Coding of auditory space in the avian brain

Abstract [This resubmitted project carries on the study of how auditory space is encoded in the barn owl's brain, with the overarching goal of understanding the interplay between midbrain and forebrain neural populations underlying discriminability and stimulus selection through auditory space. Behavioral spatial discrimination assays will be used to test the hypothesis that spatial discriminability is optimized by a built-in representation of natural cue statistics and in vivo recordings through multi-electrode arrays (MEAs) will be conducted in both anesthetized and awake barn owls for investigating activity patterns of midbrain neural populations underlying this effect (Aim 1). Population recordings in the midbrain space map, the hub of the midbrain stimulus selection network, will be used to investigate the interplay of stimulus temporal dynamics and brain oscillations in the coding of salient sounds across space (Aim 2). Simultaneous population recordings over brain regions will be used to investigate the routing of neural activity between midbrain and forebrain underlying sound localization (Aim 3). Recent findings by our group indicating commonalities of coding schemes across birds and mammals, including humans, support the premise that investigating mechanisms underlying discriminability, stimulus selection across space, and population-level midbrain and forebrain routing of activity, important open questions in sound localization, will be of significance across species. The group has recently developed multiunit recordings in awake animals, which will be used towards every specific aim.] Towards Aim 1, we will investigate the relationship between spatial discriminability and a representation of natural statistics of spatial cues, focusing on interaural time difference (ITD), a critical binaural cue for determining the azimuth location of sounds across species. This aim will test a hypothesis, based on premises supported by previous work from our group, that a built-in representation of natural ITD statistics, determined by the acoustical properties of the head, exists in the brain and optimizes sound localization. Behavioral studies will be conducted to assess spatial discriminability across frequency and space. MEAs will be used to record activity of the midbrain map of auditory space and use decoding analyses to investigate properties of population responses supporting the optimized discriminability pattern. [Recordings in awake birds will be used as a control for the effect of anesthesia. Preliminary data show feasibility of recordings in awake animals and a pattern of ITD discriminability across frequency and locations consistent with the hypothesis and properties of midbrain population responses supporting feasibility of this approach.] In Aim 2 we will scrutinize the midbrain stimulus selection network of barn owls on a population scale. Previous work suggested a role of gamma oscillations in stimulus selection and recent studies by our group showed a dependence between stimulus driven temporal spiking patterns and the location of sound sources relative to the preferred direction of space specific neurons of the owl’s midbrain. Based on this evidence, we will address the unexplored question of the interplay of brain oscillations and stimulus driven modulation of temporal spiking patterns in stimulus selection across space, a critical function of the sound localization system for detecting sounds based on their salience and location. [Population recordings in anesthetized and awake animals will be used to simultaneously track the power of brain oscillations across different frequency bands as well as envelope driven spiking patterns under competing sound stimulation. Preliminary data from MEA recordings across the midbrain space map show changes in population responses to competing sounds supporting the feasibility of the approach, and correlation between power of gamma oscillations and stimulus-driven temporal spiking patterning across the population consistent with an interplay of these signals in coding the salience of a sound. Preliminary data of recordings in awake barn owls show increased power of gamma range brain oscillations and correlation with response levels, corresponding with results obtained in anesthetized animals.] A critical open question in sound localization is the interplay of midbrain and forebrain areas displaying seemingly different coding schemes of sound localization, which we will address in Aim 3. [We will conduct simultaneous population recordings across brain regions in anesthetized and awake birds to elucidate the routing of neural activity across areas by analyzing pairwise correlation structure and trial-to-trial variability.] Previous studies by our group have shown important differences in correlation structure between midbrain and forebrain regions involved in sound localization, supporting the potential significance of investigating the bases of those results in simultaneous recordings of these brain areas and feasibility of this unprecedented approach. Thus, this project will assess the higher-order dynamics and interplay of midbrain and forebrain neural populations involved in sound localization to investigate mechanisms underlying vital functions that operate across species. [A new approach of in vivo recording in awake barn owls was recently developed by the group to validate functional significance of results across aims.] The contribution of this research to understanding central auditory processing underlying sound localization will lead to more accurate interpretations of auditory perception and its disruption in hearing disorders, with potential for improving treatments.