Neural responses underlying interaural time difference discrimination as a function of sensory reliability in the barn owl

Abstract

Discrimination of sensory stimuli is fundamentally constrained by the information encoded in neuronal responses. In the barn owl, interaural time difference (ITD) serves as a primary cue for azimuthal sound localization and is represented topographically in the midbrain auditory space map in the external nucleus of the inferior colliculus (ICx). While prior studies have demonstrated a correspondence between spatial tuning and behavioral acuity, it remains unclear how changes in sensory reliability influence this relationship. Here, we examined how behavioral and neuronal ITD discrimination thresholds vary with binaural correlation (BC), which manipulates ITD cue reliability. Using the pupil dilation response (PDR) as a behavioral metric in head-fixed owls of either sex, we found that ITD just-noticeable-differences increased exponentially as BC decreased. In contrast, the widths of ICx ITD tuning curves increased more modestly, indicating that tuning resolution alone does not account for behavioral discrimination performance. By computing the Fisher information from ICx neuronal responses, we showed that the average neuronal discriminability predicts behavioral thresholds across BC values. A habituation-based model incorporating BC-dependent changes in tuning width, firing rate, and response variability successfully accounted for both direction and ITD discrimination. These findings support a model in which perceptual acuity is governed by the combined influence of neuronal tuning and variability and provide a unified framework for understanding how midbrain auditory representations underlie adaptive spatial hearing.

Significance Statement Determining the relationship between neural coding and perception is a major goal in neuroscience. We studied how barn owls discriminate interaural time differences (ITDs), a primary sound localization cue, when sensory reliability is degraded. Behavioral sensitivity declined sharply with reduced cue reliability, more than expected from changes in neural tuning resolution alone. Instead, behavioral thresholds align with a population-level measure of neural information that accounts for both tuning sharpness and response variability. A computational model suggests that discrimination performance arises from the interaction between neural habituation and degraded signal quality. These findings provide a mechanistic framework for understanding how the brain adapts to noisy environments by integrating reliability into sensory coding.