It's About Time: How Input Timing Is Used and Not Used To Create Emergent Properties in the Auditory System

Abstract

The hypothesis for directional selectivity of frequency modulations (FMs) invokes a mechanism with an honored tradition in sensory neurobiology, the relative timing of excitation and inhibition. The proposal is that the timing disparity is created by asymmetrical locations of excitatory tuning and inhibitory sidebands. Thus, cells in which the inhibitory sidebands are tuned to frequencies lower than the excitatory tuning are selective for downward sweeping FMs, because frequencies first generate excitation followed by inhibition. Upward sweeping FMs, in contrast, first evoke inhibition that either leads or is coincident with the excitation and prevents discharges. Here we evaluated FM directional selectivity with in vivo whole-cell recordings from the inferior colliculus of awake bats. From the whole-cell recordings, we derived synaptic conductance waveforms evoked by downward and upward FMs. We then tested the effects of shifting inhibition relative to excitation in a model and found that latency shifts had only minor effects on EPSP amplitudes that were often <1.0 mV/ms shift. However, when the PSPs peaked close to spike threshold, even small changes in latency could cause some cells to fire more strongly to a particular FM direction and thus change its directional selectivity. Furthermore, the effect of shifting inhibition depended strongly on initial latency differences and the shapes of the conductance waveforms. We conclude that "timing" is more than latency differences between excitation and inhibition, and response selectivity depends on a complex interaction between the timing, the shapes, and magnitudes of the excitatory and inhibitory conductances and spike threshold.