Properties and functional role of voltage-dependent potassium channels in dendrites of rat cerebellar Purkinje neurons

Marco Martina, Gui Lan Yao, Bruce P. Bean*

*Corresponding author for this work

Research output: Contribution to journalArticle

97 Citations (Scopus)

Abstract

We characterized the properties and functional roles of voltage-dependent potassium channels in the dendrites of Purkinje neurons studied in rat cerebellar slices. Using outside-out patches formed ≤250 μm away from the soma, we found that depolarization-activated potassium channels were present at high density throughout the dendritic tree. Currents required relatively large depolarizations for activation (midpoint, approximately - 10 mV), had rapid activation and deactivation kinetics, and inactivated partially (20-70% over 200 msec) with both fast (time constant, 15-20 msec) and slow (300-400 msec) components. Inactivating and noninactivating components were both blocked potently by external tetraethylammonium (half-block by 150 μM) and 4-aminopyridine (half-block by 110 μM). The voltage dependence, kinetics, and pharmacology suggest a predominant contribution by Kv3 family subunits, and immunocytochemical experiments showed staining for both Kv3.3 and Kv3.4 subunits in the dendritic tree. In the proximal dendrite, potassium channels were activated by passively spread sodium spikes recorded at the same position, and experiments using dual recordings showed that the channels serve to actively dampen back-propagation of somatic sodium spikes. In more distal dendrites, potassium currents were activated by voltage waveforms taken from climbing fiber responses, suggesting that they help shape these responses as well. The requirement for large depolarizations allows dendritic Kv3 channels to shape large depolarizing events while not disrupting spatial and temporal summation of smaller excitatory postsynaptic potentials.

Original languageEnglish (US)
Pages (from-to)5698-5707
Number of pages10
JournalJournal of Neuroscience
Volume23
Issue number13
StatePublished - Jul 1 2003

Fingerprint

Purkinje Cells
Potassium Channels
Dendrites
Sodium
4-Aminopyridine
Tetraethylammonium
Excitatory Postsynaptic Potentials
Carisoprodol
Potassium
Pharmacology
Staining and Labeling

Keywords

  • 4-aminopyridine
  • Climbing fiber
  • Kv3
  • Kv3.3
  • Kv3.4
  • Purkinje cell
  • Tetraethylammonium

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

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title = "Properties and functional role of voltage-dependent potassium channels in dendrites of rat cerebellar Purkinje neurons",
abstract = "We characterized the properties and functional roles of voltage-dependent potassium channels in the dendrites of Purkinje neurons studied in rat cerebellar slices. Using outside-out patches formed ≤250 μm away from the soma, we found that depolarization-activated potassium channels were present at high density throughout the dendritic tree. Currents required relatively large depolarizations for activation (midpoint, approximately - 10 mV), had rapid activation and deactivation kinetics, and inactivated partially (20-70{\%} over 200 msec) with both fast (time constant, 15-20 msec) and slow (300-400 msec) components. Inactivating and noninactivating components were both blocked potently by external tetraethylammonium (half-block by 150 μM) and 4-aminopyridine (half-block by 110 μM). The voltage dependence, kinetics, and pharmacology suggest a predominant contribution by Kv3 family subunits, and immunocytochemical experiments showed staining for both Kv3.3 and Kv3.4 subunits in the dendritic tree. In the proximal dendrite, potassium channels were activated by passively spread sodium spikes recorded at the same position, and experiments using dual recordings showed that the channels serve to actively dampen back-propagation of somatic sodium spikes. In more distal dendrites, potassium currents were activated by voltage waveforms taken from climbing fiber responses, suggesting that they help shape these responses as well. The requirement for large depolarizations allows dendritic Kv3 channels to shape large depolarizing events while not disrupting spatial and temporal summation of smaller excitatory postsynaptic potentials.",
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Properties and functional role of voltage-dependent potassium channels in dendrites of rat cerebellar Purkinje neurons. / Martina, Marco; Yao, Gui Lan; Bean, Bruce P.

In: Journal of Neuroscience, Vol. 23, No. 13, 01.07.2003, p. 5698-5707.

Research output: Contribution to journalArticle

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N2 - We characterized the properties and functional roles of voltage-dependent potassium channels in the dendrites of Purkinje neurons studied in rat cerebellar slices. Using outside-out patches formed ≤250 μm away from the soma, we found that depolarization-activated potassium channels were present at high density throughout the dendritic tree. Currents required relatively large depolarizations for activation (midpoint, approximately - 10 mV), had rapid activation and deactivation kinetics, and inactivated partially (20-70% over 200 msec) with both fast (time constant, 15-20 msec) and slow (300-400 msec) components. Inactivating and noninactivating components were both blocked potently by external tetraethylammonium (half-block by 150 μM) and 4-aminopyridine (half-block by 110 μM). The voltage dependence, kinetics, and pharmacology suggest a predominant contribution by Kv3 family subunits, and immunocytochemical experiments showed staining for both Kv3.3 and Kv3.4 subunits in the dendritic tree. In the proximal dendrite, potassium channels were activated by passively spread sodium spikes recorded at the same position, and experiments using dual recordings showed that the channels serve to actively dampen back-propagation of somatic sodium spikes. In more distal dendrites, potassium currents were activated by voltage waveforms taken from climbing fiber responses, suggesting that they help shape these responses as well. The requirement for large depolarizations allows dendritic Kv3 channels to shape large depolarizing events while not disrupting spatial and temporal summation of smaller excitatory postsynaptic potentials.

AB - We characterized the properties and functional roles of voltage-dependent potassium channels in the dendrites of Purkinje neurons studied in rat cerebellar slices. Using outside-out patches formed ≤250 μm away from the soma, we found that depolarization-activated potassium channels were present at high density throughout the dendritic tree. Currents required relatively large depolarizations for activation (midpoint, approximately - 10 mV), had rapid activation and deactivation kinetics, and inactivated partially (20-70% over 200 msec) with both fast (time constant, 15-20 msec) and slow (300-400 msec) components. Inactivating and noninactivating components were both blocked potently by external tetraethylammonium (half-block by 150 μM) and 4-aminopyridine (half-block by 110 μM). The voltage dependence, kinetics, and pharmacology suggest a predominant contribution by Kv3 family subunits, and immunocytochemical experiments showed staining for both Kv3.3 and Kv3.4 subunits in the dendritic tree. In the proximal dendrite, potassium channels were activated by passively spread sodium spikes recorded at the same position, and experiments using dual recordings showed that the channels serve to actively dampen back-propagation of somatic sodium spikes. In more distal dendrites, potassium currents were activated by voltage waveforms taken from climbing fiber responses, suggesting that they help shape these responses as well. The requirement for large depolarizations allows dendritic Kv3 channels to shape large depolarizing events while not disrupting spatial and temporal summation of smaller excitatory postsynaptic potentials.

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