Effect of Stimulus-Dependent Spike Timing on Population Coding of Sound Location in the Owl's Auditory Midbrain

In the auditory system, the spectrotemporal structure of acoustic signals determines the temporal pattern of spikes. Here, we investigated this effect in neurons of the barn owl's auditory midbrain (Tyto furcata) that are selective for auditory space and whether it can influence the coding of sound direction. We found that in the nucleus where neurons first become selective to combinations of sound localization cues, reproducibility of spike trains across repeated trials of identical sounds, a metric of across-trial temporal fidelity of spiking patterns evoked by a stimulus, was maximal at the sound direction that elicited the highest firing rate. We then tested the hypothesis that this stimulus-dependent patterning resulted in rate co-modulation of cells with similar frequency and spatial selectivity, driving stimulus-dependent synchrony of population responses. Tetrodes were used to simultaneously record multiple nearby units in the optic tectum (OT), where auditory space is topographically represented. While spiking of neurons in OT showed lower reproducibility across trials compared with upstream nuclei, spike-time synchrony between nearby OT neurons was highest for sounds at their preferred direction. A model of the midbrain circuit explained the relationship between stimulus-dependent reproducibility and synchrony, and demonstrated that this effect can improve the decoding of sound location from the OT output. Thus, stimulus-dependent spiking patterns in the auditory midbrain can have an effect on spatial coding. This study reports a functional connection between spike patterning elicited by spectrotemporal features of a sound and the coding of its location.