Computational model predicts a role for ERG current in repolarizing plateau potentials in dopamine neurons: Implications for modulation of neuronal activity

Journal of Neurophysiology

Volumn 98, Issue 5, 2007, Pages 3006-3022

  Canavier, Carmen C ^a,e   Oprisan, Sorinel A ^b   Callaway, Joseph C ^c   Ji, Huifang ^e   Shepard, Paul D ^d  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b School of Business   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

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

^e Neuroscience Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APAMIN; CALCIUM CHELATING AGENT; CALCIUM ION; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; POTASSIUM CHANNEL HERG; POTASSIUM ION; TETRODOTOXIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOPAMINERGIC ACTIVITY; DOPAMINERGIC NERVE CELL; FREQUENCY ANALYSIS; IN VITRO STUDY; MALE; MODEL; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE POTENTIAL; NEUROMODULATION; NEUROPHYSIOLOGY; NONHUMAN; OSCILLATION; POTASSIUM CURRENT; PREDICTION; PRIORITY JOURNAL; RAT; REPOLARIZATION;

1-NAPHTHYLAMINE; ANIMALS; ANIMALS, NEWBORN; APAMIN; CALCIUM; CHELATING AGENTS; COMPUTER SIMULATION; DOPAMINE; DOPAMINE ANTAGONISTS; EGTAZIC ACID; HALOPERIDOL; MALE; MEMBRANE POTENTIALS; MESENCEPHALON; MODELS, NEUROLOGICAL; NEURONS; POTASSIUM CHANNEL BLOCKERS; RATS; RATS, SPRAGUE-DAWLEY; SMALL-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS;

EID: 35649002144     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00422.2007     Document Type: Article

References (80)

