Glutamatergic signaling at the vestibular hair cell calyx synapse
In the vestibular periphery a unique postsynaptic terminal, the calyx, completely covers the basolateral walls of type I hair cells and receives input from multiple ribbon synapses. To date, the functional role of this specialized synapse remains elusive. There is limited data supporting glutamaterg...
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Veröffentlicht in: | The Journal of neuroscience 2014-10, Vol.34 (44), p.14536-14550 |
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description | In the vestibular periphery a unique postsynaptic terminal, the calyx, completely covers the basolateral walls of type I hair cells and receives input from multiple ribbon synapses. To date, the functional role of this specialized synapse remains elusive. There is limited data supporting glutamatergic transmission, K(+) or H(+) accumulation in the synaptic cleft as mechanisms of transmission. Here the role of glutamatergic transmission at the calyx synapse is investigated. Whole-cell patch-clamp recordings from calyx endings were performed in an in vitro whole-tissue preparation of the rat vestibular crista, the sensory organ of the semicircular canals that sense head rotation. AMPA-mediated EPSCs showed an unusually wide range of decay time constants, from 500 ms. Decay time constants of EPSCs increased (or decreased) in the presence of a glutamate transporter blocker (or a competitive glutamate receptor blocker), suggesting a role for glutamate accumulation and spillover in synaptic transmission. Glutamate accumulation caused slow depolarizations of the postsynaptic membrane potentials, and thereby substantially increased calyx firing rates. Finally, antibody labelings showed that a high percentage of presynaptic ribbon release sites and postsynaptic glutamate receptors were not juxtaposed, favoring a role for spillover. These findings suggest a prominent role for glutamate spillover in integration of inputs and synaptic transmission in the vestibular periphery. We propose that similar to other brain areas, such as the cerebellum and hippocampus, glutamate spillover may play a role in gain control of calyx afferents and contribute to their high-pass properties. |
doi_str_mv | 10.1523/jneurosci.0369-13.2014 |
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To date, the functional role of this specialized synapse remains elusive. There is limited data supporting glutamatergic transmission, K(+) or H(+) accumulation in the synaptic cleft as mechanisms of transmission. Here the role of glutamatergic transmission at the calyx synapse is investigated. Whole-cell patch-clamp recordings from calyx endings were performed in an in vitro whole-tissue preparation of the rat vestibular crista, the sensory organ of the semicircular canals that sense head rotation. AMPA-mediated EPSCs showed an unusually wide range of decay time constants, from <5 to >500 ms. Decay time constants of EPSCs increased (or decreased) in the presence of a glutamate transporter blocker (or a competitive glutamate receptor blocker), suggesting a role for glutamate accumulation and spillover in synaptic transmission. Glutamate accumulation caused slow depolarizations of the postsynaptic membrane potentials, and thereby substantially increased calyx firing rates. Finally, antibody labelings showed that a high percentage of presynaptic ribbon release sites and postsynaptic glutamate receptors were not juxtaposed, favoring a role for spillover. These findings suggest a prominent role for glutamate spillover in integration of inputs and synaptic transmission in the vestibular periphery. We propose that similar to other brain areas, such as the cerebellum and hippocampus, glutamate spillover may play a role in gain control of calyx afferents and contribute to their high-pass properties.