Auditory Competition and Coding of Relative Stimulus Strength across Midbrain Space Maps of Barn Owls

• Published in: The Journal of neuroscience Vol. 44; no. 21; p. e2081232024
• Main Authors: Bae, Andrea J, Ferger, Roland, Peña, José L
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 22.05.2024
• Subjects: Acoustic Stimulation - methods; Action Potentials - physiology; Animals; Auditory Pathways - physiology; Auditory Perception - physiology; Brain Mapping; Coding; Competition; Female; Hearing; Inferior Colliculi - physiology; Inferior colliculus; Localization; Male; Mesencephalon; Mesencephalon - physiology; Natural environment; Neural coding; Neurons - physiology; Oscillations; Owls; Response rates; Sensory integration; Sound localization; Sound Localization - physiology; Strigiformes - physiology; Superior colliculus; Tectum; Topographic mapping; Topographic maps; Tyto alba; Visual stimuli; salience; barn owl; sound localization; synchrony; stimulus competition; gamma oscillations
• ISSN: 0270-6474; 1529-2401; 1529-2401
• DOI: 10.1523/JNEUROSCI.2081-23.2024

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 present diverse auditory competitors (concurrent flat noise and amplitude-modulated noise) and record 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 the OT. Furthermore, changes in synchrony by sound competition in the OT are correlated to gamma range oscillations of local field potentials 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 readout.