Slow Temporal Integration Enables Robust Neural Coding and Perception of a Cue to Sound Source Location

Abstract

In mammals, localization of sound sources in azimuth depends on sensitivity to interaural differences in sound timing (ITD) and level (ILD). Paradoxically, while typical ILD-sensitive neurons of the auditory brainstem require millisecond synchrony of excitatory and inhibitory inputs for the encoding of ILDs, human and animal behavioral ILD sensitivity is robust to temporal stimulus degradations (e.g., interaural decorrelation due to reverberation), or, in humans, bilateral clinical device processing. Here we demonstrate that behavioral ILD sensitivity is only modestly degraded with even complete decorrelation of left-and right-ear signals, suggesting the existence of a highly integrative ILD-coding mechanism. Correspondingly, we find that a majority of auditory midbrain neurons in the central nucleus of the inferior colliculus (of chinchilla) effectively encode ILDs despite complete decorrelation of left-and right-ear signals. We show that such responses can be accounted for by relatively long windows of bilateral excitatory-inhibitory interaction, which we explicitly measure using trains of narrowband clicks. Neural and behavioral data are compared with the outputs of a simple model of ILD processing with a single free parameter, the duration of excitatory-inhibitory interaction. Behavioral, neural, and modeling data collectively suggest that ILD sensitivity depends on binaural integration of excitation and inhibition within a տ3 ms temporal window, significantly longer than observed in lower brainstem neurons. This relatively slow integration potentiates a unique role for the ILD system in spatial hearing that may be of particular importance when informative ITD cues are unavailable.

Temporal binding of auditory spatial information across dynamic binaural events

“…Indeed, brain-stem physiology suggests slower ILD integration versus greater transient sensitivity to ITD change (Remme et al, 2014 ). On their own, those differences are too small to account for the differences found here, but may become exaggerated along the auditory pathway (Brown & Tollin, 2016 ). In fact, whereas ITD can only be computed via early brainstem mechanisms with microsecond acuity, ILD cues could be computed de novo via binaural comparisons in slower midbrain and cortical structures that encode sound level via spike rates.…”

Sensitivity to Envelope Interaural Time Difference: Models of Diverse LSO Neurons

“…3 and 4) analyzed as functions of ITD ENV . For each of 25 stimulus presentations of a 300-ms transposed tone, we calculated a JND in ITD ENV for each population of 24 model LSO neurons, based on a method of neuronal JND(IID) calculation (Brown & Tollin, 2016), which we extended to a neuronal population:…”

“…For each stimulus repetition and model population, a neural JND (Brown & Tollin, 2016) was calculated as the standard error of the mean spike rate, divided by the derivative of mean spike rate with respect to ITD. Agreement in the algebraic sign of the derivative in at least 19 of the 25 stimulus repetitions was required.…”

A framework for computational modelling of interaural time difference discrimination of normal and hearing-impaired listeners

“…Moreover, very recent work has used that same front end to study ILD perception. The model proposed by Brown and Tollin (2016) subtracted simulated left and right ear AN spike trains within a running temporal window. This simple model was good enough to validate their physiological and psychophysical observations of ILD sensitivity and robustness.…”

“…In order to be able to model this, we would need an additional module that could integrate binaural information across cues. The latter is not a trivial task, since the questions of at what levels of the auditory pathway and to what extent are time and level cues combined are still topics of ongoing research (Brown and Tollin, 2016;Ellinger et al, 2017;Johnson and Hautus, 2010;Palom€ aki et al, 2005;Phillips and Hall, 2005;Takanen et al, 2014).…”