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/jneurosci.0369-13.2014</identifier><identifier>PMID: 25355208</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Animals ; Excitatory Amino Acid Antagonists - pharmacology ; Excitatory Postsynaptic Potentials - drug effects ; Excitatory Postsynaptic Potentials - physiology ; Female ; Glutamic Acid - metabolism ; Hair Cells, Vestibular - drug effects ; Hair Cells, Vestibular - metabolism ; Male ; Patch-Clamp Techniques ; Quinoxalines - pharmacology ; Rats ; Rats, Sprague-Dawley ; Receptors, AMPA - antagonists & inhibitors ; Receptors, AMPA - metabolism ; Synapses - drug effects ; Synapses - metabolism ; Synaptic Transmission - drug effects ; Synaptic Transmission - physiology</subject><ispartof>The Journal of neuroscience, 2014-10, Vol.34 (44), p.14536-14550</ispartof><rights>Copyright © 2014 the authors 0270-6474/14/3414536-15$15.00/0.</rights><rights>Copyright © 2014 the authors 0270-6474/14/3414536-15$15.00/0 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c566t-1eaec6e418297cc8d898674a4c18ce39bedaf2f32e579d94f4baa269b05d1ada3</citedby><cites>FETCH-LOGICAL-c566t-1eaec6e418297cc8d898674a4c18ce39bedaf2f32e579d94f4baa269b05d1ada3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4212060/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4212060/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25355208$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sadeghi, Soroush G</creatorcontrib><creatorcontrib>Pyott, Sonja J</creatorcontrib><creatorcontrib>Yu, Zhou</creatorcontrib><creatorcontrib>Glowatzki, Elisabeth</creatorcontrib><title>Glutamatergic signaling at the vestibular hair cell calyx synapse</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>In the vestibular periphery a unique postsynaptic terminal, the calyx, completely covers the basolateral walls of type I hair cells and receives input from multiple ribbon synapses. To date, the functional role of this specialized synapse remains elusive. There is limited data supporting glutamatergic transmission, K(+) or H(+) accumulation in the synaptic cleft as mechanisms of transmission. Here the role of glutamatergic transmission at the calyx synapse is investigated. Whole-cell patch-clamp recordings from calyx endings were performed in an in vitro whole-tissue preparation of the rat vestibular crista, the sensory organ of the semicircular canals that sense head rotation. AMPA-mediated EPSCs showed an unusually wide range of decay time constants, from <5 to >500 ms. Decay time constants of EPSCs increased (or decreased) in the presence of a glutamate transporter blocker (or a competitive glutamate receptor blocker), suggesting a role for glutamate accumulation and spillover in synaptic transmission. Glutamate accumulation caused slow depolarizations of the postsynaptic membrane potentials, and thereby substantially increased calyx firing rates. Finally, antibody labelings showed that a high percentage of presynaptic ribbon release sites and postsynaptic glutamate receptors were not juxtaposed, favoring a role for spillover. These findings suggest a prominent role for glutamate spillover in integration of inputs and synaptic transmission in the vestibular periphery. We propose that similar to other brain areas, such as the cerebellum and hippocampus, glutamate spillover may play a role in gain control of calyx afferents and contribute to their high-pass properties.</description><subject>Animals</subject><subject>Excitatory Amino Acid Antagonists - pharmacology</subject><subject>Excitatory Postsynaptic Potentials - drug effects</subject><subject>Excitatory Postsynaptic Potentials - physiology</subject><subject>Female</subject><subject>Glutamic Acid - metabolism</subject><subject>Hair Cells, Vestibular - drug effects</subject><subject>Hair Cells, Vestibular - metabolism</subject><subject>Male</subject><subject>Patch-Clamp Techniques</subject><subject>Quinoxalines - pharmacology</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Receptors, AMPA - antagonists & inhibitors</subject><subject>Receptors, AMPA - metabolism</subject><subject>Synapses - drug effects</subject><subject>Synapses - metabolism</subject><subject>Synaptic Transmission - drug effects</subject><subject>Synaptic Transmission - physiology</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkctO20AUhkeoCELaV4i87MZh7uPZVEJRClQIJCjr0fH4OJnIsdMZGzVvjy0oalddncV_0fn1EbJgdMkUF5e7FofYJR-WVGibM7HklMkTMhtVm3NJ2Scyo9zQXEsjz8lFSjtKqaHMnJFzroRSnBYzcnXdDD3soce4CT5LYdNCE9pNBn3WbzF7wdSHcmggZlsIMfPYNJmH5vg7S8cWDgk_k9MamoRf3u-cPH9f_1zd5HcP17erq7vcK637nCGg1yhZwa3xvqgKW2gjQXpWeBS2xApqXguOytjKylqWAFzbkqqKQQViTr699R6Gco-Vx7aP0LhDDHuIR9dBcP8qbdi6TffiJGecajoWfH0viN2vYdzl9iFNe6DFbkiOGa1swZUx_7dqZsXEQY1W_Wb1I44Usf74iFE3WdyP-_Xz48PT6tZNqBwTbkI1Bhd_7_mI_WEjXgGjzpNU</recordid><startdate>20141029</startdate><enddate>20141029</enddate><creator>Sadeghi, Soroush G</creator><creator>Pyott, Sonja J</creator><creator>Yu, Zhou</creator><creator>Glowatzki, Elisabeth</creator><general>Society for Neuroscience</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>7X8</scope><scope>7TK</scope><scope>5PM</scope></search><sort><creationdate>20141029</creationdate><title>Glutamatergic signaling at the vestibular hair cell calyx synapse</title><author>Sadeghi, Soroush G ; Pyott, Sonja J ; Yu, Zhou ; Glowatzki, Elisabeth</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c566t-1eaec6e418297cc8d898674a4c18ce39bedaf2f32e579d94f4baa269b05d1ada3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>Excitatory Amino Acid Antagonists - pharmacology</topic><topic>Excitatory Postsynaptic Potentials - drug effects</topic><topic>Excitatory Postsynaptic Potentials - physiology</topic><topic>Female</topic><topic>Glutamic Acid - metabolism</topic><topic>Hair Cells, Vestibular - drug effects</topic><topic>Hair Cells, Vestibular - metabolism</topic><topic>Male</topic><topic>Patch-Clamp Techniques</topic><topic>Quinoxalines - pharmacology</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>Receptors, AMPA - antagonists & inhibitors</topic><topic>Receptors, AMPA - metabolism</topic><topic>Synapses - drug effects</topic><topic>Synapses - metabolism</topic><topic>Synaptic Transmission - drug effects</topic><topic>Synaptic Transmission - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sadeghi, Soroush G</creatorcontrib><creatorcontrib>Pyott, Sonja J</creatorcontrib><creatorcontrib>Yu, Zhou</creatorcontrib><creatorcontrib>Glowatzki, Elisabeth</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Neurosciences Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sadeghi, Soroush G</au><au>Pyott, Sonja J</au><au>Yu, Zhou</au><au>Glowatzki, Elisabeth</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Glutamatergic signaling at the vestibular hair cell calyx synapse</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2014-10-29</date><risdate>2014</risdate><volume>34</volume><issue>44</issue><spage>14536</spage><epage>14550</epage><pages>14536-14550</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>In the vestibular periphery a unique postsynaptic terminal, the calyx, completely covers the basolateral walls of type I hair cells and receives input from multiple ribbon synapses. 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Finally, antibody labelings showed that a high percentage of presynaptic ribbon release sites and postsynaptic glutamate receptors were not juxtaposed, favoring a role for spillover. These findings suggest a prominent role for glutamate spillover in integration of inputs and synaptic transmission in the vestibular periphery. We propose that similar to other brain areas, such as the cerebellum and hippocampus, glutamate spillover may play a role in gain control of calyx afferents and contribute to their high-pass properties.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>25355208</pmid><doi>10.1523/jneurosci.0369-13.2014</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Excitatory Amino Acid Antagonists - pharmacology Excitatory Postsynaptic Potentials - drug effects Excitatory Postsynaptic Potentials - physiology Female Glutamic Acid - metabolism Hair Cells, Vestibular - drug effects Hair Cells, Vestibular - metabolism Male Patch-Clamp Techniques Quinoxalines - pharmacology Rats Rats, Sprague-Dawley Receptors, AMPA - antagonists & inhibitors Receptors, AMPA - metabolism Synapses - drug effects Synapses - metabolism Synaptic Transmission - drug effects Synaptic Transmission - physiology |
title | Glutamatergic signaling at the vestibular hair cell calyx synapse |
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