightman R.M., Carelli R.M. Subsecond dopamine release promotes cocaine seeking. Nature 2003, 422:614-618.
50. Post S.R., Hilal-Dandan R., Urasawa K., Brunton L.L., Insel P.A. Quantification of signalling components and amplification in the beta-adrenergic-receptor-adenylate cyclase pathway in isolated adult rat ventricular myocytes. Biochem. J. 1995, 311:75-80.
51. Richfield E.K., Penney J.B., Young A.B. Anatomical and affinity state comparisons between dopamine D1 and D2 receptors in the rat central nervous system. Neuroscience 1989, 30:767-777.
52. Schmitz Y., Benoit-Marand M., Gonon F., Sulzer D. Presynaptic regulation of dopaminergic neurotransmission. J.Neurochem. 2003, 87:273-289.
53. Schoffelmeer A.N., Hogenboom F., Mulder A.H., Ronken E., Stoof J.C., Drukarch B. Dopamine displays an identical apparent affinity towards functional dopamine D1 and D2 receptors in rat striatal slices: possible implications for the regulatory role of D2 receptors. Synapse 1994, 17:190-195.
54. Schultz W. Behavioral dopamine signals. Trends Neurosci. 2007, 30:203-210.
55. Schultz W. Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 2007, 30:259-288.
56. Seeman P., Weinshenker D., Quirion R., Srivastava L.K., Bhardwaj S.K., Grandy D.K., Premont R.T., Sotnikova T.D., Boksa P., El-Ghundi M., et al. Dopamine supersensitivity correlates with D2High states, implying many paths to psychosis. Proc. Natl. Acad. Sci. USA 2005, 102:3513-3518.
57. Sibley D.R., De Lean A., Creese I. Anterior pituitary dopamine receptors. Demonstration of interconvertible high and low affinity states of the D-2 dopamine receptor. J.Biol. Chem. 1982, 257:6351-6361.
58. Sibley D.R., Mahan L.C., Creese I. Dopamine receptor binding on intact cells. Absence of a high-affinity agonist-receptor binding state. Mol. Pharmacol. 1983, 23:295-302.
59. Skinbjerg M., Sibley D.R., Javitch J.A., Abi-Dargham A. Imaging the high-affinity state of the dopamine D2 receptor invivo: fact or fiction?. Biochem. Pharmacol. 2012, 83:193-198.
60. Sodickson D.L., Bean B.P. GABAB receptor-activated inwardly rectifying potassium current in dissociated hippocampal CA3 neurons. J.Neurosci. 1996, 16:6374-6385.
61. Surmeier D.J. Striatum: Cell Types, Membrane Properties and Neuromodulation; Microcircuits in the striatum 2006, The MIT Press, Cambridge, MA.
62. Surmeier D.J., Carrillo-Reid L., Bargas J. Dopaminergic modulation of striatal neurons, circuits, and assemblies. Neuroscience 2011, 198:3-18.
63. Tepper James M., Plenz Dietmar Striatum: striatal cell types and their interaction. Microcircuits: The Interface between Neurons and Global Brain Function 2006, 127-148. The MIT Press, Cambridge. G. Graybiel (Ed.).
64. Tobler P.N., Fiorillo C.D., Schultz W. Adaptive coding of reward value by dopamine neurons. Science 2005, 307:1642-1645.
65. Tritsch N.X., Sabatini B.L. Dopaminergic modulation of synaptic transmission in cortex and striatum. Neuron 2012, 76:33-50.
66. van Wieringen J.P., Booij J., Shalgunov V., Elsinga P., Michel M.C. Agonist high- and low-affinity states of dopamine D(2) receptors: methods of detection and clinical implications. Naunyn Schmiedebergs Arch. Pharmacol. 2013, 386:135-154.
67. Volkow N.D., Fowler J.S., Wang G.J., Baler R., Telang F. Imaging dopamine's role in drug abuse and addiction. Neuropharmacology 2009, 56(Suppl 1):3-8.
68. Wightman R.M., Kuhr W.G., Ewing A.G. Voltammetric detection of dopamine release in the rat corpus striatum. Ann. N Y Acad. Sci. 1986, 473:92-105.