Synthesis of Hemispheric ITD Tuning from the Readout of a Neural Map: Commonalities of Proposed Coding Schemes in Birds and Mammals

Abstract

A major cue to infer sound direction is the difference in arrival time of the sound at the left and right ears, called interaural time difference (ITD). The neural coding of ITD and its similarity across species have been strongly debated. In the barn owl, an auditory specialist relying on sound localization to capture prey, ITDs within the physiological range determined by the head width are topographically represented at each frequency. The topographic representation suggests that sound direction may be inferred from the location of maximal neural activity within the map. Such topographical representation of ITD, however, is not evident in mammals. Instead, the preferred ITD of neurons in the mammalian brainstem often lies outside the physiological range and depends on the neuron's best frequency. Because of these disparities, it has been assumed that how spatial hearing is achieved in birds and mammals is fundamentally different. However, recent studies reveal ITD responses in the owl's forebrain and midbrain premotor area that are consistent with coding schemes proposed in mammals. Particularly, sound location in owls could be decoded from the relative firing rates of two broadly and inversely ITD-tuned channels. This evidence suggests that, at downstream stages, the code for ITD may not be qualitatively different across species. Thus, while experimental evidence continues to support the notion of differences in ITD representation across species and brain regions, the latest results indicate notable commonalities, suggesting that codes driving orienting behavior in mammals and birds may be comparable.

Barn Owl's Auditory Space Map Activity Matching Conditions for a Population Vector Readout to Drive Adaptive Sound-Localizing Behavior

“…The overrepresentation of frontal space (dashed line) drives the resultant vector slightly more frontal than the actual location, matching the underestimation of sound sources observed across species. Adapted with permission from Peña et al, 2019 (their locate the OT. Recording wells over the OT in each brain hemisphere were constructed out of dental acrylic to allow for repeated recordings.…”

“…The overrepresentation of frontal space (dashed line) drives the resultant vector slightly more frontal than the actual location, matching the underestimation of sound sources observed across species. Adapted with permission fromPeña et al, 2019 (their Fig. 1).…”

Differences in the neural representation of binaural sound localization cues in the auditory midbrain of chicken and barn owl

“…At the apex of IC processing in the barn owl, the external nucleus (ICX), neurones are much more broadly frequency-tuned, suggesting convergent inputs by a range of narrowly tuned sources (Knudsen, 1984; Knudsen & Konishi, 1978; Wagner et al, 2007). However, a basic tonotopic order is maintained that runs congruent with the topographic map of azimuth, such that frontal auditory space is primarily represented by neurones sensitive to high frequencies and lateral space by neurones with progressively lower-frequency selectivity (Cazettes et al, 2014; Pena et al, 2019). If stimulated with broadband noise, the ITD tuning curves show a dominant main peak and strong side-peak suppression (Fujita & Konishi, 1991; Peña & Konishi, 2000; Takahashi & Konishi, 1986).…”

“…Another stream goes to the midbrain optic tectum (aka superior colliculus) for multimodal integration and ultimately drives fast, reflexive orienting responses to novel stimuli in the environment (Pena & Gutfreund, 2014). Owls show fast, acoustically driven orienting responses with beautiful precision (Knudsen et al, 1979), bringing novel stimuli into the zone of stereoscopic depth vision of their frontally directed eyes (Harmening & Wagner, 2011) and into their frontal acoustic field of most precise neural representation (Pena et al, 2019). Most other birds, like the chicken, do not show such precise orienting responses, indeed, probably do not need them, that is, there was no selective pressure for it.…”

Two Types of Auditory Spatial Receptive Fields in Different Parts of the Chicken's Midbrain

“…An alternative explanation is that the place coding of space in FRLx is converted to a rate code in OT. Such a mechanism has been observed in the barn owl, where ICx and OT, which have a map of auditory space based on place coding, project to the midbrain tegmentum, involved in eye gaze orientation, which operates as a rate code nucleus (Cazettes et al, 2018;Peña et al, 2019). However, rate code would generate ambiguities in a 2D environment, thus it would only be useful for coding sound directions along the azimuthal or elevational plane.…”