Dopaminergic modulation of axonal potassium channels and action potential waveform in pyramidal neurons of prefrontal cortex

Journal of Physiology

Volumn 591, Issue 13, 2013, Pages 3233-3251

  Yang, Jing ^a   Ye, Mingyu ^a   Tian, Cuiping ^a   Yang, Mingpo ^a   Wang, Yonghong ^a   Shu, Yousheng ^a  

^a Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; POTASSIUM CHANNEL; DOPAMINE; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DOPAMINERGIC ACTIVITY; DOPAMINERGIC NERVE CELL; INTRACELLULAR SIGNALING; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE POTENTIAL; NEUROMODULATION; NEUROPHYSIOLOGY; NONHUMAN; PATCH CLAMP; POTASSIUM CURRENT; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC TRANSMISSION; WAVEFORM; ACTION POTENTIAL; ANIMAL; IN VITRO STUDY; METABOLISM; NERVE FIBER; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; ANIMALS; AXONS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DOPAMINE; IN VITRO TECHNIQUES; POTASSIUM CHANNELS, VOLTAGE-GATED; PREFRONTAL CORTEX; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2;

EID: 84879838501     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.251058     Document Type: Article

References (72)

1. Alle H & Geiger JR (2006). Combined analog and action potential coding in hippocampal mossy fibers. Science 311, 1290-1293.
2. Beaulieu JM & Gainetdinov RR (2011). The physiology, signaling, and pharmacology of dopamine receptors. Pharmacol Rev 63, 182-217.
3. Bekkers JM (2000a). Distribution and activation of voltage-gated potassium channels in cell-attached and outside-out patches from large layer 5 cortical pyramidal neurons of the rat. J Physiol 525, 611-620.
4. Bekkers JM (2000b). Properties of voltage-gated potassium currents in nucleated patches from large layer 5 cortical pyramidal neurons of the rat. J Physiol 525, 593-609.
5. Bekkers JM & Delaney AJ (2001). Modulation of excitability by α-dendrotoxin-sensitive potassium channels in neocortical pyramidal neurons. J Neurosci 21, 6553-6560.
6. Bender KJ, Ford CP & Trussell LO (2010). Dopaminergic modulation of axon initial segment calcium channels regulates action potential initiation. Neuron 68, 500-511.
7. Bender KJ, Uebele VN, Renger JJ & Trussell LO (2012). Control of firing patterns through modulation of axon initial segment T-type calcium channels. J Physiol 590, 109-118.
8. Bosma MM, Allen ML, Martin TM & Tempel BL (1993). PKA-dependent regulation of mKv1.1, a mouse Shaker-like potassium channel gene, when stably expressed in CHO cells. J Neurosci 13, 5242-5250.
9. Briggs CA, Pollock NJ, Frail DE, Paxson CL, Rakowski RF, Kang CH & Kebabian JW (1991). Activation of the 5-HT1C receptor expressed in Xenopus oocytes by the benzazepines SCH 23390 and SKF 38393. Br J Pharmacol 104, 1038-1044.
10. Connors EC, Ballif BA & Morielli AD (2008). Homeostatic regulation of Kv1.2 potassium channel trafficking by cyclic AMP. J Biol Chem 283, 3445-3453.
11. Cornil CA, Balthazart J, Motte P, Massotte L & Seutin V (2002). Dopamine activates noradrenergic receptors in the preoptic area. J Neurosci 22, 9320-9330.
12. Czyrak A, Czepiel K, Mackowiak M, Chocyk A & Wedzony K (2003). Serotonin 5-HT1A receptors might control the output of cortical glutamatergic neurons in rat cingulate cortex. Brain Res 989, 42-51.
13. de Polavieja GG, Harsch A, Kleppe I, Robinson HP & Juusola M (2005). Stimulus history reliably shapes action potential waveforms of cortical neurons. J Neurosci 25, 5657-5665.
