Role of brain oscillations in midbrain and forebrain networks supporting stimulus selection in the sound localization pathway of barn owls

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PROJECT SUMMARY Modern neuroscience faces the challenge of bridging our understanding of single cell activity patterns to large population dynamics. Brain oscillations evoked by sensory stimuli are fluctuations in field potentials reflecting the combined activity of neural populations driven by a given stimulus. Oscillations have been observed in many species from invertebrates to primates, and have been implicated in various processes like attention and perceptual gating. Barn owls are specialists in sound localization studied for several decades. Their well- described midbrain stimulus selection network, a circuit dedicated to localizing salient sounds, provides a unique opportunity to evaluate the role of brain oscillations in coding. Previous in vivo recordings in the owl’s optic tectum (OT), homolog of the mammalian superior colliculus, have shown that gamma oscillations (25-140 Hz) are tuned to both visual and auditory space. However, previous recordings in deep midbrain structures, like OT, have relied on single electrodes and light tranquilization. These technical limitations impede our understanding of how oscillations may spread across the space map at a given time, and underscores the question of generalizability to awake processes like attention and perception. Our lab has pioneered population recordings across the space map using multielectrode arrays, and has recently developed chronic microdrive implants for recordings in awake owls. With these technical achievements, we will address several open questions regarding the role of oscillations in perception of salient stimuli and stimulus selection. Aim 1 will evaluate the spatial extent of gamma oscillations, and determine whether oscillations organize spike patterning to preferred phases. Initial analyses show that sound stimulation with the preferred direction increases power within the gamma range in a focal manner, supporting the hypothesis that spike patterning driven by brain oscillations has a role in coding sound location. Aim 2 will compare oscillation properties across awake and anesthetized states. Preliminary data and analysis suggest that while gamma power is higher in the awake state, phase locking of spikes to gamma oscillations is consistent across states, suggesting significant functional effects of gamma oscillations in organizing spike patterning are preserved during anesthesia. In Aim 3, we will conduct simultaneous recordings in the auditory thalamus and OT in awake behaving owls to test the hypothesis that gamma oscillations play a role in perception of salient sounds and stimulus selection. We will pair sound orienting behaviors, such as head turning and pupillary dilation responses, with electrophysiology to elucidate the coding mechanisms underlying interregional signaling during perception. Understanding how the owl’s midbrain stimulus selection circuit utilizes oscillations to conduct bottom-up relay and stimulus selection can provide insight to similar processes in human audition where the most relevant auditory stream must be prioritized in circumstances when the auditory scene is complex (cocktail party effect), and may inform novel optimization strategies for hearing aids.