The origin of the skewed amplitude distribution of spontaneous excitatory junction potentials in poorly coupled smooth muscle cells

Abstract The skewed amplitude distribution of spontaneous excitatory junction potentials (sEJPs) in the mouse vas deferens and other electrically-coupled smooth muscle syncytia has been attributed to electrically-attenuated depolarizations resulting from the spontaneous release of quantized packets...

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Veröffentlicht in:Neuroscience 2007-03, Vol.145 (1), p.153-161
Hauptverfasser: Young, J.S, Brain, K.L, Cunnane, T.C
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Brain, K.L
Cunnane, T.C
description Abstract The skewed amplitude distribution of spontaneous excitatory junction potentials (sEJPs) in the mouse vas deferens and other electrically-coupled smooth muscle syncytia has been attributed to electrically-attenuated depolarizations resulting from the spontaneous release of quantized packets of ATP acting on remote smooth muscle cells (SMCs). However, in the present investigation surface SMCs of the mouse isolated vas deferens were poorly electrically coupled, with input resistances (176±18 MΩ, range: 141–221 MΩ, n =4) similar to those of dissociated cells. Furthermore, the amplitude of evoked EJPs was more variable in surface compared with deeper SMCs ( F test, F =17.4, P
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However, in the present investigation surface SMCs of the mouse isolated vas deferens were poorly electrically coupled, with input resistances (176±18 MΩ, range: 141–221 MΩ, n =4) similar to those of dissociated cells. Furthermore, the amplitude of evoked EJPs was more variable in surface compared with deeper SMCs ( F test, F =17.4, P &lt;0.0001). Using simultaneous electrophysiology and confocal microscopy to investigate these poorly-coupled cells, it is shown that α-latrotoxin-stimulated sEJPs correlate, in timing (median delay ranged from −30 to −57 ms, P &lt;0.05 in all experiments, n =5) and amplitude (Pearson product moment correlation, ρ&gt;0.55 and P &lt;0.001), with purinergic neuroeffector Ca2+ transients (NCTs) in SMCs. The temporal correlation between sEJPs of widely ranging amplitude with NCTs in the impaled SMC demonstrates that all sEJPs could arise from neurotransmitter action on the impaled cell and that the skewed distribution of sEJPs can be explained by the variable effect of packets of ATP on a single SMC. The amplitude correlation of sEJPs and NCTs argues against the attenuation of electrical signal amplitude along the length of a single SMC. 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However, in the present investigation surface SMCs of the mouse isolated vas deferens were poorly electrically coupled, with input resistances (176±18 MΩ, range: 141–221 MΩ, n =4) similar to those of dissociated cells. Furthermore, the amplitude of evoked EJPs was more variable in surface compared with deeper SMCs ( F test, F =17.4, P &lt;0.0001). Using simultaneous electrophysiology and confocal microscopy to investigate these poorly-coupled cells, it is shown that α-latrotoxin-stimulated sEJPs correlate, in timing (median delay ranged from −30 to −57 ms, P &lt;0.05 in all experiments, n =5) and amplitude (Pearson product moment correlation, ρ&gt;0.55 and P &lt;0.001), with purinergic neuroeffector Ca2+ transients (NCTs) in SMCs. The temporal correlation between sEJPs of widely ranging amplitude with NCTs in the impaled SMC demonstrates that all sEJPs could arise from neurotransmitter action on the impaled cell and that the skewed distribution of sEJPs can be explained by the variable effect of packets of ATP on a single SMC. The amplitude correlation of sEJPs and NCTs argues against the attenuation of electrical signal amplitude along the length of a single SMC. The skewed sEJP amplitude distribution arising from neurotransmitter release on single SMCs is consistent with a broad neurotransmitter packet size distribution at sympathetic neuroeffector junctions.