Diverse processing underlying frequency integration in midbrain neurons of barn owls.

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 th...

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Autores principales: Julia C Gorman, Oliver L Tufte, Anna V R Miller, William M DeBello, José L Peña, Brian J Fischer
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Lenguaje:EN
Publicado: Public Library of Science (PLoS) 2021
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Acceso en línea:https://doaj.org/article/1eb06f4b4ec64b33ade7c879c0ca99e8
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spelling oai:doaj.org-article:1eb06f4b4ec64b33ade7c879c0ca99e82021-12-02T19:58:11ZDiverse processing underlying frequency integration in midbrain neurons of barn owls.1553-734X1553-735810.1371/journal.pcbi.1009569https://doaj.org/article/1eb06f4b4ec64b33ade7c879c0ca99e82021-11-01T00:00:00Zhttps://doi.org/10.1371/journal.pcbi.1009569https://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358Emergent 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.Julia C GormanOliver L TufteAnna V R MillerWilliam M DeBelloJosé L PeñaBrian J FischerPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 17, Iss 11, p e1009569 (2021)
institution DOAJ
collection DOAJ
language EN
topic Biology (General)
QH301-705.5
spellingShingle Biology (General)
QH301-705.5
Julia C Gorman
Oliver L Tufte
Anna V R Miller
William M DeBello
José L Peña
Brian J Fischer
Diverse processing underlying frequency integration in midbrain neurons of barn owls.
description 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.
format article
author Julia C Gorman
Oliver L Tufte
Anna V R Miller
William M DeBello
José L Peña
Brian J Fischer
author_facet Julia C Gorman
Oliver L Tufte
Anna V R Miller
William M DeBello
José L Peña
Brian J Fischer
author_sort Julia C Gorman
title Diverse processing underlying frequency integration in midbrain neurons of barn owls.
title_short Diverse processing underlying frequency integration in midbrain neurons of barn owls.
title_full Diverse processing underlying frequency integration in midbrain neurons of barn owls.
title_fullStr Diverse processing underlying frequency integration in midbrain neurons of barn owls.
title_full_unstemmed Diverse processing underlying frequency integration in midbrain neurons of barn owls.
title_sort diverse processing underlying frequency integration in midbrain neurons of barn owls.
publisher Public Library of Science (PLoS)
publishDate 2021
url https://doaj.org/article/1eb06f4b4ec64b33ade7c879c0ca99e8
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AT oliverltufte diverseprocessingunderlyingfrequencyintegrationinmidbrainneuronsofbarnowls
AT annavrmiller diverseprocessingunderlyingfrequencyintegrationinmidbrainneuronsofbarnowls
AT williammdebello diverseprocessingunderlyingfrequencyintegrationinmidbrainneuronsofbarnowls
AT joselpena diverseprocessingunderlyingfrequencyintegrationinmidbrainneuronsofbarnowls
AT brianjfischer diverseprocessingunderlyingfrequencyintegrationinmidbrainneuronsofbarnowls
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