The natural history of sound localization in mammals – a story of neuronal inhibition

Our concepts of sound localization in the vertebrate brain are widely based on the general assumption that both the ability to detect air-borne sounds and the neuronal processing are homologous in archosaurs (present day crocodiles and birds) and mammals. Yet studies repeatedly report conflicting re...

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Main Authors: Benedikt eGrothe, Michael ePecka
Format: Article
Language:English
Published: Frontiers Media S.A. 2014-10-01
Series:Frontiers in Neural Circuits
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fncir.2014.00116/full
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author Benedikt eGrothe
Michael ePecka
author_facet Benedikt eGrothe
Michael ePecka
author_sort Benedikt eGrothe
collection DOAJ
description Our concepts of sound localization in the vertebrate brain are widely based on the general assumption that both the ability to detect air-borne sounds and the neuronal processing are homologous in archosaurs (present day crocodiles and birds) and mammals. Yet studies repeatedly report conflicting results on the neuronal circuits and mechanisms, in particular the role of inhibition, as well as the coding strategies between avian and mammalian model systems.Here we argue that mammalian and avian phylogeny of spatial hearing is characterized by a convergent evolution of hearing air-borne sounds rather than by homology. In particular, the different evolutionary origins of tympanic ears and the different availability of binaural cues in early mammals and archosaurs imposed distinct constraints on the respective binaural processing mechanisms. The role of synaptic inhibition in generating binaural spatial sensitivity in mammals is highlighted, as it reveals a unifying principle of mammalian circuit design for encoding sound position. Together, we combine evolutionary, anatomical and physiological arguments for making a clear distinction between mammalian processing mechanisms and coding strategies and those of archosaurs. We emphasize that a consideration of the convergent nature of neuronal mechanisms will significantly increase the explanatory power of studies of spatial processing in both mammals and birds.
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spelling doaj.art-64367d653b3342a1bcd1a1f0236e5c6f2022-12-22T03:39:29ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102014-10-01810.3389/fncir.2014.00116109960The natural history of sound localization in mammals – a story of neuronal inhibitionBenedikt eGrothe0Michael ePecka1Ludwig-Maximilians University Munich, Biocenter Dept. II, NeurobiologyLudwig-Maximilians University Munich, Biocenter Dept. II, NeurobiologyOur concepts of sound localization in the vertebrate brain are widely based on the general assumption that both the ability to detect air-borne sounds and the neuronal processing are homologous in archosaurs (present day crocodiles and birds) and mammals. Yet studies repeatedly report conflicting results on the neuronal circuits and mechanisms, in particular the role of inhibition, as well as the coding strategies between avian and mammalian model systems.Here we argue that mammalian and avian phylogeny of spatial hearing is characterized by a convergent evolution of hearing air-borne sounds rather than by homology. In particular, the different evolutionary origins of tympanic ears and the different availability of binaural cues in early mammals and archosaurs imposed distinct constraints on the respective binaural processing mechanisms. The role of synaptic inhibition in generating binaural spatial sensitivity in mammals is highlighted, as it reveals a unifying principle of mammalian circuit design for encoding sound position. Together, we combine evolutionary, anatomical and physiological arguments for making a clear distinction between mammalian processing mechanisms and coding strategies and those of archosaurs. We emphasize that a consideration of the convergent nature of neuronal mechanisms will significantly increase the explanatory power of studies of spatial processing in both mammals and birds.http://journal.frontiersin.org/Journal/10.3389/fncir.2014.00116/fullBirdsGlycineMammalsevolutionGABAneuronal circuits
spellingShingle Benedikt eGrothe
Michael ePecka
The natural history of sound localization in mammals – a story of neuronal inhibition
Frontiers in Neural Circuits
Birds
Glycine
Mammals
evolution
GABA
neuronal circuits
title The natural history of sound localization in mammals – a story of neuronal inhibition
title_full The natural history of sound localization in mammals – a story of neuronal inhibition
title_fullStr The natural history of sound localization in mammals – a story of neuronal inhibition
title_full_unstemmed The natural history of sound localization in mammals – a story of neuronal inhibition
title_short The natural history of sound localization in mammals – a story of neuronal inhibition
title_sort natural history of sound localization in mammals a story of neuronal inhibition
topic Birds
Glycine
Mammals
evolution
GABA
neuronal circuits
url http://journal.frontiersin.org/Journal/10.3389/fncir.2014.00116/full
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