The Sound of Silence: Ionic Mechanisms Encoding Sound Termination
Offset responses upon termination of a stimulus are crucial for perceptual grouping and gap detection. These gaps are key features of vocal communication, but an ionic mechanism capable of generating fast offsets from auditory stimuli has proven elusive. Offset firing arises in the brainstem superio...
Gespeichert in:
| Veröffentlicht in: | Neuron (Cambridge, Mass.) Mass.), 2011-09, Vol.71 (5), p.911-925 |
|---|---|
| Hauptverfasser: | , , , , , |
| Format: | Artikel |
| Sprache: | eng |
| Schlagworte: | |
| Online-Zugang: | Volltext |
| Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
| container_end_page | 925 |
|---|---|
| container_issue | 5 |
| container_start_page | 911 |
| container_title | Neuron (Cambridge, Mass.) |
| container_volume | 71 |
| creator | Kopp-Scheinpflug, Cornelia Tozer, Adam J.B. Robinson, Susan W. Tempel, Bruce L. Hennig, Matthias H. Forsythe, Ian D. |
| description | Offset responses upon termination of a stimulus are crucial for perceptual grouping and gap detection. These gaps are key features of vocal communication, but an ionic mechanism capable of generating fast offsets from auditory stimuli has proven elusive. Offset firing arises in the brainstem superior paraolivary nucleus (SPN), which receives powerful inhibition during sound and converts this into precise action potential (AP) firing upon sound termination. Whole-cell patch recording in vitro showed that offset firing was triggered by IPSPs rather than EPSPs. We show that AP firing can emerge from inhibition through integration of large IPSPs, driven by an extremely negative chloride reversal potential (ECl), combined with a large hyperpolarization-activated nonspecific cationic current (IH), with a secondary contribution from a T-type calcium conductance (ITCa). On activation by the IPSP, IH potently accelerates the membrane time constant, so when the sound ceases, a rapid repolarization triggers multiple offset APs that match onset timing accuracy.
► Offset responses encode the termination of a sensory synaptic stimulus ► SPN neurons have an intrinsic ionic mechanism to generate offset firing from IPSPs ► KCC2 is required to maintain low internal chloride which results in large IPSPs ► Large IPSPs trigger IH, accelerating tau, and mediate fast offset firing |
| doi_str_mv | 10.1016/j.neuron.2011.06.028 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_907175261</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S0896627311005587</els_id><sourcerecordid>3388955201</sourcerecordid><originalsourceid>FETCH-LOGICAL-c533t-35cb1dfcd6c3c0835820921f502d6a5be8739224b9c9370a120a7304c60753243</originalsourceid><addsrcrecordid>eNp9kD1PwzAURS0EoqXwDxCKxMCU8J4dOzEDUoX4kooYKLOVOg64auxiJ0j8e1K1MDAwveXce58OIacIGQKKy2XmTB-8yyggZiAyoOUeGSPIIs1Ryn0yhlKKVNCCjchRjEsAzLnEQzKiKIFBycZkOn83yYvvXZ34JnmxK-O0uUoevbM6eTL6vXI2tjG5ddrX1r3t2LkJrXVVZ707JgdNtYrmZHcn5PXudn7zkM6e7x9vprNUc8a6lHG9wLrRtdBMD9O8pCApNhxoLSq-MGXBJKX5QmrJCqiQQlUwyLWAgjOaswm52Paug__oTexUa6M2q1XljO-jklBgwanAgTz_Qy59H9zwnEKeS8nLUtKByreUDj7GYBq1DratwpdCUBvDaqm2htXGsAKhBsND7GxX3i9aU_-GfpQOwPUWMIOMT2uCitpurNY2GN2p2tv_F74BoaqLew</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1549958892</pqid></control><display><type>article</type><title>The Sound of Silence: Ionic Mechanisms Encoding Sound Termination</title><source>MEDLINE</source><source>Elsevier ScienceDirect Journals Complete</source><source>Free E-Journal (出版社公開部分のみ）</source><source>Cell Press Free Archives(OpenAccess)</source><creator>Kopp-Scheinpflug, Cornelia ; Tozer, Adam J.B. ; Robinson, Susan W. ; Tempel, Bruce L. ; Hennig, Matthias H. ; Forsythe, Ian D.</creator><creatorcontrib>Kopp-Scheinpflug, Cornelia ; Tozer, Adam J.B. ; Robinson, Susan W. ; Tempel, Bruce L. ; Hennig, Matthias H. ; Forsythe, Ian D.</creatorcontrib><description>Offset responses upon termination of a stimulus are crucial for perceptual grouping and gap detection. These gaps are key features of vocal communication, but an ionic mechanism capable of generating fast offsets from auditory stimuli has proven elusive. Offset firing arises in the brainstem superior paraolivary nucleus (SPN), which receives powerful inhibition during sound and converts this into precise action potential (AP) firing upon sound termination. Whole-cell patch recording in vitro showed that offset firing was triggered by IPSPs rather than EPSPs. We show that AP firing can emerge from inhibition through integration of large IPSPs, driven by an extremely negative chloride reversal potential (ECl), combined with a large hyperpolarization-activated nonspecific cationic current (IH), with a secondary contribution from a T-type calcium conductance (ITCa). On activation by the IPSP, IH potently accelerates the membrane time constant, so when the sound ceases, a rapid repolarization triggers multiple offset APs that match onset timing accuracy.