</description><subject>Adenosine Triphosphate - metabolism</subject><subject>Animals</subject><subject>ATP</subject><subject>Biological and medical sciences</subject><subject>calcium imaging</subject><subject>Calcium Signaling - drug effects</subject><subject>Calcium Signaling - physiology</subject><subject>Cellular Neuroscience</subject><subject>confocal microscopy</subject><subject>Dose-Response Relationship, Immunologic</subject><subject>Electric Impedance</subject><subject>Electric Stimulation - methods</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>In Vitro Techniques</subject><subject>Male</subject><subject>Membrane Potentials - drug effects</subject><subject>Membrane Potentials - physiology</subject><subject>Membrane Potentials - radiation effects</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Microscopy, Confocal - methods</subject><subject>Myocytes, Smooth Muscle - physiology</subject><subject>Neurology</subject><subject>Neuromuscular Junction - drug effects</subject><subject>Neuromuscular Junction - physiology</subject><subject>neurotransmission</subject><subject>sEJP</subject><subject>smooth muscle</subject><subject>Spider Venoms - pharmacology</subject><subject>Time Factors</subject><subject>Vas Deferens - cytology</subject><subject>Vertebrates: nervous system and sense organs</subject><issn>0306-4522</issn><issn>1873-7544</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2007</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkk1v1DAQhi0EosvCX0AWEtx28diJk3CoVJVPqRIHytnyOpOut4kdbKewZ_44TndFCxfIJbH85PV4niHkBbA1MJCvd2uHU_DRWHQG15wxuQZYs7J4QBZQV2JVlUXxkCyYYHJVlJyfkCcx7lh-ykI8JidQcVaLGhbk5-UWqQ_2yjrqO5ryKl7jd2ypHsbepqlF2tqYgt1MyfpbKI7eJe3QT5HiD2OTTj7s6W5y5hYZfUKXrO4jtfPKh35PjZ_GPsfGwfu0pcMUTY_UYN_Hp-RRl2F8dnwvydf37y7PP64uPn_4dH52sTKSQVpxwWpZVA3vGDQlSGSSYSd1C7LMn502EnTVtRuxEWXBoRAbwwVUrGixQKHFkpwecsdpM2BrcpFB92oMdtBhr7y26s8dZ7fqyt8onrsGTOaAV8eA4L9NGJMabJyvcGiGkg0DLsrmnyA0spFVrnBJ3hxAk33GgN3vaoCpWbbaqfuy1SxbAahZ5JI8v3-fu1-PdjPw8gjoaHTfBe2MjXdcXeY-1Txzbw8c5u7fWAzqeFxrA5qkWm__r57Tv2JMb53NJ1_jHuPOT8FlvwpU5IqpL_N4ztOZ5WWFeW5_AeC26B8</recordid><startdate>20070302</startdate><enddate>20070302</enddate><creator>Young, J.S</creator><creator>Brain, K.L</creator><creator>Cunnane, T.C</creator><general>Elsevier Ltd</general><general>Elsevier</general><general>Elsevier Science</general><scope>6I.</scope><scope>AAFTH</scope><scope>IQODW</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>7TK</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20070302</creationdate><title>The origin of the skewed amplitude distribution of spontaneous excitatory junction potentials in poorly coupled smooth muscle cells</title><author>Young, J.S ; Brain, K.L ; Cunnane, T.C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c601t-230864792f019516e060ef6ad165060fac61a7fdb3b3542143bc231704de4e3a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2007</creationdate><topic>Adenosine Triphosphate - metabolism</topic><topic>Animals</topic><topic>ATP</topic><topic>Biological and medical sciences</topic><topic>calcium imaging</topic><topic>Calcium Signaling - drug effects</topic><topic>Calcium Signaling - physiology</topic><topic>Cellular Neuroscience</topic><topic>confocal microscopy</topic><topic>Dose-Response Relationship, Immunologic</topic><topic>Electric Impedance</topic><topic>Electric Stimulation - methods</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>In Vitro Techniques</topic><topic>Male</topic><topic>Membrane Potentials - drug effects</topic><topic>Membrane Potentials - physiology</topic><topic>Membrane Potentials - radiation effects</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Microscopy, Confocal - methods</topic><topic>Myocytes, Smooth Muscle - physiology</topic><topic>Neurology</topic><topic>Neuromuscular Junction - drug effects</topic><topic>Neuromuscular Junction - physiology</topic><topic>neurotransmission</topic><topic>sEJP</topic><topic>smooth muscle</topic><topic>Spider Venoms - pharmacology</topic><topic>Time Factors</topic><topic>Vas Deferens - cytology</topic><topic>Vertebrates: nervous system and sense organs</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Young, J.S</creatorcontrib><creatorcontrib>Brain, K.L</creatorcontrib><creatorcontrib>Cunnane, T.C</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Young, J.S</au><au>Brain, K.L</au><au>Cunnane, T.C</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The origin of the skewed amplitude distribution of spontaneous excitatory junction potentials in poorly coupled smooth muscle cells</atitle><jtitle>Neuroscience</jtitle><addtitle>Neuroscience</addtitle><date>2007-03-02</date><risdate>2007</risdate><volume>145</volume><issue>1</issue><spage>153</spage><epage>161</epage><pages>153-161</pages><issn>0306-4522</issn><eissn>1873-7544</eissn><coden>NRSCDN</coden><abstract>Abstract The skewed amplitude distribution of spontaneous excitatory junction potentials (sEJPs) in the mouse vas deferens and other electrically-coupled smooth muscle syncytia has been attributed to electrically-attenuated depolarizations resulting from the spontaneous release of quantized packets of ATP acting on remote smooth muscle cells (SMCs). However, in the present investigation surface SMCs of the mouse isolated vas deferens were poorly electrically coupled, with input resistances (176±18 MΩ, range: 141–221 MΩ, n =4) similar to those of dissociated cells. Furthermore, the amplitude of evoked EJPs was more variable in surface compared with deeper SMCs ( F test, F =17.4, P &lt;0.0001). Using simultaneous electrophysiology and confocal microscopy to investigate these poorly-coupled cells, it is shown that α-latrotoxin-stimulated sEJPs correlate, in timing (median delay ranged from −30 to −57 ms, P &lt;0.05 in all experiments, n =5) and amplitude (Pearson product moment correlation, ρ&gt;0.55 and P &lt;0.001), with purinergic neuroeffector Ca2+ transients (NCTs) in SMCs. The temporal correlation between sEJPs of widely ranging amplitude with NCTs in the impaled SMC demonstrates that all sEJPs could arise from neurotransmitter action on the impaled cell and that the skewed distribution of sEJPs can be explained by the variable effect of packets of ATP on a single SMC. The amplitude correlation of sEJPs and NCTs argues against the attenuation of electrical signal amplitude along the length of a single SMC. The skewed sEJP amplitude distribution arising from neurotransmitter release on single SMCs is consistent with a broad neurotransmitter packet size distribution at sympathetic neuroeffector junctions.</abstract><cop>Oxford</cop><pub>Elsevier Ltd</pub><pmid>17208381</pmid><doi>10.1016/j.neuroscience.2006.11.054</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record>
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subjects Adenosine Triphosphate - metabolism
Animals
ATP
Biological and medical sciences
calcium imaging
Calcium Signaling - drug effects
Calcium Signaling - physiology
Cellular Neuroscience
confocal microscopy
Dose-Response Relationship, Immunologic
Electric Impedance
Electric Stimulation - methods
Fundamental and applied biological sciences. Psychology
In Vitro Techniques
Male
Membrane Potentials - drug effects
Membrane Potentials - physiology
Membrane Potentials - radiation effects
Mice
Mice, Inbred BALB C
Microscopy, Confocal - methods
Myocytes, Smooth Muscle - physiology
Neurology
Neuromuscular Junction - drug effects
Neuromuscular Junction - physiology
neurotransmission
sEJP
smooth muscle
Spider Venoms - pharmacology
Time Factors
Vas Deferens - cytology
Vertebrates: nervous system and sense organs
title The origin of the skewed amplitude distribution of spontaneous excitatory junction potentials in poorly coupled smooth muscle cells
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