1. + channel multiprotein complexes. J Neurosci 27: 2369-2376, 2007.
2. Amini B, Clark JW Jr, Canavier CC. Calcium dynamics underlying pacemakerlike and burst firing oscillations in midbrain dopaminergic neurons: a computational study. J Neurophysiol 82: 2249-2261, 1999.
3. Bernheimer H, Birkmayer W, Hornykiewicz O, Jellinger K, Seitelberger F. Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. J Neurol Sci 20: 415-455, 1973.
4. Bertram R, Sherman A. Negative calcium feedback: the road from Chay-Keizer. In: Bursting: The Genesis of Rhythm in the Nervous System, edited by Coombes S, Bressloff PC. Singapore: World Scientific Publishing, 2005.
5. + channels and regulates channel gating. Neuron 43: 847-858, 2004.
6. Brodie MS, McElvain MA, Bunney EB, Appel SB. Pharmacological reduction of small conductance calcium-activated potassium current (SK) potentiates the excitatory effect of ethanol on ventral tegmental area dopamine neurons. J Pharmacol Exp Ther 290: 325-333, 1999.
7. Callaway JC, Wilson CJ, Shepard PD. Calcium transients during apamin induced bursting in dopaminergic neurons in the substantia nigra pars compacta. Soc Neurosci Abstr 30: 556.3, 2000.
8. Cardozo DL, Bean BP. Voltage-dependent calcium channels in rat midbrain dopamine neurons: modulation by dopamine and GABAB receptors. J Neurophysiol 74: 1137-1148, 1995.
9. Chay TR, Keizer J. Minimal model for membrane oscillations in the pancreatic β-cell. Biophys J 42: 181-190, 1983.
10. Chergui K, Nomikos GG, Mathe JM, Gonon F, Svensson TH. Burst stimulation of the medial forebrain bundle selectively increases fos-like immunoreactivity in the limbic forebrain of the rat. Neuroscience 72: 141-156, 1996.
11. Diener M. The canard unchained or how fast/slow dynamical systems bifurcate. Math Intell 6: 38-49, 1984.
12. Drover J, Rubin J, Su J, Ermentrout B. Analysis of a canard mechanism by which excitatory synaptic coupling can synchronize neurons at low firing frequencies. SIAM J Appl Math 65: 69-92, 2004.
13. Durante P, Cardenas CG, Whittaker JA, Kitai S, Scroggs RS. Low-threshold L-type calcium channels in rat dopamine neurons. J Neurophysiol 91: 1450-1454, 2004.
14. Fiorillo CD, Williams JT. Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons. Nature 394: 19-21, 1998.
15. Fiorillo CD, Williams JT. Cholinergic inhibition of ventral midbrain dopamine neurons. J Neurosci 20: 7855-7860, 2000.
16. Fisher TE, Bourque CW. Calcium-channel subtypes in the somata and axon terminals of magnocellular neuroscecretory cells. Trends Neurosci 19: 440-444, 1996.
17. Fujimura K, Matsuda Y. Autogenous oscillatory potentials in neurons of the guinea pig substantia nigra pars compacta in vitro. Neurosci Lett 104: 53-57, 1989.
18. 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.
19. Grace AA, Bunney BS. The control of firing pattern in nigral dopamine neurons: single spike firing. J Neurosci 4: 2866-2876, 1984a.
20. Grace AA, Bunney BS. The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 4: 2877-2890, 1984b.
21. Grace AA, Bunney BS. Induction of depolarization block in midbrain dopamine neurons by repeated administration of haloperidol: analysis using in vivo intracellular recording. J Pharmacol Exp Ther 238: 1092-1100, 1986.
22. Grace AA, Bunney BS, Moore H, Todd CL. Dopamine-cell depolarization block as a model for the therapeutic actions of antipsychotic drugs. Trends Neurosci 20: 31-37, 1997.
23. Grynkiewicz G, Poenie M, Tsien RY. A new generation of calcium indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450, 1985.
24. Hairer E, Wanner G. Solving Ordinary Differential Equations. II. Stiff and Differential-Algebraic Problems. New York: Springer-Verlag, 1990.
25. Harris NC, Webb C, Greenfield SA. A possible pacemaker mechanism in pars compacta neurons of the guinea-pig substantia nigra revealed by various ion channel blocking agents. Neuroscience 31: 355-362, 1989.
26. Heien ML, Wightman RM. Phasic dopamine signaling during behavior, reward, and disease states. CNS Neurol Disord Drug Targets 5: 99-108, 2006.
27. Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117: 400-544, 1952.
