Interaction of Kv3 potassium channels and resurgent sodium current influences the rate of spontaneous firing of purkinje neurons

Journal of Neuroscience

Volumn 26, Issue 17, 2006, Pages 4602-4612

  Akemann, Walther ^a   Knöpfel, Thomas ^a  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Cerebellum; Knock out mice; Potassium channels; Purkinje neurons; Sodium channel; Spike trains

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; CALCIUM ION; POTASSIUM CHANNEL; POTASSIUM CHANNEL KV3.3; PROTEIN SUBUNIT; SODIUM; SODIUM CHANNEL; UNCLASSIFIED DRUG; KCNC3 PROTEIN, MOUSE; POTASSIUM; SHAW POTASSIUM CHANNEL;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CURRENT; CALCIUM TRANSPORT; COMPUTER SIMULATION; CONTROLLED STUDY; ION CURRENT; KNOCKOUT MOUSE; MOLECULAR INTERACTION; MOUSE; NONHUMAN; PATCH CLAMP; POTASSIUM CURRENT; PRIORITY JOURNAL; PURKINJE CELL; SIMULATION; SODIUM CURRENT; ANIMAL; BIOLOGICAL RHYTHM; C57BL MOUSE; CELL CULTURE; CHANNEL GATING; INSTITUTE FOR CANCER RESEARCH MOUSE; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; BIOLOGICAL CLOCKS; CELLS, CULTURED; ION CHANNEL GATING; MICE; MICE, INBRED C57BL; MICE, INBRED ICR; MICE, KNOCKOUT; POTASSIUM; PURKINJE CELLS; SHAW POTASSIUM CHANNELS; SODIUM;

EID: 33646835722     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5204-05.2006     Document Type: Article

References (54)

