A-type voltage-gated K+ currents influence firing properties of isolectin B4-positive but not isolectin B4-negative primary sensory neurons

J Neurophysiol. 2005 Jun;93(6):3401-9. doi: 10.1152/jn.01267.2004. Epub 2005 Jan 12.

Abstract

Voltage-gated K+ channels (Kv) in primary sensory neurons are important for regulation of neuronal excitability. The dorsal root ganglion (DRG) neurons are heterogeneous, and the types of native Kv currents in different groups of nociceptive DRG neurons are not fully known. In this study, we determined the difference in the A-type Kv current and its influence on the firing properties between isolectin B4 (IB4)-positive and -negative DRG neurons. Whole cell voltage- and current-clamp recordings were performed on acutely dissociated small DRG neurons of rats. The total Kv current density was significantly higher in IB+-positive than that in IB(4)-negative neurons. Also, 4-aminopyridine (4-AP) produced a significantly greater reduction in Kv currents in IB4-positive than in IB4-negative neurons. In contrast, IB4-negative neurons exhibited a larger proportion of tetraethylammonium-sensitive Kv currents. Furthermore, IB4-positive neurons showed a longer latency of firing and required a significantly larger amount of current injection to evoke action potentials. 4-AP significantly decreased the latency of firing and increased the firing frequency in IB4-positive but not in IB4-negative neurons. Additionally, IB4-positive neurons are immunoreactive to Kv1.4 but not to Kv1.1 and Kv1.2 subunits. Collectively, this study provides new information that 4-AP-sensitive A-type Kv currents are mainly present in IB4-positive DRG neurons and preferentially dampen the initiation of action potentials of this subpopulation of nociceptors. The difference in the density of A-type Kv currents contributes to the distinct electrophysiological properties of IB4-positive and -negative DRG neurons.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • 4-Aminopyridine / pharmacology
  • Animals
  • Animals, Newborn
  • Cells, Cultured
  • Electric Stimulation / methods
  • Ganglia, Spinal / cytology*
  • Immunohistochemistry / methods
  • Ion Channel Gating / drug effects
  • Ion Channel Gating / physiology
  • KCNQ Potassium Channels
  • KCNQ1 Potassium Channel
  • Male
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology*
  • Membrane Potentials / radiation effects
  • Neural Inhibition / drug effects
  • Neural Inhibition / radiation effects
  • Neurons, Afferent / classification
  • Neurons, Afferent / physiology*
  • Patch-Clamp Techniques / methods
  • Plant Lectins / metabolism*
  • Plant Lectins / pharmacology
  • Potassium Channel Blockers / pharmacology
  • Potassium Channels, Voltage-Gated / drug effects
  • Potassium Channels, Voltage-Gated / physiology*
  • Potassium Channels, Voltage-Gated / radiation effects
  • Rats
  • Rats, Sprague-Dawley
  • Tetraethylammonium / pharmacology

Substances

  • KCNQ Potassium Channels
  • KCNQ1 Potassium Channel
  • Kcnq1 protein, rat
  • Plant Lectins
  • Potassium Channel Blockers
  • Potassium Channels, Voltage-Gated
  • Tetraethylammonium
  • 4-Aminopyridine