The role of Kv3-type potassium channels in cerebellar physiology and behavior

Cerebellum

Volumn 8, Issue 3, 2009, Pages 323-333

  Joho, Rolf H ^a   Hurlock, Edward C ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Cerebellum; Kv3 subfamily; Motor dysfunction; Potassium channels; Purkinje cell

Indexed keywords

SHAW POTASSIUM CHANNEL;

ACTION POTENTIAL; CELL FUNCTION; CEREBELLAR ATAXIA; CEREBELLUM CORTEX; ELECTRIC POTENTIAL; HUMAN; MOTOR DYSFUNCTION; NERVE CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL; REVIEW;

ACTION POTENTIALS; ANIMALS; BEHAVIOR; CEREBELLUM; GENE EXPRESSION; HUMANS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MOVEMENT DISORDERS; NEURONS; PROTEIN SUBUNITS; PSYCHOMOTOR PERFORMANCE; SHAW POTASSIUM CHANNELS;

EID: 69549103035     PISSN: 14734222     EISSN: 14734230     Source Type: Journal    
DOI: 10.1007/s12311-009-0098-4     Document Type: Review

References (79)

1. CD Aizenman DJ Linden 1999 Regulation of rebound depolarization and spontaneous firing patterns of deep nuclear neurons in slices of rat cerebellum J Neurophysiol 82 1697 1709
2. CD Aizenman DJ Linden 2000 Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons Nature Neurosci 3 109 111
3. CD Aizenman PB Manis DJ Linden 1998 Polarity of long-term synaptic gain change is related to postsynaptic spike firing at a cerebellar inhibitory synapse Neuron 21 828 835
4. CD Aizenman EJ Huang DJ Linden 2003 Morphological correlates of intrinsic electrical excitability in neurons of the deep cerebellar nuclei J Neurophysiol 89 1738 1747
5. V Alonso-Espinaco I Elezgarai J Diez-Garcia N Puente T Knöpfel P Grandes 2008 Subcellular localization of the voltage-gated potassium channels Kv3.1b and Kv3.3 in the cerebellar dentate nucleus of glutamic acid decarboxylase 67-green fluorescent protein transgenic mice Neurosci 155 1059 1069
6. A receptors in cerebellar granule neurons by ethanol: a review of genetic and electrophysiological studies Alcohol 41 187 199
7. Chan E (1997) Regulation and function of Kv3.3. Ph.D. Thesis, The Rockefeller University
8. Chan-Palay V (1997) Cerebellar dentate nucleus: organization, cytology and transmitters. Springer, New York
9. SY Chang E Zagha ES Kwon A Ozaita M Bobik ME Martone MH Ellisman N Heintz B Rudy 2007 Distribution of Kv3.3 potassium channel subunits in distinct neuronal populations of mouse brain J Comp Neurol 502 953 972
10. M Carta M Mameli CF Valenzuela 2004 Alcohol enhances GABAergic transmission to cerebellar granule cells via an increase in Golgi cell excitability J Neurosci 24 3746 3751
11. JT Davie BA Clark M Häusser 2008 The origin of the complex spike in cerebellar Purkinje cells J Neurosci 28 7599 7609
12. C DeMontigny Y Lamarre 1973 Rhythmic activity induced by harmaline in the olivo-cerebello-bulbar system of the cat Brain Res 53 81 95
13. CI De Zeeuw JI Simpson CC Hoogenraad N Galjart SKE Koekkoek THJ Ruigrok 1998 Microcircuitry and function of the inferior olive Trends Neurosci 21 391 400
14. + channels in sustained high-frequency firing of fast-spiking neocortical interneurons J Neurophysiol 82 2476 2489
15. F Espinosa A McMahon E Chan S Wang CS Ho N Heintz RH Joho 2001 Alcohol hypersensitivity, increased locomotion, and spontaneous myoclonus in mice lacking the potassium channels Kv3.1 and Kv3.3 J Neurosci 21 6657 6665
16. F Espinosa GA Marks N Heintz RH Joho 2004 Increased motor drive and sleep loss in mice lacking Kv3-type potassium channels Genes Brain Behavior 3 90 100
