Axon–glia interactions in the ascending auditory system
The auditory system detects and encodes sound information with high precision to provide a high‐fidelity representation of the environment and communication. In mammals, detection occurs in the peripheral sensory organ (the cochlea) containing specialized mechanosensory cells (hair cells) that initi...
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Veröffentlicht in: | Developmental neurobiology (Hoboken, N.J.) N.J.), 2021-07, Vol.81 (5), p.546-567 |
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creator | Kohrman, David C. Borges, Beatriz C. Cassinotti, Luis R. Ji, Lingchao Corfas, Gabriel |
description | The auditory system detects and encodes sound information with high precision to provide a high‐fidelity representation of the environment and communication. In mammals, detection occurs in the peripheral sensory organ (the cochlea) containing specialized mechanosensory cells (hair cells) that initiate the conversion of sound‐generated vibrations into action potentials in the auditory nerve. Neural activity in the auditory nerve encodes information regarding the intensity and frequency of sound stimuli, which is transmitted to the auditory cortex through the ascending neural pathways. Glial cells are critical for precise control of neural conduction and synaptic transmission throughout the pathway, allowing for the precise detection of the timing, frequency, and intensity of sound signals, including the sub‐millisecond temporal fidelity is necessary for tasks such as sound localization, and in humans, for processing complex sounds including speech and music. In this review, we focus on glia and glia‐like cells that interact with hair cells and neurons in the ascending auditory pathway and contribute to the development, maintenance, and modulation of neural circuits and transmission in the auditory system. We also discuss the molecular mechanisms of these interactions, their impact on hearing and on auditory dysfunction associated with pathologies of each cell type. |
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In mammals, detection occurs in the peripheral sensory organ (the cochlea) containing specialized mechanosensory cells (hair cells) that initiate the conversion of sound‐generated vibrations into action potentials in the auditory nerve. Neural activity in the auditory nerve encodes information regarding the intensity and frequency of sound stimuli, which is transmitted to the auditory cortex through the ascending neural pathways. Glial cells are critical for precise control of neural conduction and synaptic transmission throughout the pathway, allowing for the precise detection of the timing, frequency, and intensity of sound signals, including the sub‐millisecond temporal fidelity is necessary for tasks such as sound localization, and in humans, for processing complex sounds including speech and music. 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We also discuss the molecular mechanisms of these interactions, their impact on hearing and on auditory dysfunction associated with pathologies of each cell type.</description><identifier>ISSN: 1932-8451</identifier><identifier>ISSN: 1932-846X</identifier><identifier>EISSN: 1932-846X</identifier><identifier>DOI: 10.1002/dneu.22813</identifier><identifier>PMID: 33561889</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>Acoustic Stimulation ; Animals ; astrocytes ; Auditory nerve ; Auditory pathways ; Auditory Pathways - physiology ; Auditory system ; Axons ; Cochlea ; Cochlea - physiology ; Cortex (auditory) ; Cortex (somatosensory) ; Cortex (temporal) ; glia ; Glial cells ; Hair cells ; Hearing ; hearing loss ; Humans ; Localization ; Mammals ; Molecular modelling ; Neural networks ; Neuroglia ; Neuronal-glial interactions ; neuron–glia interactions ; oligodendrocytes ; satellite glial cells ; Schwann cells ; Sense organs ; Sound ; supporting cells ; Synaptic transmission ; Vibrations</subject><ispartof>Developmental neurobiology (Hoboken, N.J.), 2021-07, Vol.81 (5), p.546-567</ispartof><rights>2021 Wiley Periodicals LLC.