► Offset responses encode the termination of a sensory synaptic stimulus ► SPN neurons have an intrinsic ionic mechanism to generate offset firing from IPSPs ► KCC2 is required to maintain low internal chloride which results in large IPSPs ► Large IPSPs trigger IH, accelerating tau, and mediate fast offset firing</description><identifier>ISSN: 0896-6273</identifier><identifier>EISSN: 1097-4199</identifier><identifier>DOI: 10.1016/j.neuron.2011.06.028</identifier><identifier>PMID: 21903083</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Acoustic Stimulation - methods ; Action Potentials - drug effects ; Action Potentials - physiology ; Animals ; Animals, Newborn ; Auditory Pathways - physiology ; Biophysics ; Calcium - metabolism ; Calcium Channel Blockers - pharmacology ; Calcium Channels, T-Type - metabolism ; Chlorides - metabolism ; Computer Simulation ; Cyclic Nucleotide-Gated Cation Channels - deficiency ; Electric Stimulation ; Experiments ; Functional Laterality ; Furosemide - pharmacology ; Gene Expression Regulation - genetics ; Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels ; In Vitro Techniques ; Ion Channel Gating - genetics ; Ion Channel Gating - physiology ; K Cl- Cotransporters ; Mammals ; Mibefradil - pharmacology ; Mice ; Mice, Inbred CBA ; Mice, Knockout ; Models, Neurological ; Neurons ; Neurons - drug effects ; Neurons - physiology ; Olivary Nucleus - cytology ; Patch-Clamp Techniques - methods ; Potassium ; Potassium Channels - deficiency ; Psychoacoustics ; Pyrimidines - pharmacology ; Reaction Time - drug effects ; Reaction Time - genetics ; Reaction Time - physiology ; Sodium Potassium Chloride Symporter Inhibitors - pharmacology ; Sound ; Statistical methods ; Stilbamidines - metabolism ; Symporters - metabolism ; Synaptic Potentials - drug effects ; Synaptic Potentials - physiology</subject><ispartof>Neuron (Cambridge, Mass.), 2011-09, Vol.71 (5), p.911-925</ispartof><rights>2011 Elsevier Inc.</rights><rights>Copyright © 2011 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Sep 8, 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c533t-35cb1dfcd6c3c0835820921f502d6a5be8739224b9c9370a120a7304c60753243</citedby><cites>FETCH-LOGICAL-c533t-35cb1dfcd6c3c0835820921f502d6a5be8739224b9c9370a120a7304c60753243</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.neuron.2011.06.028$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21903083$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kopp-Scheinpflug, Cornelia</creatorcontrib><creatorcontrib>Tozer, Adam J.B.</creatorcontrib><creatorcontrib>Robinson, Susan W.</creatorcontrib><creatorcontrib>Tempel, Bruce L.</creatorcontrib><creatorcontrib>Hennig, Matthias H.</creatorcontrib><creatorcontrib>Forsythe, Ian D.</creatorcontrib><title>The Sound of Silence: Ionic Mechanisms Encoding Sound Termination</title><title>Neuron (Cambridge, Mass.)</title><addtitle>Neuron</addtitle><description>Offset responses upon termination of a stimulus are crucial for perceptual grouping and gap detection. These gaps are key features of vocal communication, but an ionic mechanism capable of generating fast offsets from auditory stimuli has proven elusive. Offset firing arises in the brainstem superior paraolivary nucleus (SPN), which receives powerful inhibition during sound and converts this into precise action potential (AP) firing upon sound termination. Whole-cell patch recording in vitro showed that offset firing was triggered by IPSPs rather than EPSPs. We show that AP firing can emerge from inhibition through integration of large IPSPs, driven by an extremely negative chloride reversal potential (ECl), combined with a large hyperpolarization-activated nonspecific cationic current (IH), with a secondary contribution from a T-type calcium conductance (ITCa). On activation by the IPSP, IH potently accelerates the membrane time constant, so when the sound ceases, a rapid repolarization triggers multiple offset APs that match onset timing accuracy.
