Development shaped by cue reliability in the barn owl’s auditory midbrain

Abstract

Sensory systems display capability to preferentially choose stimuli based on their reliability at conveying accurate information. While previous reports have shown the ability of the brain to reweigh cues based on ongoing or dynamic changes in reliability, how the brain may learn and maintain neural responses to sensory statistics expected to be stable over longer time periods remain significant open questions of potential mechanisms underlying naturalistic biased perception. This study provides evidence that the barn owl’s midbrain is shaped by permanent statistics experienced during development. The barn owl’s midbrain features a topographic map of auditory space where neurons compute horizontal sound location from the interaural time difference (ITD). Previous work has shown that frequency tuning of these midbrain map neurons is correlated with the pattern of most reliable frequencies for the neurons’ preferred ITD. This pattern of ITD reliability is due to the filtering properties of the head, primarily determined by the facial ruff in the barn owl. In this study, we found that the absence of a facial ruff led to a decrease in the reliability of high frequencies originating from frontal space. To test if the owl’s frequency tuning of midbrain map neurons is driven by permanent changes in the pattern of ITD reliability, these neurons were recorded from adult owls, who had the facial ruff removed as juveniles, and from juvenile owls, before the facial ruff developed. In both groups, we found that frontally-tuned neurons displayed tunings to frequencies lower than reported in normal adult owls, consistent with the difference in ITD reliability between the normal and ruff removed conditions. Juvenile owls also exhibited more heterogeneous frequency tuning, suggesting developmental processes that refine tuning to match the pattern of ITD reliability. Additional recordings immediately upstream of the midbrain map displayed ITD tuned neural responses for all frequencies across the owl’s normal hearing range. Broader analysis of the effects of ruff-removal on the acoustical properties of spatial cues indicated a dominant role of ITD reliability in driving the adaptive changes in frequency tuning. These results support the hypothesis that frequency tuning in the midbrain map is developmentally adapted to permanent statistics of spatial cues, implementing probabilistic coding for sound localization.