17. F Espinosa MA Torres-Vega GA Marks RH Joho 2008 Ablation of Kv3.1 and Kv3.3 potassium channels disrupts thalamocortical oscillations in vitro and in vivo J Neurosci 28 5570 5581
18. SC Fowler BR Birkestrand R Chen SJ Moss E Vorontsova G Wang TJ Zarcone 2001 A force-plate actometer for quantitating rodent behaviors: illustrative data on locomotion, rotation, spatial pattering, stereotypies, and tremor J Neurosci Methods 107 107 124
19. M Fukuda T Yamamoto R Llinás 2001 The isochronic band hypothesis and climbing fibre regulation of motricity: an experimental study Europ J Neurosci 13 315 326
20. AR Gibson KM Horn M Pong 2002 Inhibitory control of olivary discharge Ann N Y Acad Sci 978 219 231
21. DS Goldman-Wohl E Chan D Baird N Heintz 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
22. Goldowitz D, Moran TH, Wetts R (1992) Mouse chimeras in the study of genetic and structural determinants of behavior. In: Goldowitz D, Wahlsten D, Wimer RE (eds) Techniques for the genetic analysis of brain and behavior. Elsevier, Amsterdam
23. A receptor activity Nat Neurosci 8 339 345
24. Hille B (2001) Ion channels of excitable membranes, 3rd edn. Sinauer, Sunderland
25. + channel gene: reduced body weight, impaired motor skills and muscle contraction, but no seizures Proc Natl Acad Sci USA 94 1533 1538
26. EC Hurlock A McMahon RH Joho 2008 Purkinje-cell-restricted restoration of Kv3.3 function restores complex spikes and rescues motor coordination in KCNC3 mutants J Neurosci 28 4640 4648
27. M Ito JI Simpson 1971 Discharges in Purkinje cells axons during climbing fiber activation Brain Res 31 215 219
28. RH Joho CS Ho GA Marks 1999 Increased gamma- and decreased delta-oscillations in a mouse deficient for a potassium channel expressed in fast-spiking interneurons J Neurophysiol 82 1855 1864
29. RH Joho C Street S Matsushita T Knöpfel 2006 Behavioral motor dysfunction in Kv3-type potassium channel-deficient mice Genes Brain Behavior 5 472 482
30. RH Joho GA Marks F Espinosa 2006 Kv3 potassium channels control the duration of different arousal states by distinct stochastic and clock-like mechanisms Europ J Neurosci 23 1567 1574
31. ZM Khaliq IM Raman 2005 Axonal propagation of simple and complex spikes in cerebellar Purkinje neurons J Neurosci 25 454 463
32. WM Kistler MTG De Jeu Y Elgersma RS van der Giessen R Hensbroek C Luo SKE Koekkoek CC Hoogenraad FPT Hamers M Gueldenagel G Sohl K Willecke CI De Zeeuw 2002 Analysis of Cx36 knockout does not support tenet that olivary gap junctions are required for complex spike synchronization and normal motor performance Ann N Y Acad Sci 978 391 404
33. ST Kitai RA McCrea RJ Preston GA Bishop 1977 Electrophysiological and horseradish peroxidase studies of precerebellar afferents to the nucleus interpositus anterior. I. Climbing fiber system Brain Res 122 197 214
34. + channel protein J Neurosci 20 9071 9085
35. G Laube J Röper JC Pitt S Sewing U Kistner CC Garner O Pongs RW Veh 1996 Ultrastructural localization of Shaker-related potassium channel subunits and synapse-associated protein 90 to septate-like junctions in rat cerebellar Pinceaux Mol Brain Res 42 51 61
36. CC Lien P Jonas 2003 Kv3 potassium conductance is necessary and kinetically optimized for high-frequency action potential generation in hippocampal interneurons J Neurosci 23 2058 2068
37. R Llinás 1974 Eighteenth Bowditch lecture: motor aspects of cerebellar control Physiol 17 19 26
