Specific and rapid effects of acoustic stimulation on the tonotopic distribution of Kv3.1b potassium channels in the adult rat

Neuroscience. 2010 May 19;167(3):567-72. doi: 10.1016/j.neuroscience.2010.02.046. Epub 2010 Feb 26.

Abstract

Recent studies have demonstrated that total cellular levels of voltage-gated potassium channel subunits can change on a time scale of minutes in acute slices and cultured neurons, raising the possibility that rapid changes in the abundance of channel proteins contribute to experience-dependent plasticity in vivo. In order to investigate this possibility, we took advantage of the medial nucleus of the trapezoid body (MNTB) sound localization circuit, which contains neurons that precisely phase-lock their action potentials to rapid temporal fluctuations in the acoustic waveform. Previous work has demonstrated that the ability of these neurons to follow high-frequency stimuli depends critically upon whether they express adequate amounts of the potassium channel subunit Kv3.1. To test the hypothesis that net amounts of Kv3.1 protein would be rapidly upregulated when animals are exposed to sounds that require high frequency firing for accurate encoding, we briefly exposed adult rats to acoustic environments that varied according to carrier frequency and amplitude modulation (AM) rate. Using an antibody directed at the cytoplasmic C-terminus of Kv3.1b (the adult splice isoform of Kv3.1), we found that total cellular levels of Kv3.1b protein-as well as the tonotopic distribution of Kv3.1b-labeled cells-was significantly altered following 30 min of exposure to rapidly modulated (400 Hz) sounds relative to slowly modulated (0-40 Hz, 60 Hz) sounds. These results provide direct evidence that net amounts of Kv3.1b protein can change on a time scale of minutes in response to stimulus-driven synaptic activity, permitting auditory neurons to actively adapt their complement of ion channels to changes in the acoustic environment.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acoustic Stimulation
  • Adaptation, Physiological / physiology
  • Animals
  • Antibody Specificity
  • Auditory Pathways / cytology
  • Auditory Pathways / metabolism*
  • Auditory Threshold / physiology
  • Immunohistochemistry / methods
  • Ion Channel Gating / physiology
  • Nerve Tissue Proteins / metabolism*
  • Neuronal Plasticity / physiology*
  • Rats
  • Rats, Sprague-Dawley
  • Reaction Time / physiology
  • Rhombencephalon / cytology
  • Rhombencephalon / metabolism*
  • Shaw Potassium Channels / metabolism*
  • Sound Localization / physiology*
  • Synaptic Transmission / physiology
  • Time Factors
  • Up-Regulation / physiology

Substances

  • Kcnc1 protein, rat
  • Nerve Tissue Proteins
  • Shaw Potassium Channels