Wide-ranging Frequency Preferences of Auditory Midbrain Neurons: Roles of Membrane Time Constant and Synaptic Properties

Eur J Neurosci. 2009 Jul;30(1):76-90. doi: 10.1111/j.1460-9568.2009.06797.x. Epub 2009 Jun 25.

Abstract

Periodicity is a fundamental sound attribute. Its coding has been the subject of intensive research, most of which has focused on investigating how the periodicity of sounds is processed through the synaptic machinery in the brain. The extent to which the intrinsic properties of cells play in periodicity coding, particularly in the creation of selectivity to periodic signals, is not well understood. We performed in vitro whole-cell patch recordings in the frog torus semicircularis to investigate each neuron's intrinsic membrane properties as well as responses to sinusoidal current injected through the electrode and periodic stimulation of the ascending afferent. We found that: (i) toral neurons were heterogeneous, showing diverse biophysical phenotypes having distinct membrane characteristics, including membrane time constants (tau) and ionic channel compositions (I(h), I(kir), I(kv) and I(NaP)); (ii) a neuron's tau was tightly correlated with its current-evoked frequency preference (FP; range: 0.05-50 Hz); (iii) application of blockers for I(h), I(kir) and I(kv) (but not I(NaP)) shifted the tau as well as the cell's current-evoked FP, suggesting that these ion channels contribute to the cell's FP through regulation of tau; (iv) a neuron's tau was also correlated with its afferent-evoked FP (range: 10-300 pulses/s); and (v) the range of afferent-evoked FP was approximately one order higher than the range of current-evoked FPs, suggesting that both the cell's intrinsic membrane and synaptic properties contribute to determining the afferent-evoked cell-specific FP (whose range matched those of cell-specific responses to sound stimulation, e.g. selectivity to amplitude modulation rate).

Publication types

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

MeSH terms

  • Animals
  • Auditory Perception / physiology*
  • Cell Membrane / drug effects
  • Cell Membrane / physiology*
  • Electric Stimulation
  • Evoked Potentials, Auditory, Brain Stem / drug effects
  • In Vitro Techniques
  • Ion Channels / metabolism
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Mesencephalon / drug effects
  • Mesencephalon / physiology*
  • Neurons / drug effects
  • Neurons / physiology*
  • Neurons, Afferent / physiology
  • Patch-Clamp Techniques
  • Periodicity*
  • Rana pipiens
  • Synapses / drug effects
  • Synapses / physiology*
  • Synaptic Transmission / physiology
  • Time Factors

Substances

  • Ion Channels