Auditory competition and coding of relative stimulus strength across midbrain space maps of Barn Owls

Abstract

The natural environment challenges the brain to prioritize the processing of salient stimuli. The barn owl, a sound localization specialist, exhibits a circuit called the midbrain stimulus selection network, dedicated to representing locations of the most salient stimulus in circumstances of concurrent stimuli. Previous competition studies using unimodal (visual) and bimodal (visual and auditory) stimuli have shown that relative strength is encoded in spike response rates. However, open questions remain concerning auditory-auditory competition on coding. To this end, we presented diverse auditory competitors (concurrent flat noise and amplitude modulated noise) and recorded neural responses of awake barn owls of both sexes in subsequent midbrain space maps, the external nucleus of the inferior colliculus (ICx) and optic tectum (OT). While both ICx and OT exhibit a topographic map of auditory space, OT also integrates visual input and is part of the global-inhibitory midbrain stimulus selection network. Through comparative investigation of these regions, we show that while increasing strength of a competitor sound decreases spike response rates of spatially distant neurons in both regions, relative strength determines spike train synchrony of nearby units only in OT. Furthermore, changes in synchrony by sound competition in OT are correlated to gamma range oscillations of local field potentials (LFPs), associated with input from the midbrain stimulus selection network. The results of this investigation suggest that modulations in spiking synchrony between units by gamma oscillations are an emergent coding scheme representing relative strength of concurrent stimuli, which may have relevant implications for downstream read out.Significance Statement While natural auditory scenes are comprised of many acoustic signals, the brain is capable of segregating sources, and prioritizing representation of the most salient sound. This study demonstrates that midbrain space map neurons in the owl's optic tectum, homologue to the superior colliculus, represent relative strength of concurrent auditory stimuli by modulating inter-neuronal spike train synchrony. This synchrony correlates strongly with the low gamma range LFP, which reflects inputs from a midbrain stimulus selection network. These results may provide insight to similar processes in mammalian superior colliculus and human audition where the most relevant auditory signals must be prioritized in complex noisy environments and may inform optimization strategies for hearing aids.