Diverse processing underlying frequency integration in midbrain neurons of barn owls

Emergent response properties of sensory neurons depend on circuit connectivity and somat-odendritic 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. Author summary Neurons at higher stages of sensory pathways often display selectivity for properties of sensory stimuli that result from computations performed within the nervous system. These emergent response properties can be produced by patterns of neural connectivity and processing that occur within individual cells. Here we investigated whether neural connectivity and single-neuron computation may contribute to the emergence of spatial selectivity in auditory neurons in the barn owl's midbrain. We used data from in vivo intracellular recordings to test the hypothesis from previous modeling work that these cells function as point neurons that perform a linear sum of their inputs in their subthreshold responses. Results indicate that while some neurons show responses consistent with the point neuron hypothesis, others match predictions of nonlinear integration, indicating a diversity of frequency integration properties across neurons. Modeling further showed that varied connectivity patterns and forms of single-neuron computation may underlie observed responses. These results demonstrate that neurons with complex morphologies may implement diverse integration of synaptic inputs, relevant for adaptive coding and learning.