Auditory competition and stimulus selection across spatial locations from midbrain to forebrain in barn owls

Abstract

Barn owls enable investigation of neural mechanisms underlying stimulus selection of concurrent stimuli. The audio-visual space map in the optic tectum (OT), avian homologue of the superior colliculus, encodes relative strength of concurrent auditory stimuli through spike response rate and interneuronal spike train synchrony (STS). Open questions remain regarding stimulus selection in downstream forebrain regions lacking topographic coding of auditory space, including the functional consequences of interneuronal STS on interregional signaling. To this end, we presented concurrent stimuli at different locations and manipulated relative strength while simultaneously recording neural responses from OT and its downstream thalamic target, nucleus rotundus (nRt), in awake barn owls of both sexes. Results demonstrated that broadly spatially tuned nRt units exhibit different spike response patterns to competition depending on spatial tuning preferences. Modeling suggests nRt units integrate convergent inputs from distant locations across midbrain map regions. Additionally, STS within nRt reflects the temporal properties of the strongest stimulus. Furthermore, interregional STS between OT and nRt was strongest when spatial tuning overlap between units across regions was large and when the strongest stimulus location during competition was favorable for units in both regions. Additionally, though gamma oscillations synthesized within OT are weakly propagated within nRt, average gamma power across regions correlates with strength of interregional STS. Overall, we demonstrate that nRt integrates inputs across distant areas of OT, retains spatial information through differences in strength of inputs from various locations of the midbrain map across neurons, and prioritizes coding of identity features to the strongest sound.Significance StatementThe brain strategically selects and preferentially processes salient stimuli. A critical function to this process involves transferring salient information across regions that may exhibit drastic transformations in coding schemes. Our study in barn owls investigates bottom-up signaling between the midbrain space map and its downstream thalamic target, which lacks spatial topography as also observed in mammalian auditory forebrain regions to elucidate general mechanisms underlying how spatial location information and other properties of the strongest sound are relayed between regions. Results show that the thalamus integrates neural responses widely across the midbrain map, retains coding of spatial location through varying strength of inputs of the map across neurons, and prioritizes further coding of identity features only to the strongest sound.