28. Hyland BI, Reynolds JN, Hay J, Perk CG, Miller R. Firing modes of midbrain dopamine cells in the freely moving rat. Neuroscience 114: 475-492, 2002.
29. Johnson JP Jr, Balser JR, Bennett PB. A novel extracellular calcium sensing mechanism in voltage-gated potassium ion channels. J Neurosci 21: 4143-4153, 2001.
30. Johnson SW, Wu Y-N. Multiple mechanisms underlie burst firing in rat midbrain dopamine neurons in vitro. Brain Res 1019: 293-296, 2004.
31. Kang Y, Kitai S. Calcium spike underlying rhythmic firing in dopaminergic neurons of the rat substantia nigra. Neurosci Res 18: 195-207, 1993a.
32. Kang Y, Kitai S. A whole cell patch-clamp study on the pacemaker potential in dopaminergic neurons of rat substantia nigra compacta. Neurosci Res 18: 209-221, 1993b.
33. Kapur S. How anti-psychotics become anti-"psychotic" - from dopamine to salience to psychosis. Trends Pharmacol Sci 25: 402-406, 2004.
34. Kiyatkin EA, Rebec GV. Heterogeneity of ventral tegmental area neurons: single-unit recordings and iotophoresis in awake, unrestrained rats. Neuroscience 85: 1285-1309, 1998.
35. Kohler M, Hirschberg B, Bond CT, Kinzie JM, Marrion NV, Maylie J, Adelman JP. Small-conductance, calcium-activated potassium channels from mammalian brain. Science 273: 1709-1714, 1996.
36. A and NMDA receptors and the SK channel in regulating the firing pattern in midbrain dopamine neurons. J Neurophysiol 91: 346-357, 2004.
37. Kongsamut S, Kang J, Chen XL, Roehr J, Rampe D. A comparison of the receptor binding and HERG channel affinities for a series of antipsychotic drugs. Eur J Pharmacol 450: 37-41, 2002.
38. Koob GF, Le HT, Creese I. The D1 dopamine receptor antagonist SCH23390 increases cocaine self-administration in the rat. Neurosci Lett 79: 315-320, 1987.
39. + current in MMQ lactotrophs and its accommodating role during slow firing and prolactin release. J Neurosci 22: 3414-3425, 2002.
40. Mercuri NB, Bonci A, Calabresi P, Stefani A, Bernardi G. Properties of the hyperpolarization-activated cation current Ih in rat midbrain dopaminergic neurons. Eur J Neurosci 7: 462-469, 1995.
41. Mercuri NB, Bonci A, Calabresi P, Stratta F, Stefani A, Bernardi G. Effects of dihydropyridine calcium antagonists on rat midbrain dopaminergic neurones. Br J Pharmacol 113: 831-838, 1994.
42. 2+-independent slow afterhyperpolarization in substantia nigra compacta neurons. Neuroscience 125: 841-852, 2004.
43. 2+ conductances in guinea-pig substantia nigra pars compacta neurones. J Physiol 466: 727-747, 1993.
44. Neuhoff H, Neu A, Liss B, Roeper J. IH channels contribute to the different functional properties of identified dopaminergic subpopulations in midbrain. J Neurosci 22: 1290-1302, 2002.
45. Nowycky MC, Fox AP, Tsien RW. Three types of neuronal calcium channel with different calcium agonist sensitivity. Nature 316: 400-443, 1985.
46. H) is an ethanol target in midbrain dopamine neurons of mice. J Neurophysiol 95: 619-626, 2006.
47. + channels in the repolarization of bursting plateau potentials in nigral dopamine neurons. Program No. 987.5. 2005 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2005. Online.
48. Paladini CA, Fiorillo CD, Morikawa H, Williams JT. Amphetamine selectively blocks inhibitory glutamate transmission in dopamine neurons. Nat Neurosci 4: 275-281, 2001.
49. + channel-encoding genes ERG1, ERG2, and ERG3 in the adult rat central nervous system. J Comp Neurol 466: 119-135, 2003.
50. Perko L. Differential Equations and Dynamical Systems. Berlin: Springer-Verlag, 1991.
51. + channels regulate pacemaker activity in nigral dopamine neurons. Neuroreport 7: 809-814, 1996.
52. 2+ chelation evokes bursting plateau potentials in nigral dopamine neurons in vitro. Soc Neurosci Abstr 23: 1211, 1997.
53. Pucak ML, Grace AA. Effects of haloperidol on the activity and membrane physiology of substantia nigra dopamine neurons recorded in vitro. Brain Res 713: 44-52, 1996.
54. Richards CD, Shiroyama T, Kitai ST. Electrophysiological and immunocytochemical characterization of GABA and dopamine neurons in the substantia nigra of the rat. Neuroscience 80: 545-557, 1997.
