Pharmacological modulation of the gating properties of small conductance Ca2+-activated K+ channels alters the firing pattern of dopamine neurons in vivo

Journal of Neurophysiology

Volumn 104, Issue 3, 2010, Pages 1726-1735

  Herrik, Kjartan F ^a   Christophersen, Palle ^b   Shepard, Paul D ^c  

^a H LUNDBECK A S   (Denmark)

^b NEUROSEARCH A S   (Denmark)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APAMIN; CHEMICAL AGENT; DOPAMINE 2 RECEPTOR; DOPAMINE AUTORECEPTOR; NS 309; NS 8593; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; IN VIVO STUDY; ION CONDUCTANCE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SUBSTANTIA NIGRA;

1-NAPHTHYLAMINE; ACTION POTENTIALS; ANIMALS; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; INDOLES; ION CHANNEL GATING; MALE; MICE; MICE, INBRED C57BL; NEURONS; OXIMES; POTASSIUM CHANNELS, CALCIUM-ACTIVATED;

EID: 77957199476     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01126.2009     Document Type: Article

References (47)

1. + channel multiprotein complexes. J Neurosci 27: 2369-2376, 2007.
2. + channels and regulates channel gating. Neuron 43: 847-858, 2004.
3. B receptors in mouse substantia nigra dopaminergic neurons in vivo. J Neurosci 28: 10386-10398, 2008.
4. Canavier CC, Oprisan SA, Callaway JC, Ji H, Shepard PD. Computational model predicts a role for ERG current in repolarizing plateau potentials in dopamine neurons: implications for modulation of neuronal activity. J Neurophysiol 98: 3006-3022, 2007. (Pubitemid 350127958)
5. Faber ES, Delaney AJ, Power JM, Sedlak PL, Crane JW, Sah P. Modulation of SK channel trafficking by beta adrenoceptors enhances excitatory synaptic transmission and plasticity in the amygdala. J Neurosci 28: 10803-10813, 2008.
6. Floresco SB, West AR, Ash B, Moore H, Grace AA. Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat Neurosci 6: 968-973, 2003. (Pubitemid 37064759)
7. Garris PA, Ciolkowski EL, Pastore P, Wightman RM. Efflux of dopamine from the synaptic cleft in the nucleus accumbens of the rat brain. J Neurosci 14: 6084-6093, 1994. (Pubitemid 24307800)
8. Gonon FG. Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry. Neuroscience 24: 19-28, 1988.
9. Grace AA. Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 41: 1-24, 1991.
10. Grace AA, Bunney BS. Intracellular and extracellular electrophysiology of nigral dopaminergic neurons. I. Identification and characterization. Neuroscience 10: 301-315, 1983.
11. Grace AA, Bunney BS. The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 4: 2877-2890, 1984a. (Pubitemid 15224432)
12. Grace AA, Bunney BS. The control of firing pattern in nigral dopamine neurons: single spike firing. J Neurosci 4: 2866-2876, 1984b. (Pubitemid 15224431)
13. Hallworth NE, Wilson CJ, Bevan MD. Apamin-sensitive small conductance calcium-activated potassium channels, through their selective coupling to voltage-gated calcium channels, are critical determinants of the precision, pace, and pattern of action potential generation in rat subthalamic nucleus neurons in vitro. J Neurosci 23: 7525-7542, 2003.
14. + channels. Br J Pharmacol 151: 655-665, 2007.
15. Innis RB, Aghajanian GK. Pertussis toxin blocks autoreceptor-mediated inhibition of dopaminergic neurons in rat substantia nigra. Brain Res 411: 139-143, 1987.
16. 2+ sensitivity of SK channels. Eur J Neurosci 29: 1883-1895, 2009.
17. + channel ligands alter the firing pattern of dopamine-containing neurons in vivo. Neuroscience 140: 623-633, 2006.
18. Lammel S, Hetzel A, Hackel O, Jones I, Liss B, Roeper J. Unique properties of mesoprefrontal neurons within A dual mesocorticolimbic dopamine system. Neuron 57: 760-773, 2008. (Pubitemid 351335346)
19. Li W, Halling DB, Hall AW, Aldrich RW. EF hands at the N-lobe of calmodulin are required for both SK channel gating and stable SK-calmodulin interaction. J Gen Physiol 134: 281-293, 2009.
20. Lin MT, Lujan R, Watanabe M, Adelman JP, Maylie J. SK2 channel plasticity contributes to LTP at Schaffer collateral-CA1 synapses. Nat Neurosci 11: 170-177, 2008. (Pubitemid 351170501)
21. 2+ gating. Neuron 59: 439-449, 2008.
22. McMillen BA, Williams HL, Lehmann H, Shepard PD. On central muscle relaxants, strychnine-insensitive glycine receptors and two old drugs: zoxazolamine and HA-966. J Neural Transmiss 89: 11-25, 1992.
