The Passive Cable Properties of Hair Cell Stereocilia and Their Contribution to Somatic Capacitance Measurements
Somatic measurements of whole-cell capacitance are routinely used to understand physiologic events occurring in remote portions of cells. These studies often assume the intracellular space is voltage-clamped. We questioned this assumption in auditory and vestibular hair cells with respect to their s...
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description | Somatic measurements of whole-cell capacitance are routinely used to understand physiologic events occurring in remote portions of cells. These studies often assume the intracellular space is voltage-clamped. We questioned this assumption in auditory and vestibular hair cells with respect to their stereocilia based on earlier studies showing that neurons, with radial dimensions similar to stereocilia, are not always isopotential under voltage-clamp. To explore this, we modeled the stereocilia as passive cables with transduction channels located at their tips. We found that the input capacitance measured at the soma changes when the transduction channels at the tips of the stereocilia are open compared to when the channels are closed. The maximum capacitance is felt with the transducer closed but will decrease as the transducer opens due to a length-dependent voltage drop along the stereocilium length. This potential drop is proportional to the intracellular resistance and stereocilium tip conductance and can produce a maximum capacitance error on the order of fF for single stereocilia and pF for the bundle. |
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These studies often assume the intracellular space is voltage-clamped. We questioned this assumption in auditory and vestibular hair cells with respect to their stereocilia based on earlier studies showing that neurons, with radial dimensions similar to stereocilia, are not always isopotential under voltage-clamp. To explore this, we modeled the stereocilia as passive cables with transduction channels located at their tips. We found that the input capacitance measured at the soma changes when the transduction channels at the tips of the stereocilia are open compared to when the channels are closed. The maximum capacitance is felt with the transducer closed but will decrease as the transducer opens due to a length-dependent voltage drop along the stereocilium length. This potential drop is proportional to the intracellular resistance and stereocilium tip conductance and can produce a maximum capacitance error on the order of fF for single stereocilia and pF for the bundle.</description><identifier>ISSN: 0006-3495</identifier><identifier>EISSN: 1542-0086</identifier><identifier>DOI: 10.1529/biophysj.108.137356</identifier><identifier>PMID: 18849411</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Algorithms ; Animals ; Biochemistry ; Biophysical Theory and Modeling ; Chinchilla ; Cilia - physiology ; Cilia - ultrastructure ; Computer Simulation ; Electric Capacitance ; Electric Impedance ; Hair Cells, Auditory - physiology ; Hair Cells, Auditory - ultrastructure ; Hair Cells, Vestibular - physiology ; Hair Cells, Vestibular - ultrastructure ; Intracellular Space - physiology ; Membrane Potentials - physiology ; Models, Neurological ; Neurons ; Patch-Clamp Techniques - methods ; Signal transduction ; Studies ; Turtles</subject><ispartof>Biophysical journal, 2009-01, Vol.96 (1), p.1-8</ispartof><rights>2009 Biophysical Society</rights><rights>Copyright Biophysical Society Jan 7, 2009</rights><rights>2009 by the Biophysical Society.. 2009 Biophysical Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c485t-138f23ce6a9c3702a30cf84b61c32c693e64e8e415a48da81661c686c20a36993</citedby><cites>FETCH-LOGICAL-c485t-138f23ce6a9c3702a30cf84b61c32c693e64e8e415a48da81661c686c20a36993</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/PMC2710037/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://dx.doi.org/10.1529/biophysj.108.137356$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,3550,27924,27925,45995,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18849411$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Breneman, Kathryn D.</creatorcontrib><creatorcontrib>Highstein, Stephen M.</creatorcontrib><creatorcontrib>Boyle, Richard D.</creatorcontrib><creatorcontrib>Rabbitt, Richard D.</creatorcontrib><title>The Passive Cable Properties of Hair Cell Stereocilia and Their Contribution to Somatic Capacitance Measurements</title><title>Biophysical journal</title><addtitle>Biophys J</addtitle><description>Somatic measurements of whole-cell capacitance are routinely used to understand physiologic events occurring in remote portions of cells. These studies often assume the intracellular space is voltage-clamped. We questioned this assumption in auditory and vestibular hair cells with respect to their stereocilia based on earlier studies showing that neurons, with radial dimensions similar to stereocilia, are not always isopotential under voltage-clamp. To explore this, we modeled the stereocilia as passive cables with transduction channels located at their tips. We found that the input capacitance measured at the soma changes when the transduction channels at the tips of the stereocilia are open compared to when the channels are closed. The maximum capacitance is felt with the transducer closed but will decrease as the transducer opens due to a length-dependent voltage drop along the stereocilium length. This potential drop is proportional to the intracellular resistance and stereocilium tip conductance and can produce a maximum capacitance error on the order of fF for single stereocilia and pF for the bundle.