Kv3.3 channels at the Purkinje cell soma are necessary for generation of the classical complex spike waveform

Journal of Neuroscience

Volumn 28, Issue 6, 2008, Pages 1291-1300

  Zagha, Edward ^a   Lang, Eric J ^a   Rudy, Bernardo ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Complex spike; Excitability; Kv3; Potassium channels; Purkinje cell; Spinocerebellar ataxia

Indexed keywords

POTASSIUM CHANNEL KV3.3; SHAW POTASSIUM CHANNEL; SODIUM CHANNEL; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CEREBELLUM; CHANNEL GATING; CLIMBING FIBER; CONTROLLED STUDY; DENDRITE; MOUSE; NERVE CELL; NERVE CELL EXCITABILITY; NEUROPHYSIOLOGY; NONHUMAN; PERIKARYON; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PURKINJE CELL; SIGNAL TRANSDUCTION; SODIUM CURRENT; SPIKE WAVE; SYNAPSE;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; CELL MEMBRANE; CEREBELLUM; MICE; MICE, KNOCKOUT; PHENOTYPE; POTASSIUM CHANNEL BLOCKERS; PURKINJE CELLS; SHAW POTASSIUM CHANNELS;

EID: 38949117615     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4358-07.2008     Document Type: Article

References (54)