38. RR Llinás 1988 The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function Sci 242 1654 1664
39. Llinás RR (1991) The noncontinuous nature of movement execution. In: Humphrey DR, Freund HJ (eds) Motor control, concepts and issues. Wiley, New York
40. R Llinás M Mühlenthaler 1988 Electrophysiology of guinea-pig cerebellar nuclear cells in in vitro brain-stem cerebellar preparation J Physiol (Lond.) 404 241 258
41. R Llinás RA Volkind 1973 The olivocerebellar system: functional properties as revealed by harmaline-induced tremor Exp Brain Res 18 69 87
42. MA Long MR Deans DL Paul BW Connors 2002 Rhythmicity without synchrony in the electrically uncoupled inferior olive J Neurosci 22 10898 10905
43. N Mano K Yamamoto 1980 Simple-spike activity of cerebellar Purkinje cells related to visually guided wrist tracking movement in the monkey J Neurophysiol 43 713 728
44. + channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus J Neurosci 18 8111 8125
45. M Martina GL Yao BP Bean 2003 Properties and functional role of voltage-dependent potassium channels in dendrites of rat cerebellar Purkinje neurons J Neurosci 23 5698 5707
46. H Matsukawa AM Wolf S Matsushita RH Joho T Knöpfel 2003 Motor dysfunction and altered synaptic transmission at the parallel fiber-Purkinje cell synapse in mice lacking the potassium channels Kv3.1 and Kv3.3 J Neurosci 23 7677 7684
47. RA McCrea GA Bishop ST Kitai 1977 Electrophysiological and horseradish peroxidase studies of precerebellar afferents to the nucleus interpositus anterior. II. Mossy fiber system Brain Res 122 215 228
48. + channels enable burst output in rat cerebellar Purkinje cells Europ J Neurosci 20 729 739
49. + channels control Purkinje cell output to facilitate postsynaptic rebound discharge in deep cerebellar neurons J Neurosci 25 1481 1492
50. A McMahon SC Fowler T Perney RH Joho 2004 Altered olivocerebellar circuit properties in the absence of the voltage-gated potassium channels Kv3.1 and Kv3.3 Europ J Neurosci 19 3317 3327
51. P Monsivais BA Clark A Roth M Häusser 2005 Determinants of action potential propagation in cerebellar Purkinje cell axons J Neurosci 25 464 472 (Pubitemid 40105617)
52. ML Molineux JE McRory BE McKay WH Mehaffey R Rehak TP Snutch GW Zamponi RW Turner 2006 Specific T-type calcium channel isoforms are associated with distinct burst phenotypes in deep cerebellar nuclear neurons Proc Natl Acad Sci USA 103 5555 5560
53. ML Molineux WH Mehaffey R Tadayonnejad D Anderson AF Tennent RW Turner 2008 Ionic factors governing rebound burst phenotype in rat deep cerebellar neurons J Neurophysiol 100 2684 2701
54. A Ozaita ME Martone MH Ellisman B Rudy 2002 Differential subcellular localization of the two alternatively spliced isoforms of the Kv3.1 potassium channel subunit in brain J Neurophysiol 88 394 408
55. CM Pedroarena C Schwarz 2003 Efficacy and short-term plasticity at GABAergic synapses between Purkinje and cerebellar nuclei neurons J Neurophysiol 89 704 715
56. TM Perney J Marshall KA Martin S Hockfield LK Kaczmarek 1992 Expression of the mRNAs for Kv3.1 potassium channel gene in the adult and developing rat brain J Neurophysiol 68 756 766
57. DG Placantonakis AA Bukovsky X-H Zeng H-P Kiem JP Welsh 2004 Fundamental role of inferior olive connexin 36 in muscle coherence during tremor Proc Natl Acad Sci USA 101 7164 7169
58. + channels designed for high-frequency repetitive firing Trends Neurosci 24 517 526
