Abstract

Ultrafast and temporally precise action potentials (APs) are biophysical specializations of auditory brainstem neurons; properties necessary for encoding sound localization and communication cues. Fundamental to these specializations are voltage dependent potassium (KV) and sodium (NaV) ion channels. Here, we characterized the functional development of these ion channels and quantified how they shape AP properties in the avian cochlear nucleus magnocellularis (NM). We report that late developing NM neurons (embryonic [E] days 19–21) generate fast APs that reliably phase lock to sinusoidal inputs at 75 Hz. In contrast, early developing neurons (<E12) have slower and less reliable APs that preferentially fire to lower frequencies (5–10 Hz). With development, the membrane time constant of NM neurons became faster, while input resistance and capacitance decreased. Change in input resistance was due to a 2-fold increase in KV current from E10 to E21 and when high-voltage activated potassium (K+HVA) channels were blocked, APs for all ages became significantly slower. This was most evident for early developing neurons where the ratio of K+HVA current accounted for ~85% of the total KV response. This ratio dropped to ~50% for late developing neurons, suggesting a developmental upregulation of low-voltage activated potassium (K+LVA) channels. Indeed, blockade of K+LVA eliminated remaining current and increased neural excitability for late developing neurons. We also report developmental changes in the amplitude, kinetics and voltage dependence of NaV currents. For early developing neurons, increase in NaV current amplitude was due to channel density while channel conductance dominated for late developing neurons. From E10 to E21, NaV channel currents became faster but differed in their voltage dependence; early developing neurons (<E16) had similar NaV channel inactivation voltages while late developing NM neurons (>E19) contained NaV channels that inactivate at more negative voltages, suggesting alterations in NaV channel subtypes. Taken together, our results indicate that the refinement of passive and active ion channel properties operate differentially in order to develop fast and reliable APs in the avian NM.

Highlights

  • Auditory temporal processing, or the ability to rapidly encode acoustic information in time, is a specialized ability of auditory brainstem neurons

  • A biophysical hallmark of many time-coding auditory brainstem neurons is the generation of a single onset action potentials (APs) in response to a sustained depolarizing somatic current injection (Oertel, 1983; Reyes et al, 1994)

  • These results suggest that K+HVA channels differentially regulate AP kinetics in developing nucleus magnocellularis (NM) neurons and that this difference is reflected in the relative current amounts of K+HVA for each age group

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Summary

Introduction

The ability to rapidly encode acoustic information in time, is a specialized ability of auditory brainstem neurons (for review, see Oertel, 1997; Trussell, 1997) It provides the framework for normal and abnormal hearing behaviors (Michalewski et al, 2005) and is critical for survival and communication, such as sound localization and understanding speech in noise (Shannon et al, 1995; Anderson et al, 2010). In order to accurately encode temporal information of sound, auditory brainstem neurons are functionally primed to generate ultrafast and temporally precise action potentials (APs). Such AP properties are conserved in the auditory brainstem of both avians and mammals (Carr et al, 2001). In order to accomplish this specialized function, neurons from the avian nucleus magnocellularis (NM) and the mammalian analog, the anteroventral cochlear nucleus (AVCN), must provide fast and reliable excitatory inputs to their downstream binaural circuit

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