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High Threshold, Proximal Initiation, and Slow Conduction Velocity of Action Potentials in Dentate Granule Neuron Mossy Fibers
Departments of 1 Psychiatry and 2 Anatomy and Neurobiology and 3 Program in Neuroscience, Washington University School of Medicine, St. Louis, Missouri Submitted 22 February 2008; accepted in final form 12 May 2008 Dentate granule neurons give rise to some of the smallest unmyelinated fibers in the...
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Published in: | Journal of neurophysiology 2008-07, Vol.100 (1), p.281-291 |
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creator | Kress, Geraldine J Dowling, Margaret J Meeks, Julian P Mennerick, Steven |
description | Departments of 1 Psychiatry and 2 Anatomy and Neurobiology and 3 Program in Neuroscience, Washington University School of Medicine, St. Louis, Missouri
Submitted 22 February 2008;
accepted in final form 12 May 2008
Dentate granule neurons give rise to some of the smallest unmyelinated fibers in the mammalian CNS, the hippocampal mossy fibers. These neurons are also key regulators of physiological and pathophysiological information flow through the hippocampus. We took a comparative approach to studying mossy fiber action potential initiation and propagation in hippocampal slices from juvenile rats. Dentate granule neurons exhibited axonal action potential initiation significantly more proximal than CA3 pyramidal neurons. This conclusion was suggested by phase plot analysis of somatic action potentials and by local tetrodotoxin application to the axon and somatodendritic compartments. This conclusion was also verified by immunostaining for voltage-gated sodium channel alpha subunits and by direct dual soma/axonal recordings. Dentate neurons exhibited a significantly higher action potential threshold and slower axonal conduction velocity than CA3 neurons. We conclude that while the electrotonically proximal axon location of action potential initiation allows granule neurons to sensitively detect and integrate synaptic inputs, the neurons are sluggish to initiate and propagate an action potential.
Address for reprint requests and other correspondence: S. Mennerick, Dept. of Psychiatry, Washington University School of Medicine, 660 S. Euclid Ave., Campus Box 8134, St. Louis, MO 63110 (E-mail: menneris{at}psychiatry.wustl.edu ) |
doi_str_mv | 10.1152/jn.90295.2008 |
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Submitted 22 February 2008;
accepted in final form 12 May 2008
Dentate granule neurons give rise to some of the smallest unmyelinated fibers in the mammalian CNS, the hippocampal mossy fibers. These neurons are also key regulators of physiological and pathophysiological information flow through the hippocampus. We took a comparative approach to studying mossy fiber action potential initiation and propagation in hippocampal slices from juvenile rats. Dentate granule neurons exhibited axonal action potential initiation significantly more proximal than CA3 pyramidal neurons. This conclusion was suggested by phase plot analysis of somatic action potentials and by local tetrodotoxin application to the axon and somatodendritic compartments. This conclusion was also verified by immunostaining for voltage-gated sodium channel alpha subunits and by direct dual soma/axonal recordings. Dentate neurons exhibited a significantly higher action potential threshold and slower axonal conduction velocity than CA3 neurons. We conclude that while the electrotonically proximal axon location of action potential initiation allows granule neurons to sensitively detect and integrate synaptic inputs, the neurons are sluggish to initiate and propagate an action potential.
Address for reprint requests and other correspondence: S. Mennerick, Dept. of Psychiatry, Washington University School of Medicine, 660 S. Euclid Ave., Campus Box 8134, St. Louis, MO 63110 (E-mail: menneris{at}psychiatry.wustl.edu )</description><identifier>ISSN: 0022-3077</identifier><identifier>EISSN: 1522-1598</identifier><identifier>DOI: 10.1152/jn.90295.2008</identifier><identifier>PMID: 18480368</identifier><language>eng</language><publisher>United States: Am Phys Soc</publisher><subject>Animals ; Animals, Newborn ; Ankyrins - metabolism ; Dendrites - physiology ; Dose-Response Relationship, Radiation ; Electric Stimulation - methods ; Hippocampus - cytology ; In Vitro Techniques ; Membrane Potentials - physiology ; Membrane Potentials - radiation effects ; Mossy Fibers, Hippocampal - physiology ; NAV1.2 Voltage-Gated Sodium Channel ; Nerve Tissue Proteins - metabolism ; Neural Conduction - physiology ; Neurons - classification ; Neurons - cytology ; Patch-Clamp Techniques ; Rats ; Rats, Sprague-Dawley ; Sodium Channel Blockers - pharmacology ; Sodium Channels - metabolism ; Tetrodotoxin - pharmacology</subject><ispartof>Journal of neurophysiology, 2008-07, Vol.100 (1), p.281-291</ispartof><rights>Copyright © 2008, American Physiological Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c527t-dfbc8731f9cb32cb14def4e49e70ac0a191b17ddab9721e033fc8067ae0a3b3f3</citedby><cites>FETCH-LOGICAL-c527t-dfbc8731f9cb32cb14def4e49e70ac0a191b17ddab9721e033fc8067ae0a3b3f3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18480368$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kress, Geraldine J</creatorcontrib><creatorcontrib>Dowling, Margaret J</creatorcontrib><creatorcontrib>Meeks, Julian P</creatorcontrib><creatorcontrib>Mennerick, Steven</creatorcontrib><title>High Threshold, Proximal Initiation, and Slow Conduction Velocity of Action Potentials in Dentate Granule Neuron Mossy Fibers</title><title>Journal of neurophysiology</title><addtitle>J Neurophysiol</addtitle><description>Departments of 1 Psychiatry and 2 Anatomy and Neurobiology and 3 Program in Neuroscience, Washington University School of Medicine, St. Louis, Missouri
Submitted 22 February 2008;
accepted in final form 12 May 2008
Dentate granule neurons give rise to some of the smallest unmyelinated fibers in the mammalian CNS, the hippocampal mossy fibers. These neurons are also key regulators of physiological and pathophysiological information flow through the hippocampus. We took a comparative approach to studying mossy fiber action potential initiation and propagation in hippocampal slices from juvenile rats. Dentate granule neurons exhibited axonal action potential initiation significantly more proximal than CA3 pyramidal neurons. This conclusion was suggested by phase plot analysis of somatic action potentials and by local tetrodotoxin application to the axon and somatodendritic compartments. This conclusion was also verified by immunostaining for voltage-gated sodium channel alpha subunits and by direct dual soma/axonal recordings. Dentate neurons exhibited a significantly higher action potential threshold and slower axonal conduction velocity than CA3 neurons. We conclude that while the electrotonically proximal axon location of action potential initiation allows granule neurons to sensitively detect and integrate synaptic inputs, the neurons are sluggish to initiate and propagate an action potential.
Address for reprint requests and other correspondence: S. Mennerick, Dept. of Psychiatry, Washington University School of Medicine, 660 S. Euclid Ave., Campus Box 8134, St. Louis, MO 63110 (E-mail: menneris{at}psychiatry.wustl.edu )</description><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Ankyrins - metabolism</subject><subject>Dendrites - physiology</subject><subject>Dose-Response Relationship, Radiation</subject><subject>Electric Stimulation - methods</subject><subject>Hippocampus - cytology</subject><subject>In Vitro Techniques</subject><subject>Membrane Potentials - physiology</subject><subject>Membrane Potentials - radiation effects</subject><subject>Mossy Fibers, Hippocampal - physiology</subject><subject>NAV1.2 Voltage-Gated Sodium Channel</subject><subject>Nerve Tissue Proteins - metabolism</subject><subject>Neural Conduction - physiology</subject><subject>Neurons - classification</subject><subject>Neurons - cytology</subject><subject>Patch-Clamp Techniques</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Sodium Channel Blockers - pharmacology</subject><subject>Sodium Channels - metabolism</subject><subject>Tetrodotoxin - pharmacology</subject><issn>0022-3077</issn><issn>1522-1598</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><recordid>eNp1kU1v1DAQhi1ERZfCkSvyjUuzjO2kTi5I1ZZtK7VQqVuuluOPjVeuvXIS2hz473i7VYEDJ49mnved8QxCHwjMCano502YN0Cbak4B6ldolnO0IFVTv0YzgBwz4PwQve37DQDwCugbdEjqsgZ2Us_Qrwu37vCqS6bvotfH-CbFR3cvPb4MbnBycDEcYxk0vvXxAS9i0KPaJfEP46Nyw4Sjxaf71E0cTMgi32MX8FmO5WDweZJh9AZ_M2PK0HXs-wkvXWtS_w4d2Eyb98_vEbpbfl0tLoqr7-eXi9OrQlWUD4W2rao5I7ZRLaOqJaU2tjRlYzhIBZI0pCVca9k2nBIDjFlVwwmXBiRrmWVH6Mvedzu290arPFmSXmxT_mmaRJRO_FsJrhPr-FPQsmFlTbJBsTdQKY-fjH3REhC7O4hNEE93ELs7ZP7j3w3_0M-Lz8CnPdDl_T-4ZMS2m3oXfVxPOy8C2VfQp9bs_-Ry9H5lHocseVGIrbbsN6byp8g</recordid><startdate>20080701</startdate><enddate>20080701</enddate><creator>Kress, Geraldine J</creator><creator>Dowling, Margaret J</creator><creator>Meeks, Julian P</creator><creator>Mennerick, Steven</creator><general>Am Phys Soc</general><general>American Physiological Society</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>5PM</scope></search><sort><creationdate>20080701</creationdate><title>High Threshold, Proximal