Differential regulation of action potential firing in adult murine thalamocortical neurons by Kv3.2, Kv1, and SK potassium and N-type calcium channels

J Physiol. 2007 Oct 15;584(Pt 2):565-82. doi: 10.1113/jphysiol.2007.141135. Epub 2007 Aug 30.

Abstract

Sensory signals of widely differing dynamic range and intensity are transformed into a common firing rate code by thalamocortical neurons. While a great deal is known about the ionic currents, far less is known about the specific channel subtypes regulating thalamic firing rates. We hypothesized that different K(+) and Ca(2+) channel subtypes control different stimulus-response curve properties. To define the channels, we measured firing rate while pharmacologically or genetically modulating specific channel subtypes. Inhibiting Kv3.2 K(+) channels strongly suppressed maximum firing rate by impairing membrane potential repolarization, while playing no role in the firing response to threshold stimuli. By contrast, inhibiting Kv1 channels with alpha-dendrotoxin or maurotoxin strongly increased firing rates to threshold stimuli by reducing the membrane potential where action potentials fire (V(th)). Inhibiting SK Ca(2+)-activated K(+) channels with apamin robustly increased gain (slope of the stimulus-response curve) and maximum firing rate, with minimum effects on threshold responses. Inhibiting N-type Ca(2+) channels with omega-conotoxin GVIA or omega-conotoxin MVIIC partially mimicked apamin, while inhibiting L-type and P/Q-type Ca(2+) channels had small or no effects. EPSC-like current injections closely mimicked the results from tonic currents. Our results show that Kv3.2, Kv1, SK potassium and N-type calcium channels strongly regulate thalamic relay neuron sensory transmission and that each channel subtype controls a different stimulus-response curve property. Differential regulation of threshold, gain and maximum firing rate may help vary the stimulus-response properties across and within thalamic nuclei, normalize responses to diverse sensory inputs, and underlie sensory perception disorders.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials
  • Age Factors
  • Aging / metabolism
  • Animals
  • Calcium Channel Blockers / pharmacology
  • Calcium Channels, L-Type / metabolism
  • Calcium Channels, N-Type / metabolism*
  • Calcium Channels, T-Type / genetics
  • Calcium Channels, T-Type / metabolism
  • Electric Stimulation
  • Excitatory Postsynaptic Potentials
  • KATP Channels / metabolism
  • KCNQ Potassium Channels / metabolism
  • Kinetics
  • Large-Conductance Calcium-Activated Potassium Channels / metabolism
  • Membrane Potentials
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neurons / drug effects
  • Neurons / metabolism*
  • Potassium Channel Blockers / pharmacology
  • Sensation / physiology*
  • Sensory Thresholds
  • Shaker Superfamily of Potassium Channels / antagonists & inhibitors
  • Shaker Superfamily of Potassium Channels / metabolism*
  • Shaw Potassium Channels / antagonists & inhibitors
  • Shaw Potassium Channels / deficiency
  • Shaw Potassium Channels / genetics
  • Shaw Potassium Channels / metabolism*
  • Small-Conductance Calcium-Activated Potassium Channels / antagonists & inhibitors
  • Small-Conductance Calcium-Activated Potassium Channels / metabolism*
  • Thalamus / cytology
  • Thalamus / drug effects
  • Thalamus / metabolism*

Substances

  • Cacna1g protein, mouse
  • Calcium Channel Blockers
  • Calcium Channels, L-Type
  • Calcium Channels, N-Type
  • Calcium Channels, T-Type
  • KATP Channels
  • KCNQ Potassium Channels
  • Large-Conductance Calcium-Activated Potassium Channels
  • Potassium Channel Blockers
  • Shaker Superfamily of Potassium Channels
  • Shaw Potassium Channels
  • Small-Conductance Calcium-Activated Potassium Channels
  • voltage-dependent calcium channel (P-Q type)