Octopus Cells in the Posteroventral Cochlear Nucleus Provide the Main Excitatory Input to the Superior Paraolivary Nucleus

Auditory streaming enables perception and interpretation of complex acoustic environments that contain competing sound sources. At early stages of central processing, sounds are segregated into separate streams representing attributes that later merge into acoustic objects. Streaming of temporal cue...

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Main Authors: Richard A. Felix II, Boris Gourévitch, Marcelo Gómez-Álvarez, Sara C. M. Leijon, Enrique Saldaña, Anna K. Magnusson
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-05-01
Series:Frontiers in Neural Circuits
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fncir.2017.00037/full
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spelling doaj-ecde13635d68487db2dd061c4e8784a52020-11-24T23:42:18ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102017-05-011110.3389/fncir.2017.00037248117Octopus Cells in the Posteroventral Cochlear Nucleus Provide the Main Excitatory Input to the Superior Paraolivary NucleusRichard A. Felix II0Boris Gourévitch1Boris Gourévitch2Boris Gourévitch3Marcelo Gómez-Álvarez4Marcelo Gómez-Álvarez5Marcelo Gómez-Álvarez6Sara C. M. Leijon7Enrique Saldaña8Enrique Saldaña9Anna K. Magnusson10Unit of Audiology, Department of Clinical Science, Intervention and Technology, Karolinska InstitutetStockholm, SwedenInstitut Pasteur, Unité de Génétique et Physiologie de l'AuditionParis, FranceInstitut National de la Santé et de la Recherche Médicale, UMRS 1120Paris, FranceUniversité Pierre et Marie CurieParis, FranceUnit of Audiology, Department of Clinical Science, Intervention and Technology, Karolinska InstitutetStockholm, SwedenNeuroscience Institute of Castilla y León (INCyL), Universidad de SalamancaSalamanca, SpainInstitute of Biomedical Research of Salamanca (IBSAL)Salamanca, SpainUnit of Audiology, Department of Clinical Science, Intervention and Technology, Karolinska InstitutetStockholm, SwedenNeuroscience Institute of Castilla y León (INCyL), Universidad de SalamancaSalamanca, SpainInstitute of Biomedical Research of Salamanca (IBSAL)Salamanca, SpainUnit of Audiology, Department of Clinical Science, Intervention and Technology, Karolinska InstitutetStockholm, SwedenAuditory streaming enables perception and interpretation of complex acoustic environments that contain competing sound sources. At early stages of central processing, sounds are segregated into separate streams representing attributes that later merge into acoustic objects. Streaming of temporal cues is critical for perceiving vocal communication, such as human speech, but our understanding of circuits that underlie this process is lacking, particularly at subcortical levels. The superior paraolivary nucleus (SPON), a prominent group of inhibitory neurons in the mammalian brainstem, has been implicated in processing temporal information needed for the segmentation of ongoing complex sounds into discrete events. The SPON requires temporally precise and robust excitatory input(s) to convey information about the steep rise in sound amplitude that marks the onset of voiced sound elements. Unfortunately, the sources of excitation to the SPON and the impact of these inputs on the behavior of SPON neurons have yet to be resolved. Using anatomical tract tracing and immunohistochemistry, we identified octopus cells in the contralateral cochlear nucleus (CN) as the primary source of excitatory input to the SPON. Cluster analysis of miniature excitatory events also indicated that the majority of SPON neurons receive one type of excitatory input. Precise octopus cell-driven onset spiking coupled with transient offset spiking make SPON responses well-suited to signal transitions in sound energy contained in vocalizations. Targets of octopus cell projections, including the SPON, are strongly implicated in the processing of temporal sound features, which suggests a common pathway that conveys information critical for perception of complex natural sounds.http://journal.frontiersin.org/article/10.3389/fncir.2017.00037/fullauditory brainstemtemporal processingtract tracingcalretinincluster analysis
