Accurate Sound Localization in Reverberant Environments Is Mediated by Robust Encoding of Spatial Cues in the Auditory Midbrain

Abstract

In reverberant environments, acoustic reflections interfere with the direct sound arriving at a listener’s ears, distorting the spatial cues for sound localization. Yet, human listeners have little difficulty localizing sounds in most settings. Because reverberant energy builds up over time, the source location is represented relatively faithfully during the early portion of a sound, but this representation becomes increasingly degraded later in the stimulus. We show that the directional sensitivity of single neurons in the auditory midbrain of anesthetized cats follows a similar time course, although onset dominance in temporal response patterns results in more robust directional sensitivity than expected, suggesting a simple mechanism for improving directional sensitivity in reverberation. In parallel behavioral experiments, we demonstrate that human lateralization judgments are consistent with predictions from a population rate model decoding the observed midbrain responses, suggesting a subcortical origin for robust sound localization in reverberant environments.

Effect of Reverberation on Directional Sensitivity of Auditory Neurons: Central and Peripheral Factors

“…Information transfer measures the extent to which stimulus azimuth is unambiguously encoded by spike count and is sensitive to both mean rate as well as trial-to-trial variability. Consistent with previous observations in anesthetized cat IC (Devore et al, 2009), we found that information transfer is highly correlated with the absolute range of firing rates across azimuth (data not shown, r 2 =0.83, p<0.001). Because we did not obtain enough stimulus trials to reliably estimate information transfer in many of the present units, we use the absolute range of firing rates to quantify directional sensitivity.…”

“…In a reverberant sound field, reflected acoustic waves reach the listener from all directions, interfering with the direct sound and distorting the binaural cues for sound localization such as interaural time and level differences (ITD and ILD). In previous work (Devore et al, 2009), we showed that reverberation degrades the directional sensitivity of low frequency, ITD-sensitive neurons in the inferior colliculus (IC) of anesthetized cats, although not as much as predicted by an interaural crosscorrelation model. Here, we extend this work by characterizing directional sensitivity in neurons across a wide range of the tonotopic axis in an awake rabbit preparation, while maintaining our focus on neurons that are sensitive to ITD.…”

“…In previous work, we showed that, at low CFs, compression of DRF in reverberation can be qualitatively attributed to decorrelation of the ear input signals after taking into account peripheral filtering (Devore et al, 2009). Here we use recordings from the AN to examine whether the disparity in the effect of reverberation for low-CF (ITD fs -sensitive) and high-CF (ITD env -sensitive) neurons can be explained by a similar, common type of binaural processing across all frequencies.…”

“…Methods for recording from single neurons in the IC of unanesthetized Dutch-Belted rabbits, (Oryctolagus cuniculus) were based on those of Kuwada et al (1987). Our protocol for characterizing the directional sensitivity of IC neurons is similar to that described previously (Devore et al, 2009). Responses were measured as a function of azimuth for each virtual room condition (anechoic, reverberant) and stimulus type (ITD-only, ITD+ILD) in pseudorandom order.…”

Physiological and Psychophysical Modeling of the Precedence Effect

“…Listeners have a remarkable ability to localize sounds accurately in reverberant settings, a feat attributed to the fact that they give greater perceptual weight to location cues at sound onsets, suppressing cues from later-arriving reflections (Zurek 1980;Freyman et al 1997;Devore et al 2009). This "precedence effect" (PE;Wallach et al 1949) has been studied using a range of paradigms whereby a pair of dichotic clicks is presented with a brief inter-stimulus delay (ISD).…”