1. Akemann W, Knopfel T (2006) Interaction of Kv3 potassium channels and resurgent sodium current influences the rate of spontaneous firing of Purkinje neurons. J Neurosci 26:4602-4612.
2. Blenkinsop TA, Lang EJ (2005) Synchronous complex spike activity is associated with changes in deep cerebellar nuclear firing patterns. Soc Neurosci Abstr 31:179.1.
3. Callaway JC, Ross WN (1997) Spatial distribution of synaptically activated sodium concentration changes in cerebellar Purkinje neurons. J Neurophysiol 77:145-152.
4. i increases in the dendrites of cerebellar Purkinje neurons. J Neurosci 15:2777-2787.
5. Chang SY, Zagha E, Kwon ES, Ozaita A, Bobik M, Martone ME, Ellisman MH, Heintz N, Rudy B (2007) Distribution of Kv3.3 potassium channel subunits in distinct neuronal populations of mouse brain. J Comp Neurol 502:953-972.
6. + channels. Ann NY Acad Sci 868:233-285.
7. Davie JT, Hausser M (2004) Determinants of the complex spike waveform in cerebellar Purkinje cells. Soc Neurosci Abstr 30:169.10.
8. de Montigny C, Lamarre Y (1973) Rhythmic activity induced by harmaline in the olivo-cerebello-bulbar system of the cat. Brain Res 53:81-95.
9. Eccles JC, Llinas R, Sasaki K (1966) The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum. J Physiol (Lond) 182:268-296.
10. + channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82:2476-2489.
11. 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.
12. Hansel C, Linden DJ (2000) Long-term depression of the cerebellar climbing fiber-Purkinje neuron synapse. Neuron 26:473-482.
13. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179-1209.
14. Ito M (1993) Synaptic plasticity in the cerebellar cortex and its role in motor learning. Can J Neurol Sci 20 [Suppl 3]:S70-S74.
15. Ito M (2006) Cerebellar circuitry as a neuronal machine. Prog Neurobiol 78:272-303.
16. Joho RH, Street C, Matsushita S, Knopfel T (2006) Behavioral motor dysfunction in Kv3-type potassium channel-deficient mice. Genes Brain Behav 5:472-482.
17. 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.
18. Khavandgar S, Walter JT, Sageser K, Khodakhah K (2005) Kv1 channels selectively prevent dendritic hyperexcitability in rat Purkinje cells. J Physiol (Lond) 569:545-557.
19. Lang EJ, Sugihara I, Llinas R (2006) Olivocerebellar modulation of motor cortex ability to generate vibrissal movements in rat. J Physiol (Lond) 571:101-120.
20. Larramendi EM, Victor T (1967) Synapses on the Purkinje cell spines in the mouse. An electronmicroscopic study. Brain Res 5:15-30.
21. + channel proteins. J Neurosci 20:9071-9085.
22. 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.
23. Linden DJ, Connor JA (1993) Cellular mechanisms of long-term depression in the cerebellum. Curr Opin Neurobiol 3:401-406.
24. Llano I, Marty A, Armstrong CM, Konnerth A (1991) Synaptic- and agonist-induced excitatory currents of Purkinje cells in rat cerebellar slices. J Physiol (Lond) 434:183-213.
25. Llinas R, Nicholson C (1976) Reversal properties of climbing fiber potential in cat Purkinje cells: an example of a distributed synapse. J Neurophysiol 39:311-323.
26. Llinas R, Sugimori M (1980a) Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol (Lond) 305:171-195.
27. Llinas R, Sugimori M (1980b) Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol (Lond) 305:197-213.
28. Llinas R, Volkind RA (1973) The olivo-cerebellar system: functional properties as revealed by harmaline-induced tremor. Exp Brain Res 18:69-87.
29. + channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus. J Neurosci 18:8111-8125.
30. 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.
31. Martina M, Metz AE, Bean BP (2007) Voltage-dependent potassium currents during fast spikes of rat cerebellar Purkinje neurons: inhibition by BDS-I toxin. J Neurophysiol 97:563-571.
32. Matsukawa H, Wolf AM, Matsushita S, Joho RH, Knopfel 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.
33. McKay BE, Turner RW (2004) Kv3 K+ channels enable burst output in rat cerebellar Purkinje cells. Eur J Neurosci 20:729-739.
34. + channels control Purkinje cell output to facilitate postsynaptic rebound discharge in deep cerebellar neurons. J Neurosci 25:1481-1492.
35. McMahon A, Fowler SC, Perney TM, Akemann W, Knopfel 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.
36. Raman IM, Bean BP (1997) Resurgent sodium current and action potential formation in dissociated cerebellar Purkinje neurons. J Neurosci 17:4517-4526.
37. Raman IM, Bean BP (1999) Ionic currents underlying spontaneous action potentials in isolated cerebellar Purkinje neurons. J Neurosci 19:1663-1674.
38. Raman IM, Bean BP (2001) Inactivation and recovery of sodium currents in cerebellar Purkinje neurons: evidence for two mechanisms. Biophys J 80:729-737.
39. Rudy B, McBain CJ (2001) Kv3 channels: voltage-gated K+ 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 de Miera E (1999) Contributions of Kv3 channels to neuronal excitability. Ann NY Acad Sci 868:304-343.
41. Sasaki K, Bower JM, Llinas R (1989) Multiple purkinje cell recording in rodent cerebellar cortex. Eur J Neurosci 1:572-586.
42. Schmolesky MT, Weber JT, De Zeeuw CI, Hansel C (2002) The making of a complex spike: ionic composition and plasticity. Ann NY Acad Sci 978:359-390.
43. Simpson JI, Wylie DR, DeZeeuw CI (1996) On climbing fiber signals and their consequence(s). Behav Brain Sci 19:384-398.
44. + currents in cerebellar basket and Purkinje cells: Kv1 and Kv3 channel subfamilies are present in basket cell nerve terminals. J Neurosci 20:114-122.
45. Stuart G, Hausser M (1994) Initiation and spread of sodium action potentials in cerebellar Purkinje cells. Neuron 13:703-712.
46. Swensen AM, Bean BP (2003) Ionic mechanisms of burst firing in dissociated Purkinje neurons. J Neurosci 23:9650-9663.
47. Thach Jr WT (1967) Somatosensory receptive fields of single units in cat cerebellar cortex. J Neurophysiol 30:675-696.
48. Vega-Saenz de Miera E, Moreno H, Fruhling D, Kentros C, Rudy B (1992) Cloning of ShIII (Shaw-like) cDNAs encoding a novel high-voltage-activating, TEA-sensitive, type-A K+ channel. Proc Biol Sci 248:9-18.
49. Wang LY, Gan L, Forsythe ID, Kaczmarek LK (1998) Contribution of the Kv3.1 potassium channel to high-frequency firing in mouse auditory neurones. J Physiol (Lond) 509:183-194.
50. Waters MF, Minassian NA, Stevanin G, Figueroa KP, Bannister JP, Nolte D, Mock AF, Evidente VG, Fee DB, Muller U, Durr A, Brice A, Papazian DM, Pulst SM (2006) Mutations in voltage-gated potassium channel KCNC3 cause degenerative and developmental central nervous system phenotypes. Nat Genet 38:447-451.
51. Weber JT, De Zeeuw CI, Linden DJ, Hansel C (2003) Long-term depression of climbing fiber-evoked calcium transients in Purkinje cell dendrites. Proc Natl Acad Sci USA 100:2878-2883.
52. Weiser M, Vega-Saenz de Miera E, Kentros C, Moreno H, Franzen L, Hillman D, Baker H, Rudy B (1994) Differential expression of Shaw-related K+ channels in the rat central nervous system. J Neurosci 14:949-972.
53. Welsh JP, Lang EJ, Suglhara I, Llinas R (1995) Dynamic organization of motor control within the olivocerebellar system. Nature 374:453-457.
54. + channels in cerebellar Purkinje neurons. Eur J Neurosci 16:1214-1222.