</rights><rights>Copyright © 2021 Wiley Periodicals LLC</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4483-fae443e0e0914fae2898b7268bfeb53df23d0855dfceff0c6123d6bc14510b373</citedby><cites>FETCH-LOGICAL-c4483-fae443e0e0914fae2898b7268bfeb53df23d0855dfceff0c6123d6bc14510b373</cites><orcidid>0000-0001-5412-9473</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fdneu.22813$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fdneu.22813$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,778,782,883,1414,1430,27911,27912,45561,45562,46396,46820</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33561889$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kohrman, David C.</creatorcontrib><creatorcontrib>Borges, Beatriz C.</creatorcontrib><creatorcontrib>Cassinotti, Luis R.</creatorcontrib><creatorcontrib>Ji, Lingchao</creatorcontrib><creatorcontrib>Corfas, Gabriel</creatorcontrib><title>Axon–glia interactions in the ascending auditory system</title><title>Developmental neurobiology (Hoboken, N.J.)</title><addtitle>Dev Neurobiol</addtitle><description>The auditory system detects and encodes sound information with high precision to provide a high‐fidelity representation of the environment and communication. In mammals, detection occurs in the peripheral sensory organ (the cochlea) containing specialized mechanosensory cells (hair cells) that initiate the conversion of sound‐generated vibrations into action potentials in the auditory nerve. Neural activity in the auditory nerve encodes information regarding the intensity and frequency of sound stimuli, which is transmitted to the auditory cortex through the ascending neural pathways. Glial cells are critical for precise control of neural conduction and synaptic transmission throughout the pathway, allowing for the precise detection of the timing, frequency, and intensity of sound signals, including the sub‐millisecond temporal fidelity is necessary for tasks such as sound localization, and in humans, for processing complex sounds including speech and music. 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We also discuss the molecular mechanisms of these interactions, their impact on hearing and on auditory dysfunction associated with pathologies of each cell type.</description><subject>Acoustic Stimulation</subject><subject>Animals</subject><subject>astrocytes</subject><subject>Auditory nerve</subject><subject>Auditory pathways</subject><subject>Auditory Pathways - physiology</subject><subject>Auditory system</subject><subject>Axons</subject><subject>Cochlea</subject><subject>Cochlea - physiology</subject><subject>Cortex (auditory)</subject><subject>Cortex (somatosensory)</subject><subject>Cortex (temporal)</subject><subject>glia</subject><subject>Glial cells</subject><subject>Hair cells</subject><subject>Hearing</subject><subject>hearing loss</subject><subject>Humans</subject><subject>Localization</subject><subject>Mammals</subject><subject>Molecular modelling</subject><subject>Neural networks</subject><subject>Neuroglia</subject><subject>Neuronal-glial interactions</subject><subject>neuron–glia interactions</subject><subject>oligodendrocytes</subject><subject>satellite glial cells</subject><subject>Schwann cells</subject><subject>Sense organs</subject><subject>Sound</subject><subject>supporting cells</subject><subject>Synaptic transmission</subject><subject>Vibrations</subject><issn>1932-8451</issn><issn>1932-846X</issn><issn>1932-846X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kctKAzEUhoMoXqobH0AG3IhQPblMmmyE4h1ENwruQmYmUyPTRJMZtTvfwTf0SYy2FnXhKjnJx8d_-BHaxLCHAch-5Uy3R4jAdAGtYklJXzB-uzi_53gFrcV4D5BTwmEZrVCacyyEXEVy-OLd--vbqLE6s641QZet9S6mIWvvTKZjaVxl3SjTXWVbHyZZnMTWjNfRUq2baDZmZw_dnBxfH571L65Ozw-HF_2SMUH7tTaMUQMGJGZpIEKKYkC4KGpT5LSqCa1A5HlVl6auoeQ4PfCixCk2FHRAe-hg6n3oirGpUpo26EY9BDvWYaK8tur3j7N3auSflARghOIk2JkJgn_sTGzV2KalmkY747uoCBMCDwiTPKHbf9B73wWX1lMk5yAkB5CJ2p1SZfAxBlPPw2BQn42oz0bUVyMJ3voZf45-V5AAPAWebWMm_6jU0eXxzVT6Afexl_I</recordid><startdate>202107</startdate><enddate>202107</enddate><creator>Kohrman, David C.</creator><creator>Borges, Beatriz C.</creator><creator>Cassinotti, Luis R.