Modulation of potassium channels preserves temporal fidelity in auditory network models

Potassium channels in auditory neurons are rapidly modified by changes in the auditory environment. In response to elevated auditory stimulation, short-term mechanisms such as protein phosphorylation and long-term mechanisms linked to channel synthesis increase the activity of channels that promote high frequency firing. We have now used simple simulations of cochlear hair cells and postsynaptic neurons to demonstrate that the amplitudes of potassium currents in neurons required for optimal encoding of a low-level auditory signal differs substantially from that for louder sounds. Specifically, the cross correlation of the output of a neuron with an auditory stimulus is increased by increasing potassium currents as sound amplitude increases. Although it has been suggested that channel modulation allows neurons to fire at high rates in response to high sound levels, we found that the cross correlation is entirely independent of firing rate and that combinations of currents that maximize firing to a stimulus provide very poor temporal fidelity. We also found that levels of potassium currents that maximize the temporal fidelity of the output of an ensemble of thirty neurons differ from those that maximize temporal fidelity for a single neuron. This suggests that, to maximize preservation of temporal information, modulatory mechanisms must coordinate channel activity in groups of neurons receiving similar synaptic inputs. The simulations provide an explanation for the modulation of the intrinsic excitability of auditory brainstem neurons by changes in environmental sound levels, and the results may extend to information processing in other neural systems.