</description><subject>Algorithms</subject><subject>Animals</subject><subject>Biochemistry</subject><subject>Biophysical Theory and Modeling</subject><subject>Chinchilla</subject><subject>Cilia - physiology</subject><subject>Cilia - ultrastructure</subject><subject>Computer Simulation</subject><subject>Electric Capacitance</subject><subject>Electric Impedance</subject><subject>Hair Cells, Auditory - physiology</subject><subject>Hair Cells, Auditory - ultrastructure</subject><subject>Hair Cells, Vestibular - physiology</subject><subject>Hair Cells, Vestibular - ultrastructure</subject><subject>Intracellular Space - physiology</subject><subject>Membrane Potentials - physiology</subject><subject>Models, Neurological</subject><subject>Neurons</subject><subject>Patch-Clamp Techniques - methods</subject><subject>Signal transduction</subject><subject>Studies</subject><subject>Turtles</subject><issn>0006-3495</issn><issn>1542-0086</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9UU1v1DAUtBCILgu_AAlZXDhla8eO1zmAVK2gRSoCqeVsvTgvrFdJHGxnpf77erVboD1wsp5n5n3MEPKWsxWvyvq8cX7a3sXdijO94mItKvWMLHgly4IxrZ6TBWNMFULW1Rl5FeOOMV5WjL8kZ1xrWUvOF2S63SL9ATG6PdINNH2ugp8wJIeR-o5egQt0g31PbxIG9Nb1DiiMLc3KA-THFFwzJ-dHmjy98QMkZ3OvCaxLMFqk3xDiHHDAMcXX5EUHfcQ3p3dJfn75fLu5Kq6_X37dXFwXVuoqFVzorhQWFdRWrFkJgtlOy0ZxK0qraoFKokbJK5C6Bc1VRpRWtmQgVF2LJfl07DvNzYCtzbMD9GYKboBwZzw48xgZ3db88ntTrjlj2c0l-XBqEPzvGWMyg4s2GwEj-jmatZA8W8h1Zr5_wtz5OYz5OlPy6rCMrDJJHEk2-BgDdn9W4cwc8jQPeeYPbY55ZtW7f6_4qzkFmAkfjwTMXu4dBhOtw2x66wLaZFrv_jvgHsOWtDc</recordid><startdate>200901</startdate><enddate>200901</enddate><creator>Breneman, Kathryn D.</creator><creator>Highstein, Stephen M.</creator><creator>Boyle, Richard D.</creator><creator>Rabbitt, Richard D.</creator><general>Elsevier Inc</general><general>Biophysical Society</general><general>The Biophysical Society</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>7QO</scope><scope>7QP</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>200901</creationdate><title>The Passive Cable Properties of Hair Cell Stereocilia and Their Contribution to Somatic Capacitance Measurements</title><author>Breneman, Kathryn D. ; Highstein, Stephen M. ; Boyle, Richard D. ; Rabbitt, Richard D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c485t-138f23ce6a9c3702a30cf84b61c32c693e64e8e415a48da81661c686c20a36993</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Algorithms</topic><topic>Animals</topic><topic>Biochemistry</topic><topic>Biophysical Theory and Modeling</topic><topic>Chinchilla</topic><topic>Cilia - physiology</topic><topic>Cilia - ultrastructure</topic><topic>Computer Simulation</topic><topic>Electric Capacitance</topic><topic>Electric Impedance</topic><topic>Hair Cells, Auditory - physiology</topic><topic>Hair Cells, Auditory - ultrastructure</topic><topic>Hair Cells, Vestibular - physiology</topic><topic>Hair Cells, Vestibular - ultrastructure</topic><topic>Intracellular Space - physiology</topic><topic>Membrane Potentials - physiology</topic><topic>Models, Neurological</topic><topic>Neurons</topic><topic>Patch-Clamp Techniques - methods</topic><topic>Signal transduction</topic><topic>Studies</topic><topic>Turtles</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Breneman, Kathryn D.</creatorcontrib><creatorcontrib>Highstein, Stephen M.</creatorcontrib><creatorcontrib>Boyle, Richard D.</creatorcontrib><creatorcontrib>Rabbitt, Richard 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>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</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>Biophysical journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Breneman, Kathryn D.</au><au>Highstein, Stephen M.</au><au>Boyle, Richard D.</au><au>Rabbitt, Richard D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The Passive Cable Properties of Hair Cell Stereocilia and Their Contribution to Somatic Capacitance Measurements</atitle><jtitle>Biophysical journal</jtitle><addtitle>Biophys J</addtitle><date>2009-01</date><risdate>2009</risdate><volume>96</volume><issue>1</issue><spage>1</spage><epage>8</epage><pages>1-8</pages><issn>0006-3495</issn><eissn>1542-0086</eissn><abstract>Somatic measurements of whole-cell capacitance are routinely used to understand physiologic events occurring in remote portions of cells. These studies often assume the intracellular space is voltage-clamped. We questioned this assumption in auditory and vestibular hair cells with respect to their stereocilia based on earlier studies showing that neurons, with radial dimensions similar to stereocilia, are not always isopotential under voltage-clamp. To explore this, we modeled the stereocilia as passive cables with transduction channels located at their tips. We found that the input capacitance measured at the soma changes when the transduction channels at the tips of the stereocilia are open compared to when the channels are closed. The maximum capacitance is felt with the transducer closed but will decrease as the transducer opens due to a length-dependent voltage drop along the stereocilium length. 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subjects | Algorithms Animals Biochemistry Biophysical Theory and Modeling Chinchilla Cilia - physiology Cilia - ultrastructure Computer Simulation Electric Capacitance Electric Impedance Hair Cells, Auditory - physiology Hair Cells, Auditory - ultrastructure Hair Cells, Vestibular - physiology Hair Cells, Vestibular - ultrastructure Intracellular Space - physiology Membrane Potentials - physiology Models, Neurological Neurons Patch-Clamp Techniques - methods Signal transduction Studies Turtles |
title | The Passive Cable Properties of Hair Cell Stereocilia and Their Contribution to Somatic Capacitance Measurements |
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