55. Sacco T, Bruno TA, Wanke E, Tempia F. Functional roles of an ERG current isolated in cerebellar Purkinje neurons. J Neurophysiol 90: 1817-1828, 2003.
56. + channels in the brain. J Neurosci 21: 4609-4624, 2001.
57. + countertransport and net charge displacement. J Biol Chem 273: 18230-18234, 1998.
58. + channels. Eur J Neurosci 11: 753-760, 1999.
59. Schultz W. Behavioral theories and the neurophysiology of reward. Annu Rev Psychol 57: 87-115, 2006.
60. Scroggs RS, Cardenas CG, Whittaker JA, Kitai ST. Muscarine reduces calcium-dependent electrical activity in substantia nigra dopaminergic neurons. J Neurophysiol 86: 2966-2972, 1997.
61. H on the firing of a subgroup of midbrain dopamine neurons. Neuroreport 12: 255-258, 2001.
62. Seutin V, Mkahli F, Massotte L, Dresse A. Calcium release from internal stores is required for the generation of spontaneous hyperpolarizations in dopaminergic neurons of neonatal rats. J Neurophysiol 83: 192-197, 2000.
63. + conductance. Exp Brain Res 86: 141-150, 1991.
64. Shepard PD, Stump D. Nifedipine blocks apamin-induced bursting activity in nigral dopamine-containing neurons. Brain Res 877: 104-109, 1999.
65. + channel. Open-channel block by methanesulfonanilides. Circ Res 78: 499-503, 1996.
66. + channels by the synthetic compound (R)-N-(benzimidazol-2-yl)-1,2,3,4-tetrahydro-1-naphthylamine (NS8593) reduces afterhyperpolarizing current in hippocampal CA1 neurons. Mol Pharmacol 70: 1771-1782, 2006.
67. Suessbrich H, Schonherr R, Heinemann SH, Attali B, Lang F, Busch AE. The inhibitory effect of the antipsychotic drug haloperidol on HERG potassium channels expressed in Xenopus oocytes. Br J Pharmacol 120: 968-974, 1997.
68. Takada M, Kang Y, Imanashi M. Immunohistochemical localization of voltage-gated calcium-channels in substantia nigra dopamine neurons. Eur J Neurosci 13: 757-762, 2001.
69. 2+ concentration resembling bursting electrical activity in single mouse islets of Langerhans. FEBS Lett 259: 19-23, 1989.
70. Wanaverbecq N, Marsh SJ, Al-Qatari M, Brown DA. The plasma membrane calcium-ATPase as a major mechanism for intracellular calcium regulation in neurones from the rat superior cervical ganglion. J Physiol 550: 83-101, 2003.
71. Wang S, Liu S, Morales MJ, Strauss HC, Rasmusson RL. A quantitative analysis of the activation and inactivation kinetics of HERG expressed in Xenopus oocytes. J Physiol 502: 45-60, 1997.
72. Wang T, French ED. L-Glutamate excitation of A10 dopamine neurons is preferentially mediated by activation of NMDA receptors: extra- and intracellular electrophysiological studies in brain slices. Brain Res 627: 229-306, 1993.
73. Weinberger DR. Implications of normal brain development for the pathogenesis of schizophrenia. Arch Gen Psychiatry 44: 660-669, 1987.
74. Weinsberg F, Bauer CK, Schwarz JR. The class III antiarrhythmic agent E-4031 selectively blocks the inactivating inward-rectifying potassium current in rat anterior pituitary tumor cells (GH3/B6 cells). Pfluegers Arch 434: 1-10, 1997.
75. Werkman TR, Kruse CG, Nievelstein H, Long SK, Wadman WJ. In vitro modulation of the firing rate of dopamine neurons in the rat substantia nigra pars compacta and the ventral tegmental area by antipsychotic drugs. Neuropharmacology 40: 927-936, 2001.
76. Williams ME, Feldman DH, McCue AF, Brenner R, Velicelebi G, Ellis SB, Harpold MM. Structure and functional expression of alpha 1, alpha 2, and beta subunits of a novel human neuronal calcium channel subtype. Neuron 8: 71-84, 1992.
77. Wilson CJ, Callaway JC. Coupled oscillator model of the dopaminergic neuron of the substantia nigra. J Neurophysiol 83: 3084-3100, 2000.
78. Witchel HJ, Hancox JC, Nutt DJ. Psychotropic drugs, cardiac arrhythmia, and sudden death. J Clin Psychopharmacol 23: 58-77, 2003.
79. 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.
80. Yung WH, Hausser MA, Jack JJ. Electrophysiology of dopaminergic and non-dopaminergic neurones of the guinea-pig substantia nigra pars compacta in vitro. J Physiol 436: 643-667, 1991.