Abstract
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.
Highlights
How connectivity and neuronal properties jointly contribute to efficient and adaptable functions of neural networks remains a central question in neuroscience
It is known that the spatial selectivity of ICx neurons in the horizontal direction is primarily due to their tuning to interaural time difference (ITD) [9,10,11]
We used known properties of ITD and frequency tuning in ICx and its input region inferior colliculus (ICcl) to infer the connectivity between ICcl and ICx, and the presence of nonlinear subthreshold frequency integration in ICx
Summary
How connectivity and neuronal properties jointly contribute to efficient and adaptable functions of neural networks remains a central question in neuroscience. We examined how circuit connectivity and the integrative properties of individual neurons contribute to the responses of space-specific neurons in the sound localization system of the barn owl. ITD is initially computed in the owl’s sound localization pathway by neurons that are narrowly tuned to frequency [12] Because of their narrow frequency tuning, the ITD-detecting neurons and their downstream targets have spatially ambiguous responses to ITD [12,13]. Nonlinear spiking responses of ICx neurons could be produced by a nonlinear conversion of membrane potentials to spikes [14,23,24,28] It remains unknown whether frequency integration, a critical function for resolving spatial ambiguity across species [14,17,29], is underlied by linear or nonlinear processing of subthreshold responses of ICx neurons
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