Diverse processing underlying frequency integration in midbrain neurons of barn owls

• Published in: PLoS computational biology Vol. 17; no. 11; p. e1009569
• Main Authors: Gorman, Julia C, Tufte, Oliver L, Miller, Anna V R, DeBello, William M, Peña, José L, Fischer, Brian J
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 01.11.2021; Public Library of Science (PLoS)
• Subjects: Acoustic Stimulation; Analysis; Animals; Barn owl; Biology and Life Sciences; Brain stem; Circuits; Coding; Colliculus; Computational Biology - methods; Dendritic branching; Dendritic spines; Dendritic structure; Engineering and Technology; Horizontal orientation; Inferior colliculi; Inferior Colliculi - physiology; Inferior colliculus; Localization; Medicine and Health Sciences; Mesencephalon; Mesencephalon - cytology; Neural coding; Neural networks; Neurons; Neurons - physiology; Owls; Physiological aspects; Physiology; Questions; Selectivity; Sensory integration; Sensory neurons; Sound; Sound localization; Sound Localization - physiology; Sound sources; Spines; Strigiformes - physiology; Timing; Trees; Tyto alba; United States
• ISSN: 1553-7358; 1553-734X; 1553-7358
• DOI: 10.1371/journal.pcbi.1009569

Emergent response properties of sensory neurons depend on circuit connectivity and somatodendritic processing. Neurons of the barn owl's external nucleus of the inferior colliculus (ICx) display emergence of spatial selectivity. These neurons use interaural time difference (ITD) as a cue for the horizontal direction of sound sources. ITD is detected by upstream brainstem neurons with narrow frequency tuning, resulting in spatially ambiguous responses. This spatial ambiguity is resolved by ICx neurons integrating inputs over frequency, a relevant processing in sound localization across species. Previous models have predicted that ICx neurons function as point neurons that linearly integrate inputs across frequency. However, the complex dendritic trees and spines of ICx neurons raises the question of whether this prediction is accurate. Data from in vivo intracellular recordings of ICx neurons were used to address this question. Results revealed diverse frequency integration properties, where some ICx neurons showed responses consistent with the point neuron hypothesis and others with nonlinear dendritic integration. Modeling showed that varied connectivity patterns and forms of dendritic processing may underlie observed ICx neurons' frequency integration processing. These results corroborate the ability of neurons with complex dendritic trees to implement diverse linear and nonlinear integration of synaptic inputs, of relevance for adaptive coding and learning, and supporting a fundamental mechanism in sound localization.