Elsevier

Neuroscience

Volume 167, Issue 3, 19 May 2010, Pages 567-572
Neuroscience

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

https://doi.org/10.1016/j.neuroscience.2010.02.046Get rights and content

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.

Section snippets

Acoustic stimulation

Twenty-seven awake adult (8–12 week-old) Sprague–Dawley rats (Charles River Laboratories, Wilmington, MA, USA) were exposed to amplitude modulation (AM) stimuli for a 30 min period at 65 dB sound pressure level (SPL) in a small sound attenuating chamber. All experimental protocols involving animals were approved by the Yale University Animal Use and Care Committee. Protocols were carefully designed to minimize both the number of animals used and their suffering. A total of six stimuli were used

Results

In vivo single-unit studies have demonstrated that MNTB principal neurons synchronize their action potentials to the phase of AM sound stimuli across a wide range of modulation rates (Joris and Yin, 1998, Kadner and Berrebi, 2008, Kopp-Scheinpflug et al., 2008), making it possible to precisely control their activity patterns in vivo by exposing animals to AM sounds. In vitro, MNTB neurons from animals lacking the Kv3.1 gene can readily follow 60 Hz stimulation, but are incapable of following

Discussion

The amount of Kv3.1b current in an MNTB principal neuron determines its ability to follow high rates of synaptic stimulation (Macica et al., 2003, Song et al., 2005). One established mechanism by which Kv3.1b currents become enhanced to permit high frequency firing is through dephosphorylation at Ser503 (Macica et al., 2003). Whereas Kv3.1b is basally phosphorylated at Ser503 under quiet/control conditions, it undergoes dephosphorylation following seconds to minutes of auditory stimulation in

Acknowledgments

This work was supported by National Institutes of Health (NIH) grants DC001919 (L.K.K.) and DC009488 (D.B.P.). We thank Gregory Derderian for technical assistance and Christian von Hehn for critical reading of the manuscript.

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    Present address: Eaton-Peabody Laboratory, Massachusetts Eye and Ear Infirmary, Boston, MA 02114, USA.

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