14. Devoto P, Flore G, Pani L & Gessa G (2001). Evidence for co-release of noradrenaline and dopamine from noradrenergic neurons in the cerebral cortex. Mol Psychiatr 6, 657-664.
15. 2-adrenoceptor mediated co-release of dopamine and noradrenaline from noradrenergic neurons' in the cerebral cortex. J Neurochem 88, 1003-1009.
16. Di Pietro NC & Seamans JK (2011). Dopamine and serotonin interactively modulate prefrontal cortex neurons in vitro. Biol Psychiatry 69, 1204-1211.
17. Dong Y, Cooper D, Nasif F, Hu XT & White FJ (2004). Dopamine modulates inwardly rectifying potassium currents in medial prefrontal cortex pyramidal neurons. J Neurosci 24, 3077-3085.
18. Dong Y, Nasif FJ, Tsui JJ, Ju WY, Cooper DC, Hu XT, Malenka RC & White FJ (2005). Cocaine-induced plasticity of intrinsic membrane properties in prefrontal cortex pyramidal neurons: adaptations in potassium currents. J Neurosci 25, 936-940.
19. Dong Y & White FJ (2003). Dopamine D1-class receptors selectively modulate a slowly inactivating potassium current in rat medial prefrontal cortex pyramidal neurons. J Neurosci 23, 2686-2695.
20. + channel inactivation gating by the cAMP-dependent protein kinase. Neuron 12, 1097-1109.
21. Fiorentini C, Busi C, Spano P & Missale C (2010). Dimerization of dopamine D1 and D3 receptors in the regulation of striatal function. Curr Opin Pharmacol 10, 87-92.
22. Gao WJ, Krimer LS & Goldman-Rakic PS (2001). Presynaptic regulation of recurrent excitation by D1 receptors in prefrontal circuits. Proc Natl Acad Sci U S A 98, 295-300.
23. Gee S, Ellwood I, Patel T, Luongo F, Deisseroth K & Sohal VS (2012). Synaptic activity unmasks dopamine D2 receptor modulation of a specific class of layer V pyramidal neurons in prefrontal cortex. J Neurosci 32, 4959-4971.
24. + channels in hippocampal mossy fiber boutons. Neuron 28, 927-939.
25. Geijo-Barrientos E & Pastore C (1995). The effects of dopamine on the subthreshold electrophysiological responses of rat prefrontal cortex neurons in vitro. Eur J Neurosci 7, 358-366.
26. + channels at the axon initial segment dampen near-threshold excitability of neocortical fast-spiking GABAergic interneurons. Neuron 58, 387-400.
27. Goldman-Rakic PS (1998). The cortical dopamine system: role in memory and cognition. Adv Pharmacol 42, 707-711.
28. Gorelova N, Seamans JK & Yang CR (2002). Mechanisms of dopamine activation of fast-spiking interneurons that exert inhibition in rat prefrontal cortex. J Neurophysiol 88, 3150-3166.
29. Gorelova NA & Yang CR (2000). Dopamine D1/D5 receptor activation modulates a persistent sodium current in rat prefrontal cortical neurons in vitro. J Neurophysiol 84, 75-87.
30. Greif GJ, Lin YJ & Freedman JE (1995). Role of cyclic AMP in dopamine modulation of potassium channels on rat striatal neurons: regulation of a subconductance state. Synapse 21, 275-277.
31. Han KA, Millar NS, Grotewiel MS & Davis RL (1996). DAMB, a novel dopamine receptor expressed specifically in Drosophila mushroom bodies. Neuron 16, 1127-1135.
32. Harris-Warrick RM, Coniglio LM, Barazangi N, Guckenheimer J & Gueron S (1995). Dopamine modulation of transient potassium current evokes phase shifts in a central pattern generator network. J Neurosci 15, 342-358.
33. Hasbi A, O'Dowd BF & George SR (2010). Heteromerization of dopamine D2 receptors with dopamine D1 or D5 receptors generates intracellular calcium signaling by different mechanisms. Curr Opin Pharmacol 10, 93-99.