1. Armstrong DM, Rawson JA (1979) Activity patterns of cerebellar cortical neurons and climbing fibre afferents in the awake cat. J Physiol (Lond) 289:425-448.
2. Atzori M, Lau D, Tansey EP, Chow A, Ozaita A, Rudy B, McBain CJ (2000) H2 histamine receptor-phosphorylation of Kv3.2 modulates interneuron fast spiking. Nat Neurosci 3:791-798.
3. Bal T, McCormick DA (1997) Synchronized oscillations in the inferior olive are controlled by the hyperpolarization-activated cation current I(h). J Neurophysiol 77:3145-3156.
4. Behnisch T, Matsushita S, Knöpfel T (2004) Imaging of gene expression during long-term potentiation. NeuroReport 15:2039-2043.
5. Benardo LS, Foster RE (1986) Oscillatory behavior in inferior olive neurons: mechanism, modulation, cell aggregates. Brain Res Bull 17:773-784.
6. Cerminara NL, Rawson JA (2004) Evidence that climbing fibers control an intrinsic spike generator in cerebellar Purkinje cells. J Neurosci 24:4510-4517.
7. Chan E (1997) Regulation and function of Kv3.3. PhD thesis, Rockefeller University.
8. Chung YH, Joo KM, Kim MJ, Cha CI (2003) Age-related changes in the distribution of Na(v)1.1 and Na(v)1.2 in rat cerebellum. NeuroReport 14:841-845.
9. Do MT, Bean BP (2003) Subthreshold sodium currents and pacemaking of subthalamic neurons: modulation by slow inactivation. Neuron 39:109-120.
10. Do MT, Bean BP (2004) Sodium currents in subthalamic nucleus neurons from Nav1.6-null mice. J Neurophysiol 92:726-733.
11. + channels to rat Purkinje neuron function. J Physiol (Lond) 548:53-69.
12. + channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82:2476-2489.
13. Goldman-Wohl DS, Chan E, Baird D, Heintz N (1994) Kv3.3b: a novel Shaw type potassium channel expressed in terminally differentiated cerebellar Purkinje cells and deep cerebellar nuclei. J Neurosci 14:511-522.
14. Granit R, Phillips CG (1956) Excitatory and inhibitory processes acting upon individual Purkinje cells of the cerebellum in cats. J Physiol (Lond) 133:520-547.
15. Grieco TM, Raman IM (2004) Production of resurgent current in NaV1.6-null Purkinje neurons by slowing sodium channel inactivation with β-pompilidotoxin. J Neurosci 24:35-42.
16. Grieco TM, Malhotra JD, Chen C, Isom LL, Raman IM (2005) Open-channel block by the cytoplasmic tail of sodium channel beta4 as a mechanism for resurgent sodium current. Neuron 45:233-244.
17. Häusser M, Clark BA (1997) Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration. Neuron 19:665-678.
18. Häusser M, Raman IM, Otis T, Smith SL, Nelson A, du Lac S, Loewenstein Y, Mahon S, Pennartz C, Cohen I, Yarom Y (2004) The beat goes on: spontaneous firing in mammalian neuronal microcircuits. J Neurosci 24:9215-9219.
19. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179-1209.
20. Itri JN, Michel S, Vansteensel MJ, Meijer JH, Colwell CS (2005) Fast delayed rectifier potassium current is required for circadian neural activity. Nat Neurosci 8:650-656.
21. Joho RH, Street C, Matsushita S, Knöpfel T (2006) Behavioral motor dysfunction in Kv3-type potassium channel-deficient mice. Genes Brain Behav, in press.
22. Kay AR, Sugimori M, Llinas R (1998) Kinetic and stochastic properties of a persistent sodium current in mature guinea pig cerebellar Purkinje cells. J Neurophysiol 80:1167-1179.
23. Khaliq ZM, Gouwens NW, Raman IM (2003) The contribution of resurgent sodium current to high-frequency firing in Purkinje neurons: an experimental and modeling study. J Neurosci 23:4899-4912.
24. Kohrman DC, Smith MR, Goldin AL, Harris J, Meisler MH (1996) A missense mutation in the sodium channel Scn8a is responsible for cerebellar ataxia in the mouse mutant jolting. J Neurosci 16:5993-5999.
25. Kullmann PH, Wheeler DW, Beacom J, Horn JP (2004) Implementation of a fast 16-bit dynamic clamp using LabVIEW-RT. J Neurophysiol 91:542-554.
26. Lien CC, Jonas P (2003) Kv3 potassium conductance is necessary and kinetically optimized for high-frequency action potential generation in hippocampal interneurons. J Neurosci 23:2058-2068.
27. Llinas R, Sugimori M (1980) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol (Lond) 305:171-195.
28. Llinas R, Yarom Y (1986) Oscillatory properties of guinea-pig inferior olivary neurones and their pharmacological modulation: an in vitro study. J Physiol (Lond) 376:163-182.
29. Martina M, Yao GL, Bean BP (2003) Properties and functional role of voltage-dependent potassium channels in dendrites of rat cerebellar Purkinje neurons. J Neurosci 23:5698-5707.
30. Matsukawa H, Wolf AM, Matsushita S, Joho RH, Knöpfel T (2003) Motor dysfunction and altered synaptic transmission at the parallel fiber-Purkinje cell synapse in mice lacking potassium channels Kv3.1 and Kv3.3. J Neurosci 23:7677-7684.
31. + channels enable burst output in rat cerebellar Purkinje cells. Eur J Neurosci 20:729-739.
32. + channels control Purkinje cell output to facilitate postsynaptic rebound discharge in deep cerebellar neurons. J Neurosci 25:1481-1492.
33. McMahon A, Fowler SC, Perney TM, Akemann W, Knöpfel T, Joho RH (2004) Allele-dependent changes of olivocerebellar circuit properties in the absence of the voltage-gated potassium channels Kv3.1 and Kv3.3. Eur J Neurosci 19:3317-3327.
34. Nelson AB, Krispel CM, Sekirnjak C, du LS (2003) Long-lasting increases in intrinsic excitability triggered by inhibition. Neuron 40:609-620.
35. Raman IM, Bean BP (1997) Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J Neurosci 17:4517- 4526.
36. Raman IM, Bean BP (1999) Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J Neurosci 19:1663-1674.
37. Raman IM, Bean BP (2001) Inactivation and recovery of sodium currents in cerebellar Purkinje neurons: evidence for two mechanisms. Biophys J 80:729-737.
38. Raman IM, Sprunger LK, Meisler MH, Bean BP (1997) Altered subthreshold sodium currents and disrupted firing patterns in Purkinje neurons of Scn8a mutant mice. Neuron 19:881-891.
39. + channels designed for high-frequency repetitive firing. Trends Neurosci 24:517-526.
40. Rudy B, Chow A, Lau D, Amarillo Y, Ozaita A, Saganich M, Moreno H, Nadal MS, Hernandez-Pineda R, Hernandez-Cruz A, Erisir A, Leonard C, Vega-Saenz dM (1999) Contributions of Kv3 channels to neuronal excitability. Ann NY Acad Sci 868:304-343.
41. Sacco T, Tempia F (2002) A-type potassium currents active at subthreshold potentials in mouse cerebellar Purkinje cells. J Physiol (Lond) 543:505-520.
42. + channel deficiency. Proc Natl Acad Sci USA 101:9474-9478.
43. Schaller KL, Caldwell JH (2003) Expression and distribution of voltage-gated sodium channels in the cerebellum. Cerebellum 2:2-9.
44. Shah BS, Stevens EB, Pinnock RD, Dixon AK, Lee K (2001) Developmental expression of the novel voltage-gated sodium channel auxiliary subunit beta3, in rat CNS. J Physiol (Lond) 534:763-776.
45. Smith SL, Otis TS (2003) Persistent changes in spontaneous firing of Purkinje neurons triggered by the nitric oxide signaling cascade. J Neurosci 23:367-372.
46. Song P, Yang Y, Barnes-Davies M, Bhattacharjee A, Hamann M, Forsythe ID, Oliver DL, Kaczmarek LK (2005) Acoustic environment determines phosphorylation state of the Kv3.1 potassium channel in auditory neurons. Nat Neurosci 8:1335-1342.
47. 2+ channel alpha1B subunit gene-deficient mice with a CBA/JN genetic background. Exp Anim 54:29-36.
48. Vega-Saenz de Miera EC, Rudy B, Sugimori M, Llinas R (1997) Molecular characterization of the sodium channel subunits expressed in mammalian cerebellar Purkinje cells. Proc Natl Acad Sci USA 94:7059-7064.
49. von Hehn CA, Bhattacharjee A, Kaczmarek LK (2004) Loss of Kv3.1 tonotopicity and alterations in cAMP response element-binding protein signaling in central auditory neurons of hearing impaired mice. J Neurosci 24:1936-1940.
50. + channels in the rat central nervous system. J Neurosci 14:949-972.
51. Williams SR, Christensen SR, Stuart GJ, Häusser M (2002) Membrane potential bistability is controlled by the hyperpolarization-activated current I(H) in rat cerebellar Purkinje neurons in vitro. J Physiol (Lond) 539:469-483.
52. + channels in cerebellar Purkinje neurons. Eur J Neurosci 16:1214-1222.
53. Xu M, Welling A, Paparisto S, Hofmann F, Klugbauer N (2003) Enhanced expression of L-type Cav1.3 calcium channels in murine embryonic hearts from Cav1.2-deficient mice. J Biol Chem 278:40837-40841.
54. Zerr P, Adelman JP, Maylie J (1998) Episodic ataxia mutations in Kv1.1 alter potassium channel function by dominant negative effects or haploinsufficiency. J Neurosci 18:2842-2848.