 |
Previous Article | Next Article 
The Journal of Neuroscience, January 1, 2000, 20(1):114-122
Electrophysiological Characterization of Voltage-Gated
K+ Currents in Cerebellar Basket and Purkinje Cells: Kv1
and Kv3 Channel Subfamilies Are Present in Basket Cell Nerve
Terminals
Andrew P.
Southan and
Brian
Robertson
Electrophysiology Group, Department of Biochemistry, Imperial
College of Science, Technology and Medicine, London SW7 2AY, United
Kingdom
To understand the processes underlying fast synaptic transmission
in the mammalian CNS, we must have detailed knowledge of the identity,
location, and physiology of the ion channels in the neuronal membrane.
From labeling studies we can get clues regarding the distribution of
ion channels, but electrophysiological methods are required to
determine the importance of each ion channel in CNS transmission.
Dendrotoxin-sensitive potassium channel subunits are highly
concentrated in cerebellar basket cell nerve terminals, and we have
previously shown that they are responsible for a significant fraction
of the voltage-gated potassium current in this region. Here, we further
investigate the characteristics and pharmacology of the
voltage-dependent potassium currents in these inhibitory nerve
terminals and compare these observations with those obtained from
somatic recordings in basket and Purkinje cell soma regions. We find
that -DTX blocks basket cell nerve terminal currents and not somatic
currents, and the IC50 for -DTX in basket cell terminals
is 3.2 nM. There are at least two distinct types of potassium currents in the nerve terminal, a DTX-sensitive low-threshold component, and a second component that activates at much more positive
voltages. Pharmacological experiments also reveal that nerve terminal
potassium currents are also markedly reduced by 4-AP and TEA, with both
high-sensitivity (micromolar) and low-sensitivity (millimolar)
components present. We suggest that basket cell nerve terminals have
potassium channels from both the Kv1 and Kv3 subfamilies, whereas
somatic currents in basket cell and Purkinje cell bodies are more homogeneous.
Key words:
potassium channels; cerebellum; synapse; basket cell; electrophysiology; mouse
Copyright © 2000 Society for Neuroscience 0270-6474/0/201114-09$05.00/0
This article has been cited by other articles:

|
 |

|
 |
 
B.-S. Chen, H. Peng, and S.-N. Wu
Dexmedetomidine, an {alpha}2-adrenergic agonist, inhibits neuronal delayed-rectifier potassium current and sodium current
Br. J. Anaesth.,
August 1, 2009;
103(2):
244 - 254.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Liu, T.-S. Tang, H. Tu, O. Nelson, E. Herndon, D. P. Huynh, S. M. Pulst, and I. Bezprozvanny
Deranged Calcium Signaling and Neurodegeneration in Spinocerebellar Ataxia Type 2
J. Neurosci.,
July 22, 2009;
29(29):
9148 - 9162.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Wang, N. C. Wong, Y. Cheng, S. J. Kehl, and D. Fedida
Control of voltage-gated K+ channel permeability to NMDG+ by a residue at the outer pore
J. Gen. Physiol.,
April 1, 2009;
133(4):
361 - 374.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Lorincz and Z. Nusser
Cell-Type-Dependent Molecular Composition of the Axon Initial Segment
J. Neurosci.,
December 31, 2008;
28(53):
14329 - 14340.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Zagha, E. J. Lang, and B. Rudy
Kv3.3 Channels at the Purkinje Cell Soma Are Necessary for Generation of the Classical Complex Spike Waveform
J. Neurosci.,
February 6, 2008;
28(6):
1291 - 1300.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Wang, B. Robertson, and D. Fedida
Gating currents from a Kv3 subfamily potassium channel: charge movement and modification by BDS-II toxin
J. Physiol.,
November 1, 2007;
584(3):
755 - 767.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Shu, Y. Yu, J. Yang, and D. A. McCormick
Selective control of cortical axonal spikes by a slowly inactivating K+ current
PNAS,
July 3, 2007;
104(27):
11453 - 11458.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. E. Metz, N. Spruston, and M. Martina