34. v1.2 in action potential initiation and backpropagation. Nat Neurosci 12, 996-1002.
35. Johnson RP, El-Yazbi AF, Hughes MF, Schriemer DC, Walsh EJ, Walsh MP & Cole WC (2009). Identification and functional characterization of protein kinase A-catalyzed phosphorylation of potassium channel Kv1.2 at serine 449. J Biol Chem 284, 16562-16574.
36. Jonas EA & Kaczmarek LK (1996). Regulation of potassium channels by protein kinases. Curr Opin Neurobiol 6, 318-323.
37. Juusola M, Robinson HP & de Polavieja GG (2007). Coding with spike shapes and graded potentials in cortical networks. Bioessays 29, 178-187.
38. Kang J, Huguenard JR & Prince DA (2000). Voltage-gated potassium channels activated during action potentials in layer V neocortical pyramidal neurons. J Neurophysiol 83, 70-80.
39. Kim J, Wei DS & Hoffman DA (2005). Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones. J Physiol 569, 41-57.
40. Kole MH, Letzkus JJ & Stuart GJ (2007). Axon initial segment Kv1 channels control axonal action potential waveform and synaptic efficacy. Neuron 55, 633-647.
41. Lee SP, So CH, Rashid AJ, Varghese G, Cheng R, Lanca AJ, O'Dowd BF & George SR (2004). Dopamine D1 and D2 receptor Co-activation generates a novel phospholipase C-mediated calcium signal. J Biol Chem 279, 35671-35678.
42. Lewis DA, Sesack SR, Levey AI & Rosenberg DR (1998). Dopamine axons in primate prefrontal cortex: specificity of distribution, synaptic targets, and development. Adv Pharmacol 42, 703-706.
43. Lin L, Sun W, Wikenheiser AM, Kung F & Hoffman DA (2010). KChIP4a regulates Kv4.2 channel trafficking through PKA phosphorylation. Mol Cell Neurosci 43, 315-325.
44. Maurice N, Tkatch T, Meisler M, Sprunger LK & Surmeier DJ (2001). D1/D5 dopamine receptor activation differentially modulates rapidly inactivating and persistent sodium currents in prefrontal cortex pyramidal neurons. J Neurosci 21, 2268-2277.
45. Millan MJ, Newman-Tancredi A, Quentric Y & Cussac D (2001). The "selective" dopamine D1 receptor antagonist, SCH23390, is a potent and high efficacy agonist at cloned human serotonin2C receptors. Psychopharmacology (Berl) 156, 58-62.
46. Mitterdorfer J & Bean BP (2002). Potassium currents during the action potential of hippocampal CA3 neurons. J Neurosci 22, 10106-10115.
47. + currents. J Physiol 586, 1565-1579.
48. Neve KA, Seamans JK & Trantham-Davidson H (2004). Dopamine receptor signaling. J Recept Signal Transduct Res 24, 165-205.
49. Nusser Z, Sieghart W, Benke D, Fritschy JM & Somogyi P (1996). Differential synaptic localization of two major gamma-aminobutyric acid type A receptor alpha subunits on hippocampal pyramidal cells. Proc Natl Acad Sci U S A 93, 11939-11944.
50. Pan Z, Kao T, Horvath Z, Lemos J, Sul JY, Cranstoun SD, Bennett V, Scherer SS & Cooper EC (2006). A common ankyrin-G-based mechanism retains KCNQ and NaV channels at electrically active domains of the axon. J Neurosci 26, 2599-2613.
51. Rotaru DC, Lewis DA & Gonzalez-Burgos G (2007). Dopamine D1 receptor activation regulates sodium channel-dependent EPSP amplification in rat prefrontal cortex pyramidal neurons. J Physiol 581, 981-1000.
52. Santana N, Mengod G & Artigas F (2009). Quantitative analysis of the expression of dopamine D1 and D2 receptors in pyramidal and GABAergic neurons of the rat prefrontal cortex. Cereb Cortex 19, 849-860.