23. Paladini CA, Robinson S, Morikawa H, Williams JT, Palmiter RD. Dopamine controls the firing pattern of dopamine neurons via a network feedback mechanism. Proc Natl Acad Sci USA 100: 2866-2871, 2003. (Pubitemid 36297590)
24. Pedarzani P, McCutcheon JE, Rogge G, Jensen BS, Christophersen P, Hougaard C, Strobaek D, Stocker M. Specific enhancement of SK channel activity selectively potentiates the afterhyperpolarizing current I(AHP) and modulates the firing properties of hippocampal pyramidal neurons. J Biol Chem 280: 41404-41411, 2005. (Pubitemid 41832199)
25. + channels. J Biol Chem 276: 9762-9769, 2001.
26. 2+-activated potassium channel, Sk2, through direct phosphorylation by cAMP-dependent protein kinase. J Biol Chem 281: 11769-11779, 2006.
27. Robinson S, Smith DM, Mizumori SJ, Palmiter RD. 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, 2004. (Pubitemid 39209665)
28. 2+-activated potassium channel subunits, SK1, SK2, and SK3 in mouse brain. Mol Cell Neurosci 26: 458-469, 2004.
29. Sanghera MK, Trulson ME, German DC. Electrophysiological properties of mouse dopamine neurons: in vivo and in vitro studies. Neuroscience 12: 793-801, 1984. (Pubitemid 14092493)
30. Schultz W. Behavioral dopamine signals. Trends Neurosci 30: 203-210, 2007.
31. Shepard PD, Bunney BS. Effects of apamin on the discharge properties of putative dopamine-containing neurons in vitro. Brain Res 463: 380-384, 1988.
32. + conductance. Exp Brain Res Exp Hirnforsch 86: 141-150, 1991.
33. Shepard PD, Connelly ST. Pertussis toxin lesions of the rat substantia nigra block the inhibitory effects of the γ-hydroxybutyrate agent, S(-)HA-966 without affecting the basal firing properties of dopamine neurons. Neuropsychopharmacology 21: 650-661, 1999.
34. Sombers LA, Beyene M, Carelli RM, Wightman RM. Synaptic overflow of dopamine in the nucleus accumbens arises from neuronal activity in the ventral tegmental area. J Neurosci 29: 1735-1742, 2009.
35. + channels. J Med Chem 51: 7625-7634, 2008.
36. + channels by the synthetic compound (R)-N-(benzimidazol-2-yl)-1,2,3,4-tetrahydro-1- naphtylamine (NS8593) reduces afterhyperpolarizing current in hippocampal CA1 neurons. Mol Pharmacol 70: 1771-1782, 2006.
37. + channels by NS309 (6,7-dichloro-1H- indole-2,3-dione 3-oxime). Biochim Biophys Acta 1665: 1-5, 2004.
38. Tepper JM, Martin LP, Anderson DR. GABAA receptor-mediated inhibition of rat substantia nigra dopaminergic neurons by pars reticulata projection neurons. J Neurosci 15: 3092-3103, 1995.
39. Tepper JM, Sun BC, Martin LP, Creese I. Functional roles of dopamine D2 and D3 autoreceptors on nigrostriatal neurons analyzed by antisense knockdown in vivo. J Neurosci 17: 2519-2530, 1997.
40. Venton BJ, Zhang H, Garris PA, Phillips PE, Sulzer D, Wightman RM. Real-time decoding of dopamine concentration changes in the caudateputamen during tonic and phasic firing. J Neurochem 87: 1284-1295, 2003. (Pubitemid 37485084)
41. Waroux O, Massotte L, Alleva L, Graulich A, Thomas E, Liegeois JF, Scuvee-Moreau J, Seutin V. SK channels control the firing pattern of midbrain dopaminergic neurons in vivo. Eur J Neurosci 22: 3111-3121, 2005. (Pubitemid 43001994)
42. Werner G, Mountcastle VB. The variability of central neural activity in a sensory system, and its implications for the central reflection of sensory events. J Neurophysiol 26: 958-977, 1963.
43. Wightman RM, Heien ML, Wassum KM, Sombers LA, Aragona BJ, Khan AS, Ariansen JL, Cheer JF, Phillips PE, Carelli RM. Dopamine release is heterogeneous within microenvironments of the rat nucleus accumbens. Eur J Neurosci 26: 2046-2054, 2007. (Pubitemid 47493181)
44. Wilson CJ, Callaway JC. Coupled oscillator model of the dopaminergic neuron of the substantia nigra. J Neurophysiol 83: 3084-3100, 2000.
45. Wolfart J, Neuhoff H, Franz O, Roeper J. Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons. J Neurosci 21: 3443-3456, 2001. (Pubitemid 32422809)
46. Xia XM, Fakler B, Rivard A, Wayman G, Johnson-Pais T, Keen JE, Ishii T, Hirschberg B, Bond CT, Lutsenko S, Maylie J, Adelman JP. Mechanism of calcium gating in small-conductance calcium-activated potassium channels. Nature 395: 503-507, 1998. (Pubitemid 28462445)
47. 2+ release-dependent hyperpolarizations modulate the firing pattern of juvenile GABA neurons in mouse substantia nigra pars reticulata in vitro. J Physiol 577: 879-890, 2006.