Initiation, and Slow Conduction Velocity of Action Potentials in Dentate Granule Neuron Mossy Fibers</title><author>Kress, Geraldine J ; Dowling, Margaret J ; Meeks, Julian P ; Mennerick, Steven</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c527t-dfbc8731f9cb32cb14def4e49e70ac0a191b17ddab9721e033fc8067ae0a3b3f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2008</creationdate><topic>Animals</topic><topic>Animals, Newborn</topic><topic>Ankyrins - metabolism</topic><topic>Dendrites - physiology</topic><topic>Dose-Response Relationship, Radiation</topic><topic>Electric Stimulation - methods</topic><topic>Hippocampus - cytology</topic><topic>In Vitro Techniques</topic><topic>Membrane Potentials - physiology</topic><topic>Membrane Potentials - radiation effects</topic><topic>Mossy Fibers, Hippocampal - physiology</topic><topic>NAV1.2 Voltage-Gated Sodium Channel</topic><topic>Nerve Tissue Proteins - metabolism</topic><topic>Neural Conduction - physiology</topic><topic>Neurons - classification</topic><topic>Neurons - cytology</topic><topic>Patch-Clamp Techniques</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>Sodium Channel Blockers - pharmacology</topic><topic>Sodium Channels - metabolism</topic><topic>Tetrodotoxin - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kress, Geraldine J</creatorcontrib><creatorcontrib>Dowling, Margaret J</creatorcontrib><creatorcontrib>Meeks, Julian P</creatorcontrib><creatorcontrib>Mennerick, Steven</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of neurophysiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kress, Geraldine J</au><au>Dowling, Margaret J</au><au>Meeks, Julian P</au><au>Mennerick, Steven</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>High Threshold, Proximal Initiation, and Slow Conduction Velocity of Action Potentials in Dentate Granule Neuron Mossy Fibers</atitle><jtitle>Journal of neurophysiology</jtitle><addtitle>J Neurophysiol</addtitle><date>2008-07-01</date><risdate>2008</risdate><volume>100</volume><issue>1</issue><spage>281</spage><epage>291</epage><pages>281-291</pages><issn>0022-3077</issn><eissn>1522-1598</eissn><abstract>Departments of 1 Psychiatry and 2 Anatomy and Neurobiology and 3 Program in Neuroscience, Washington University School of Medicine, St. Louis, Missouri
Submitted 22 February 2008;
accepted in final form 12 May 2008
Dentate granule neurons give rise to some of the smallest unmyelinated fibers in the mammalian CNS, the hippocampal mossy fibers. These neurons are also key regulators of physiological and pathophysiological information flow through the hippocampus. We took a comparative approach to studying mossy fiber action potential initiation and propagation in hippocampal slices from juvenile rats. Dentate granule neurons exhibited axonal action potential initiation significantly more proximal than CA3 pyramidal neurons. This conclusion was suggested by phase plot analysis of somatic action potentials and by local tetrodotoxin application to the axon and somatodendritic compartments. This conclusion was also verified by immunostaining for voltage-gated sodium channel alpha subunits and by direct dual soma/axonal recordings. Dentate neurons exhibited a significantly higher action potential threshold and slower axonal conduction velocity than CA3 neurons. We conclude that while the electrotonically proximal axon location of action potential initiation allows granule neurons to sensitively detect and integrate synaptic inputs, the neurons are sluggish to initiate and propagate an action potential.
Address for reprint requests and other correspondence: S. Mennerick, Dept. of Psychiatry, Washington University School of Medicine, 660 S. Euclid Ave., Campus Box 8134, St. Louis, MO 63110 (E-mail: menneris{at}psychiatry.wustl.edu )</abstract><cop>United States</cop><pub>Am Phys Soc</pub><pmid>18480368</pmid><doi>10.1152/jn.90295.2008</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Animals, Newborn Ankyrins - metabolism Dendrites - physiology Dose-Response Relationship, Radiation Electric Stimulation - methods Hippocampus - cytology In Vitro Techniques Membrane Potentials - physiology Membrane Potentials - radiation effects Mossy Fibers, Hippocampal - physiology NAV1.2 Voltage-Gated Sodium Channel Nerve Tissue Proteins - metabolism Neural Conduction - physiology Neurons - classification Neurons - cytology Patch-Clamp Techniques Rats Rats, Sprague-Dawley Sodium Channel Blockers - pharmacology Sodium Channels - metabolism Tetrodotoxin - pharmacology |
title | High Threshold, Proximal Initiation, and Slow Conduction Velocity of Action Potentials in Dentate Granule Neuron Mossy Fibers |
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