53. Sather W, Dieudonne S, MacDonald JF & Ascher P (1992). Activation and desensitization of N-methyl-D-aspartate receptors in nucleated outside-out patches from mouse neurones. J Physiol 450, 643-672.
54. Seamans JK, Durstewitz D, Christie BR, Stevens CF & Sejnowski TJ (2001). Dopamine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cortex neurons. Proc Natl Acad Sci U S A 98, 301-306.
55. Seamans JK & Yang CR (2004). The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog Neurobiol 74, 1-58.
56. Seong HJ & Carter AG (2012). D1 receptor modulation of action potential firing in a subpopulation of layer 5 pyramidal neurons in the prefrontal cortex. J Neurosci 32, 10516-10521.
57. Shah MM, Migliore M, Valencia I, Cooper EC & Brown DA (2008). Functional significance of axonal Kv7 channels in hippocampal pyramidal neurons. Proc Natl Acad Sci U S A 105, 7869-7874.
58. Shu Y (2011). Neuronal signaling in central nervous system. Sheng Li Xue Bao 63, 1-8.
59. Shu Y, Duque A, Yu Y, Haider B & McCormick DA (2007a). Properties of action-potential initiation in neocortical pyramidal cells: evidence from whole cell axon recordings. J Neurophysiol 97, 746-760.
60. Shu Y, Hasenstaub A, Duque A, Yu Y & McCormick DA (2006). Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential. Nature 441, 761-765.
61. + current. Proc Natl Acad Sci U S A 104, 11453-11458.
62. Smiley JF, Levey AI, Ciliax BJ & Goldman-Rakic PS (1994). D1 dopamine receptor immunoreactivity in human and monkey cerebral cortex: predominant and extrasynaptic localization in dendritic spines. Proc Natl Acad Sci U S A 91, 5720-5724.
63. Song WJ, Tkatch T, Baranauskas G, Ichinohe N, Kitai ST & Surmeier DJ (1998). Somatodendritic depolarization-activated potassium currents in rat neostriatal cholinergic interneurons are predominantly of the A type and attributable to coexpression of Kv4.2 and Kv4.1 subunits. J Neurosci 18, 3124-3137.
64. Surmeier DJ & Kitai ST (1993). D1 and D2 dopamine receptor modulation of sodium and potassium currents in rat neostriatal neurons. Prog Brain Res 99, 309-324.
65. Valentijn JA, Louiset E, Vaudry H & Cazin L (1991). Dopamine-induced inhibition of action potentials in cultured frog pituitary melanotrophs is mediated through activation of potassium channels and inhibition of calcium and sodium channels. Neuroscience 42, 29-39.
66. Vincent SL, Khan Y & Benes FM (1993). Cellular distribution of dopamine D1 and D2 receptors in rat medial prefrontal cortex. J Neurosci 13, 2551-2564.
67. Werner P, Hussy N, Buell G, Jones KA & North RA (1996). D2, D3, and D4 dopamine receptors couple to G protein- regulated potassium channels in Xenopus oocytes. Mol Pharmacol 49, 656-661.
68. + (GIRK)-like channel current in pyramidal neurons of the medial prefrontal cortex. Neuroscience 155, 53-63.
69. Yang CR & Seamans JK (1996). Dopamine D1 receptor actions in layers V-VI rat prefrontal cortex neurons in vitro: modulation of dendritic-somatic signal integration. J Neurosci 16, 1922-1935.
70. Yang CR, Seamans JK & Gorelova N (1999). Developing a neuronal model for the pathophysiology of schizophrenia based on the nature of electrophysiological actions of dopamine in the prefrontal cortex. Neuropsychopharmacology 21, 161-194.
71. A in pyramidal neurons in (rat) primary visual cortex. J Neurosci 25, 9185-9194.
72. Zhu J, Jiang M, Yang M, Hou H & Shu Y (2011). Membrane potential-dependent modulation of recurrent inhibition in rat neocortex. PLoS Biol 9, e1001032.