Dendritic D-type potassium currents inhibit the spike afterdepolarization in rat hippocampal CA1 pyramidal neurons
J. Physiol.,
May 15, 2007;
581(1):
175 - 187.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Martina, A. E. Metz, and B. P. Bean
Voltage-Dependent Potassium Currents During Fast Spikes of Rat Cerebellar Purkinje Neurons: Inhibition by BDS-I Toxin
J Neurophysiol,
January 1, 2007;
97(1):
563 - 571.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. Guan, J. C. F. Lee, T. Tkatch, D. J. Surmeier, W. E. Armstrong, and R. C. Foehring
Expression and biophysical properties of Kv1 channels in supragranular neocortical pyramidal neurones
J. Physiol.,
March 1, 2006;
571(2):
371 - 389.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. M. Khaliq and I. M. Raman
Relative Contributions of Axonal and Somatic Na Channels to Action Potential Initiation in Cerebellar Purkinje Neurons
J. Neurosci.,
February 15, 2006;
26(7):
1935 - 1944.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Khavandgar, J. T. Walter, K. Sageser, and K. Khodakhah
Kv1 channels selectively prevent dendritic hyperexcitability in rat Purkinje cells
J. Physiol.,
December 1, 2005;
569(2):
545 - 557.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Y. M. Yeung, D. Thompson, Z. Wang, D. Fedida, and B. Robertson
Modulation of Kv3 Subfamily Potassium Currents by the Sea Anemone Toxin BDS: Significance for CNS and Biophysical Studies
J. Neurosci.,
September 21, 2005;
25(38):
8735 - 8745.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Chen, W. Gao, K. C. Reinert, L. S. Popa, C. M. Hendrix, M. E. Ross, and T. J. Ebner
Involvement of Kv1 Potassium Channels in Spreading Acidification and Depression in the Cerebellar Cortex
J Neurophysiol,
August 1, 2005;
94(2):
1287 - 1298.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. M. Goldberg, S. Watanabe, S. Y. Chang, R. H. Joho, Z. J. Huang, C. S. Leonard, and B. Rudy
Specific Functions of Synaptically Localized Potassium Channels in Synaptic Transmission at the Neocortical GABAergic Fast-Spiking Cell Synapse
J. Neurosci.,
May 25, 2005;
25(21):
5230 - 5235.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. M. Swensen and B. P. Bean
Robustness of Burst Firing in Dissociated Purkinje Neurons with Acute or Long-Term Reductions in Sodium Conductance
J. Neurosci.,
April 6, 2005;
25(14):
3509 - 3520.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. E. McKay, M. L. Molineux, W. H. Mehaffey, and R. W. Turner
Kv1 K+ Channels Control Purkinje Cell Output to Facilitate Postsynaptic Rebound Discharge in Deep Cerebellar Neurons
J. Neurosci.,
February 9, 2005;
25(6):
1481 - 1492.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. L Dallas, L. Atkinson, C. J Milligan, N. P Morris, D. I Lewis, S. A Deuchars, and J. Deuchars
Localization and function of the Kv3.1b subunit in the rat medulla oblongata: focus on the nucleus tractus solitarii
J. Physiol.,
February 1, 2005;
562(3):
655 - 672.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. M. Khaliq and I. M. Raman
Axonal Propagation of Simple and Complex Spikes in Cerebellar Purkinje Neurons
J. Neurosci.,
January 12, 2005;
25(2):
454 - 463.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Shen, S. Hernandez-Lopez, T. Tkatch, J. E. Held, and D. J. Surmeier
Kv1.2-Containing K+ Channels Regulate Subthreshold Excitability of Striatal Medium Spiny Neurons
J Neurophysiol,
March 1, 2004;
91(3):
1337 - 1349.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Ishikawa, Y. Nakamura, N. Saitoh, W.-B. Li, S. Iwasaki, and T. Takahashi
Distinct Roles of Kv1 and Kv3 Potassium Channels at the Calyx of Held Presynaptic Terminal
J. Neurosci.,
November 12, 2003;
23(32):
10445 - 10453.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. M. Swensen and B. P. Bean
Ionic Mechanisms of Burst Firing in Dissociated Purkinje Neurons
J. Neurosci.,
October 22, 2003;
23(29):
9650 - 9663.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Martina, G. L. Yao, and B. P. Bean
Properties and Functional Role of Voltage-Dependent Potassium Channels in Dendrites of Rat Cerebellar Purkinje Neurons
J. Neurosci.,
