TY - JOUR T1 - Effect of stimulus-dependent spike timing on population coding of sound location in the owl’s auditory midbrain JF - eneuro JO - eNeuro DO - 10.1523/ENEURO.0244-19.2020 SP - ENEURO.0244-19.2020 AU - MV Beckert AU - BJ Fischer AU - JL Pena Y1 - 2020/03/13 UR - http://www.eneuro.org/content/early/2020/03/13/ENEURO.0244-19.2020.abstract N2 - 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 to 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.Significance Statement Spike timing of auditory neurons is modulated by the spectrotemporal structure of sounds. Whether this effect may have implications for coding of sound location remains unresolved. This question was approached in neurons of the owl’s midbrain, where temporal spiking patterns are modulated by the sound’s envelope while firing rate is driven by sound direction. We found that temporal patterns were dependent on binaural cues, leading to stimulus-dependent synchrony of nearby cells. Theoretical analysis showed that stimulus-dependent temporal patterning predicts stimulus-dependent synchrony in nearby cells sharing input with similar spectrotemporal structure, which in turn can sharpen the downstream readout of sound direction. This work shows how stimulus-dependent spike timing can affect the downstream coding of sound location by firing rate, a mechanism that can be generalized to sensory neurons sensitive to the temporal structure of the stimulus. ER -