59. T Sacco A De Luca F Tempia 2006 Properties and expression of Kv3 channels in cerebellar Purkinje cells Mol Cell Neurosci 33 170 179
60. + channel-deficient mouse are not due to altered muscle excitability or fiber type but depend on the genetic background Pflügers Arch 440 34 41
61. MT Schmolesky JT Weber CI De Zeeuw C Hansel 2002 The making of a complex spike: ionic composition and plasticity Ann N Y Acad Sci 978 359 390
62. + channel subunit Kv3.1b in selected rat CNS neurons Brain Res 766 173 187
63. P Telgkamp IM Raman 2002 Depression of inhibitory synaptic transmission between Purkinje cells and neurons of the cerebellar nuclei J Neurosci 22 8447 8457
64. P Telgkamp DE Padgett VA Ledoux CS Wolley IM Raman 2004 Maintenance of high-frequency transmission at Purkinje to cerebellar nuclear synapses by spillover from boutons with multiple release sites Neuron 41 113 126
65. M Uusisaari K Obata T Knöpfel 2007 Morphological and electrophysiological properties of GABAergic and non-GABAergic cells in the deep cerebellar nuclei J Neurophysiol 97 901 911
66. VV Vyazovskiy T Deboer B Rudy D Lau AA Borbély I Tobler 2002 Sleep EEG in mice that are deficient in the potassium channel subunit Kv3.2 Brain Res 947 204 211
67. L-Y Wang L Gan ID Forsythe LK Kaczmarek 1998 Contribution of the Kv3.1 potassium channel to high-frequency firing in mouse auditory neurones J Physiol 509 183 194 (Pubitemid 28252021)
68. D Watanabe H Inokawa K Hashimoto N Suzuki M Kano R Shigemoto T Hirano K Toyama S Kaneko M Yokoi K Moriyoshi M Suzuki K Kobayashi T Nagatsu RJ Kreitman I Pastan S Nakanishi 1998 Ablation of cerebellar Golgi cells disrupts synaptic integration involving GABA inhibition and NMDA receptor activation in motor coordination Cell 95 17 27
69. MF Waters NA Minassian G Stevanin KP Figueroa JPA Bannister D Nolte AF Mock VG Evidente D Fee U Müller A Dürr A Brice DM Papazian SM Pulst 2006 Mutations in the voltage-gated potassium channel KCNC3 cause degenerative and developmental CNS phenotypes Nat Genet 38 447 451
70. + channels in the rat central nervous system J Neurosci 14 949 972
71. M Weiser E Bueno C Sekirnjak ME Martone H Baker D Hillman S Chen W Thornhill B Rudy 1995 The potassium channel subunit Kv3.1b is localized to somatic and axonal membranes of specific populations of CNS neurons J Neurosci 15 4298 4314
72. JP Welsh 2002 Functional significance of climbing-fiber synchrony. A population coding and behavioral analysis Ann NY Acad Sci 978 188 204
73. JP Welsh R Llinás 1997 Some organizing principles for the control of movement based on olivocerebellar physiology Prog Brain Res 114 449 461
74. JP Welsh EJ Lang I Sugihara R Llinás 1995 Dynamic organization of motor control within the olivocerebellar system Nature 374 453 457
75. + current in rat subthalamic nucleus neurons J Physiol 527 493 506
76. Y Yarom D Cohen 2002 The olivocerebellar system as a generator of temporal patterns Ann N Y Acad Sci 978 122 134
77. E Zagha EJ Lang B Rudy 2008 Kv3.3 channels at the Purkinje cell soma are necessary for generation of the classical complex spike waveform J Neurosci 28 1291 1300
78. W Zhang JH Shin DJ Linden 2004 Persistent changes in the intrinsic excitability of rat deep cerebellar nuclear neurons induced by EPSP or IPSP bursts J Physiol 561 3 703 719
79. T Zu LA Duvick MD Kaytor MS Berlinger HY Zoghbi HB Clark HT Orr 2004 Recovery from polyglutamine-induced neurodegeneration in conditional SCA1 transgenic mice J Neurosci 24 8853 8861