</creator><creator>Ji, Lingchao</creator><creator>Corfas, Gabriel</creator><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-5412-9473</orcidid></search><sort><creationdate>202107</creationdate><title>Axon–glia interactions in the ascending auditory system</title><author>Kohrman, David C. ; Borges, Beatriz C. ; Cassinotti, Luis R. ; Ji, Lingchao ; Corfas, Gabriel</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4483-fae443e0e0914fae2898b7268bfeb53df23d0855dfceff0c6123d6bc14510b373</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Acoustic Stimulation</topic><topic>Animals</topic><topic>astrocytes</topic><topic>Auditory nerve</topic><topic>Auditory pathways</topic><topic>Auditory Pathways - physiology</topic><topic>Auditory system</topic><topic>Axons</topic><topic>Cochlea</topic><topic>Cochlea - physiology</topic><topic>Cortex (auditory)</topic><topic>Cortex (somatosensory)</topic><topic>Cortex (temporal)</topic><topic>glia</topic><topic>Glial cells</topic><topic>Hair cells</topic><topic>Hearing</topic><topic>hearing loss</topic><topic>Humans</topic><topic>Localization</topic><topic>Mammals</topic><topic>Molecular modelling</topic><topic>Neural networks</topic><topic>Neuroglia</topic><topic>Neuronal-glial interactions</topic><topic>neuron–glia interactions</topic><topic>oligodendrocytes</topic><topic>satellite glial cells</topic><topic>Schwann cells</topic><topic>Sense organs</topic><topic>Sound</topic><topic>supporting cells</topic><topic>Synaptic transmission</topic><topic>Vibrations</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kohrman, David C.</creatorcontrib><creatorcontrib>Borges, Beatriz C.</creatorcontrib><creatorcontrib>Cassinotti, Luis R.</creatorcontrib><creatorcontrib>Ji, Lingchao</creatorcontrib><creatorcontrib>Corfas, Gabriel</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Developmental neurobiology (Hoboken, N.J.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kohrman, David C.</au><au>Borges, Beatriz C.</au><au>Cassinotti, Luis R.</au><au>Ji, Lingchao</au><au>Corfas, Gabriel</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Axon–glia interactions in the ascending auditory system</atitle><jtitle>Developmental neurobiology (Hoboken, N.J.)</jtitle><addtitle>Dev Neurobiol</addtitle><date>2021-07</date><risdate>2021</risdate><volume>81</volume><issue>5</issue><spage>546</spage><epage>567</epage><pages>546-567</pages><issn>1932-8451</issn><issn>1932-846X</issn><eissn>1932-846X</eissn><abstract>The auditory system detects and encodes sound information with high precision to provide a high‐fidelity representation of the environment and communication. In mammals, detection occurs in the peripheral sensory organ (the cochlea) containing specialized mechanosensory cells (hair cells) that initiate the conversion of sound‐generated vibrations into action potentials in the auditory nerve. Neural activity in the auditory nerve encodes information regarding the intensity and frequency of sound stimuli, which is transmitted to the auditory cortex through the ascending neural pathways. Glial cells are critical for precise control of neural conduction and synaptic transmission throughout the pathway, allowing for the precise detection of the timing, frequency, and intensity of sound signals, including the sub‐millisecond temporal fidelity is necessary for tasks such as sound localization, and in humans, for processing complex sounds including speech and music. 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subjects | Acoustic Stimulation Animals astrocytes Auditory nerve Auditory pathways Auditory Pathways - physiology Auditory system Axons Cochlea Cochlea - physiology Cortex (auditory) Cortex (somatosensory) Cortex (temporal) glia Glial cells Hair cells Hearing hearing loss Humans Localization Mammals Molecular modelling Neural networks Neuroglia Neuronal-glial interactions neuron–glia interactions oligodendrocytes satellite glial cells Schwann cells Sense organs Sound supporting cells Synaptic transmission Vibrations |
title | Axon–glia interactions in the ascending auditory system |
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