July 2, 2003;
23(13):
5698 - 5707.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. D Dodson, B. Billups, Z. Rusznak, G. Szucs, M. C Barker, and I. D Forsythe
Presynaptic rat Kv1.2 channels suppress synaptic terminal hyperexcitability following action potential invasion
J. Physiol.,
July 1, 2003;
550(1):
27 - 33.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. M. Khaliq, N. W. Gouwens, and I. M. Raman
The Contribution of Resurgent Sodium Current to High-Frequency Firing in Purkinje Neurons: An Experimental and Modeling Study
J. Neurosci.,
June 15, 2003;
23(12):
4899 - 4912.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. M Brew, J. L Hallows, and B. L Tempel
Hyperexcitability and reduced low threshold potassium currents in auditory neurons of mice lacking the channel subunit Kv1.1
J. Physiol.,
April 1, 2003;
548(1):
1 - 20.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. J. Ebner and G. Chen
Spreading Acidification and Depression in the Cerebellar Cortex
Neuroscientist,
February 1, 2003;
9(1):
37 - 45.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Sacco and F. Tempia
A-Type potassium currents active at subthreshold potentials in mouse cerebellar purkinje cells
J. Physiol.,
September 1, 2002;
543(2):
505 - 520.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. D. Dodson, M. C. Barker, and I. D. Forsythe
Two Heteromeric Kv1 Potassium Channels Differentially Regulate Action Potential Firing
J. Neurosci.,
August 15, 2002;
22(16):
6953 - 6961.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z.-L. Mo, C. L Adamson, and R. L Davis
Dendrotoxin-sensitive K+ currents contribute to accommodation in murine spiral ganglion neurons
J. Physiol.,
August 1, 2002;
542(3):
763 - 778.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. Maylie, E. Bissonnette, M. Virk, J. P. Adelman, and J. G. Maylie
Episodic Ataxia Type 1 Mutations in the Human Kv1.1 Potassium Channel Alter hKvbeta 1-Induced N-Type Inactivation
J. Neurosci.,
June 15, 2002;
22(12):
4786 - 4793.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. A. Cingolani, M. Gymnopoulos, A. Boccaccio, M. Stocker, and P. Pedarzani
Developmental Regulation of Small-Conductance Ca2+-Activated K+ Channel Expression and Function in Rat Purkinje Neurons
J. Neurosci.,
June 1, 2002;
22(11):
4456 - 4467.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Cavelier, F. Pouille, T. Desplantez, H. Beekenkamp, and J.-L. Bossu
Control of the propagation of dendritic low-threshold Ca2+ spikes in Purkinje cells from rat cerebellar slice cultures
J. Physiol.,
April 1, 2002;
540(1):
57 - 72.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C.-C. Lien, M. Martina, J. H Schultz, H. Ehmke, and P. Jonas
Gating, modulation and subunit composition of voltage-gated K+ channels in dendritic inhibitory interneurones of rat hippocampus
J. Physiol.,
January 15, 2002;
538(2):
405 - 419.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Mann-Metzer and Y. Yarom
Jittery Trains Induced by Synaptic-Like Currents in Cerebellar Inhibitory Interneurons
J Neurophysiol,
January 1, 2002;
87(1):
149 - 156.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. K. Lambe and G. K. Aghajanian
The Role of Kv1.2-Containing Potassium Channels in Serotonin-Induced Glutamate Release from Thalamocortical Terminals in Rat Frontal Cortex
J. Neurosci.,
December 15, 2001;
21(24):
9955 - 9963.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Bal and D. Oertel
Potassium Currents in Octopus Cells of the Mammalian Cochlear Nucleus
J Neurophysiol,
November 1, 2001;
86(5):
2299 - 2311.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Ishikawa and T. Takahashi
Mechanisms underlying presynaptic facilitatory effect of cyclothiazide at the calyx of Held of juvenile rats
J. Physiol.,
June 1, 2001;
533(2):
423 - 431.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. P Southan, N. P Morris, G. J Stephens, and B. Robertson
Hyperpolarization-activated currents in presynaptic terminals of mouse cerebellar basket cells
J. Physiol.,
July 1, 2000;
526(1):
91 - 97.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|