collection DOAJ
language English
format Article
sources DOAJ
author Richard A. Felix II
Boris Gourévitch
Boris Gourévitch
Boris Gourévitch
Marcelo Gómez-Álvarez
Marcelo Gómez-Álvarez
Marcelo Gómez-Álvarez
Sara C. M. Leijon
Enrique Saldaña
Enrique Saldaña
Anna K. Magnusson
spellingShingle Richard A. Felix II
Boris Gourévitch
Boris Gourévitch
Boris Gourévitch
Marcelo Gómez-Álvarez
Marcelo Gómez-Álvarez
Marcelo Gómez-Álvarez
Sara C. M. Leijon
Enrique Saldaña
Enrique Saldaña
Anna K. Magnusson
Octopus Cells in the Posteroventral Cochlear Nucleus Provide the Main Excitatory Input to the Superior Paraolivary Nucleus
Frontiers in Neural Circuits
auditory brainstem
temporal processing
tract tracing
calretinin
cluster analysis
author_facet Richard A. Felix II
Boris Gourévitch
Boris Gourévitch
Boris Gourévitch
Marcelo Gómez-Álvarez
Marcelo Gómez-Álvarez
Marcelo Gómez-Álvarez
Sara C. M. Leijon
Enrique Saldaña
Enrique Saldaña
Anna K. Magnusson
author_sort Richard A. Felix II
title Octopus Cells in the Posteroventral Cochlear Nucleus Provide the Main Excitatory Input to the Superior Paraolivary Nucleus
title_short Octopus Cells in the Posteroventral Cochlear Nucleus Provide the Main Excitatory Input to the Superior Paraolivary Nucleus
title_full Octopus Cells in the Posteroventral Cochlear Nucleus Provide the Main Excitatory Input to the Superior Paraolivary Nucleus
title_fullStr Octopus Cells in the Posteroventral Cochlear Nucleus Provide the Main Excitatory Input to the Superior Paraolivary Nucleus
title_full_unstemmed Octopus Cells in the Posteroventral Cochlear Nucleus Provide the Main Excitatory Input to the Superior Paraolivary Nucleus
title_sort octopus cells in the posteroventral cochlear nucleus provide the main excitatory input to the superior paraolivary nucleus
publisher Frontiers Media S.A.
series Frontiers in Neural Circuits
issn 1662-5110
publishDate 2017-05-01
description Auditory streaming enables perception and interpretation of complex acoustic environments that contain competing sound sources. At early stages of central processing, sounds are segregated into separate streams representing attributes that later merge into acoustic objects. Streaming of temporal cues is critical for perceiving vocal communication, such as human speech, but our understanding of circuits that underlie this process is lacking, particularly at subcortical levels. The superior paraolivary nucleus (SPON), a prominent group of inhibitory neurons in the mammalian brainstem, has been implicated in processing temporal information needed for the segmentation of ongoing complex sounds into discrete events. The SPON requires temporally precise and robust excitatory input(s) to convey information about the steep rise in sound amplitude that marks the onset of voiced sound elements. Unfortunately, the sources of excitation to the SPON and the impact of these inputs on the behavior of SPON neurons have yet to be resolved. Using anatomical tract tracing and immunohistochemistry, we identified octopus cells in the contralateral cochlear nucleus (CN) as the primary source of excitatory input to the SPON. Cluster analysis of miniature excitatory events also indicated that the majority of SPON neurons receive one type of excitatory input. Precise octopus cell-driven onset spiking coupled with transient offset spiking make SPON responses well-suited to signal transitions in sound energy contained in vocalizations. Targets of octopus cell projections, including the SPON, are strongly implicated in the processing of temporal sound features, which suggests a common pathway that conveys information critical for perception of complex natural sounds.
topic auditory brainstem
temporal processing
tract tracing
calretinin
cluster analysis
url http://journal.frontiersin.org/article/10.3389/fncir.2017.00037/full
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