► Offset responses encode the termination of a sensory synaptic stimulus ► SPN neurons have an intrinsic ionic mechanism to generate offset firing from IPSPs ► KCC2 is required to maintain low internal chloride which results in large IPSPs ► Large IPSPs trigger IH, accelerating tau, and mediate fast offset firing</description><subject>Acoustic Stimulation - methods</subject><subject>Action Potentials - drug effects</subject><subject>Action Potentials - physiology</subject><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Auditory Pathways - physiology</subject><subject>Biophysics</subject><subject>Calcium - metabolism</subject><subject>Calcium Channel Blockers - pharmacology</subject><subject>Calcium Channels, T-Type - metabolism</subject><subject>Chlorides - metabolism</subject><subject>Computer Simulation</subject><subject>Cyclic Nucleotide-Gated Cation Channels - deficiency</subject><subject>Electric Stimulation</subject><subject>Experiments</subject><subject>Functional Laterality</subject><subject>Furosemide - pharmacology</subject><subject>Gene Expression Regulation - genetics</subject><subject>Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels</subject><subject>In Vitro Techniques</subject><subject>Ion Channel Gating - genetics</subject><subject>Ion Channel Gating - physiology</subject><subject>K Cl- Cotransporters</subject><subject>Mammals</subject><subject>Mibefradil - pharmacology</subject><subject>Mice</subject><subject>Mice, Inbred CBA</subject><subject>Mice, Knockout</subject><subject>Models, Neurological</subject><subject>Neurons</subject><subject>Neurons - drug effects</subject><subject>Neurons - physiology</subject><subject>Olivary Nucleus - cytology</subject><subject>Patch-Clamp Techniques - methods</subject><subject>Potassium</subject><subject>Potassium Channels - deficiency</subject><subject>Psychoacoustics</subject><subject>Pyrimidines - pharmacology</subject><subject>Reaction Time - drug effects</subject><subject>Reaction Time - genetics</subject><subject>Reaction Time - physiology</subject><subject>Sodium Potassium Chloride Symporter Inhibitors - pharmacology</subject><subject>Sound</subject><subject>Statistical methods</subject><subject>Stilbamidines - metabolism</subject><subject>Symporters - metabolism</subject><subject>Synaptic Potentials - drug effects</subject><subject>Synaptic Potentials - physiology</subject><issn>0896-6273</issn><issn>1097-4199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kD1PwzAURS0EoqXwDxCKxMCU8J4dOzEDUoX4kooYKLOVOg64auxiJ0j8e1K1MDAwveXce58OIacIGQKKy2XmTB-8yyggZiAyoOUeGSPIIs1Ryn0yhlKKVNCCjchRjEsAzLnEQzKiKIFBycZkOn83yYvvXZ34JnmxK-O0uUoevbM6eTL6vXI2tjG5ddrX1r3t2LkJrXVVZ707JgdNtYrmZHcn5PXudn7zkM6e7x9vprNUc8a6lHG9wLrRtdBMD9O8pCApNhxoLSq-MGXBJKX5QmrJCqiQQlUwyLWAgjOaswm52Paug__oTexUa6M2q1XljO-jklBgwanAgTz_Qy59H9zwnEKeS8nLUtKByreUDj7GYBq1DratwpdCUBvDaqm2htXGsAKhBsND7GxX3i9aU_-GfpQOwPUWMIOMT2uCitpurNY2GN2p2tv_F74BoaqLew</recordid><startdate>20110908</startdate><enddate>20110908</enddate><creator>Kopp-Scheinpflug, Cornelia</creator><creator>Tozer, Adam J.B.</creator><creator>Robinson, Susan W.</creator><creator>Tempel, Bruce L.</creator><creator>Hennig, Matthias H.</creator><creator>Forsythe, Ian D.</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><scope>6I.</scope><scope>AAFTH</scope><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>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope></search><sort><creationdate>20110908</creationdate><title>The Sound of Silence: Ionic Mechanisms Encoding Sound Termination</title><author>Kopp-Scheinpflug, Cornelia ; Tozer, Adam J.B. ; Robinson, Susan W. ; Tempel, Bruce L. ; Hennig, Matthias H. ; Forsythe, Ian D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c533t-35cb1dfcd6c3c0835820921f502d6a5be8739224b9c9370a120a7304c60753243</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Acoustic Stimulation - methods</topic><topic>Action Potentials - drug effects</topic><topic>Action Potentials - physiology</topic><topic>Animals</topic><topic>Animals, Newborn</topic><topic>Auditory Pathways - physiology</topic><topic>Biophysics</topic><topic>Calcium - metabolism</topic><topic>Calcium Channel Blockers - pharmacology</topic><topic>Calcium Channels, T-Type - metabolism</topic><topic>Chlorides - metabolism</topic><topic>Computer Simulation</topic><topic>Cyclic Nucleotide-Gated Cation Channels - deficiency</topic><topic>Electric Stimulation</topic><topic>Experiments</topic><topic>Functional Laterality</topic><topic>Furosemide - pharmacology</topic><topic>Gene Expression Regulation - genetics</topic><topic>Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels</topic><topic>In Vitro Techniques</topic><topic>Ion Channel Gating - genetics</topic><topic>Ion Channel Gating - physiology</topic><topic>K Cl- Cotransporters</topic><topic>Mammals</topic><topic>Mibefradil - pharmacology</topic><topic>Mice</topic><topic>Mice, Inbred CBA</topic><topic>Mice, Knockout</topic><topic>Models, Neurological</topic><topic>Neurons</topic><topic>Neurons - drug effects</topic><topic>Neurons - physiology</topic><topic>Olivary Nucleus - cytology</topic><topic>Patch-Clamp Techniques - methods</topic><topic>Potassium</topic><topic>Potassium Channels - deficiency</topic><topic>Psychoacoustics</topic><topic>Pyrimidines - pharmacology</topic><topic>Reaction Time - drug effects</topic><topic>Reaction Time - genetics</topic><topic>Reaction Time - physiology</topic><topic>Sodium Potassium Chloride Symporter Inhibitors - pharmacology</topic><topic>Sound</topic><topic>Statistical methods</topic><topic>Stilbamidines - metabolism</topic><topic>Symporters - metabolism</topic><topic>Synaptic Potentials - drug effects</topic><topic>Synaptic Potentials - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kopp-Scheinpflug, Cornelia</creatorcontrib><creatorcontrib>Tozer, Adam J.B.</creatorcontrib><creatorcontrib>Robinson, Susan W.</creatorcontrib><creatorcontrib>Tempel, Bruce L.</creatorcontrib><creatorcontrib>Hennig, Matthias H.</creatorcontrib><creatorcontrib>Forsythe, Ian D.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</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>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>Neuron (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kopp-Scheinpflug, Cornelia</au><au>Tozer, Adam J.B.</au><au>Robinson, Susan W.</au><au>Tempel, Bruce L.</au><au>Hennig, Matthias H.</au><au>Forsythe, Ian D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Sound of Silence: Ionic Mechanisms Encoding Sound Termination</atitle><jtitle>Neuron (Cambridge, Mass.)</jtitle><addtitle>Neuron</addtitle><date>2011-09-08</date><risdate>2011</risdate><volume>71</volume><issue>5</issue><spage>911</spage><epage>925</epage><pages>911-925</pages><issn>0896-6273</issn><eissn>1097-4199</eissn><abstract>Offset responses upon termination of a stimulus are crucial for perceptual grouping and gap detection. These gaps are key features of vocal communication, but an ionic mechanism capable of generating fast offsets from auditory stimuli has proven elusive. Offset firing arises in the brainstem superior paraolivary nucleus (SPN), which receives powerful inhibition during sound and converts this into precise action potential (AP) firing upon sound termination. Whole-cell patch recording in vitro showed that offset firing was triggered by IPSPs rather than EPSPs. We show that AP firing can emerge from inhibition through integration of large IPSPs, driven by an extremely negative chloride reversal potential (ECl), combined with a large hyperpolarization-activated nonspecific cationic current (IH), with a secondary contribution from a T-type calcium conductance (ITCa). On activation by the IPSP, IH potently accelerates the membrane time constant, so when the sound ceases, a rapid repolarization triggers multiple offset APs that match onset timing accuracy.
► Offset responses encode the termination of a sensory synaptic stimulus ► SPN neurons have an intrinsic ionic mechanism to generate offset firing from IPSPs ► KCC2 is required to maintain low internal chloride which results in large IPSPs ► Large IPSPs trigger IH, accelerating tau, and mediate fast offset firing</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>21903083</pmid><doi>10.1016/j.neuron.2011.06.028</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0896-6273 |
| ispartof | Neuron (Cambridge, Mass.), 2011-09, Vol.71 (5), p.911-925 |
| issn | 0896-6273 1097-4199 |
| language | eng |
| recordid | cdi_proquest_miscellaneous_907175261 |
| source | MEDLINE; Elsevier ScienceDirect Journals Complete; Free E-Journal (出版社公開部分のみ）; Cell Press Free Archives(OpenAccess) |
| subjects | Acoustic Stimulation - methods Action Potentials - drug effects Action Potentials - physiology Animals Animals, Newborn Auditory Pathways - physiology Biophysics Calcium - metabolism Calcium Channel Blockers - pharmacology Calcium Channels, T-Type - metabolism Chlorides - metabolism Computer Simulation Cyclic Nucleotide-Gated Cation Channels - deficiency Electric Stimulation Experiments Functional Laterality Furosemide - pharmacology Gene Expression Regulation - genetics Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels In Vitro Techniques Ion Channel Gating - genetics Ion Channel Gating - physiology K Cl- Cotransporters Mammals Mibefradil - pharmacology Mice Mice, Inbred CBA Mice, Knockout Models, Neurological Neurons Neurons - drug effects Neurons - physiology Olivary Nucleus - cytology Patch-Clamp Techniques - methods Potassium Potassium Channels - deficiency Psychoacoustics Pyrimidines - pharmacology Reaction Time - drug effects Reaction Time - genetics Reaction Time - physiology Sodium Potassium Chloride Symporter Inhibitors - pharmacology Sound Statistical methods Stilbamidines - metabolism Symporters - metabolism Synaptic Potentials - drug effects Synaptic Potentials - physiology |
| title | The Sound of Silence: Ionic Mechanisms Encoding Sound Termination |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-28T07%3A31%3A48IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=The%20Sound%20of%20Silence:%20Ionic%20Mechanisms%20Encoding%20Sound%20Termination&rft.jtitle=Neuron%20(Cambridge,%20Mass.)&rft.au=Kopp-Scheinpflug,%20Cornelia&rft.date=2011-09-08&rft.volume=71&rft.issue=5&rft.spage=911&rft.epage=925&rft.pages=911-925&rft.issn=0896-6273&rft.eissn=1097-4199&rft_id=info:doi/10.1016/j.neuron.2011.06.028&rft_dat=%3Cproquest_cross%3E3388955201%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1549958892&rft_id=info:pmid/21903083&rft_els_id=S0896627311005587&rfr_iscdi=true |