Axonal Na+ Channels Ensure Fast Spike Activation and Back-Propagation in Cerebellar Granule Cells
1 Department of Physiological and Pharmacological Sciences, University of Pavia, Pavia, Italy; 2 Consorzio Nazionale Interuniversitario per le Scienze Fisiche della Materia, Pavia Unit, Pavia, Italy; 3 Department of Mathematics, University of Milan, Milan, Italy; 4 and Department of Biological Scien...
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| Veröffentlicht in: | Journal of neurophysiology 2009-02, Vol.101 (2), p.519-532 |
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| creator | Diwakar, Shyam Magistretti, Jacopo Goldfarb, Mitchell Naldi, Giovanni D'Angelo, Egidio |
| description | 1 Department of Physiological and Pharmacological Sciences, University of Pavia, Pavia, Italy; 2 Consorzio Nazionale Interuniversitario per le Scienze Fisiche della Materia, Pavia Unit, Pavia, Italy; 3 Department of Mathematics, University of Milan, Milan, Italy; 4 and Department of Biological Sciences, Hunter College of City University, New York, New York
Submitted 20 March 2008;
accepted in final form 19 November 2008
In most neurons, Na + channels in the axon are complemented by others localized in the soma and dendrites to ensure spike back-propagation. However, cerebellar granule cells are neurons with simplified architecture in which the dendrites are short and unbranched and a single thin ascending axon travels toward the molecular layer before bifurcating into parallel fibers. Here we show that in cerebellar granule cells, Na + channels are enriched in the axon, especially in the hillock, but almost absent from soma and dendrites. The impact of this channel distribution on neuronal electroresponsiveness was investigated by multi-compartmental modeling. Numerical simulations indicated that granule cells have a compact electrotonic structure allowing excitatory postsynaptic potentials to diffuse with little attenuation from dendrites to axon. The spike arose almost simultaneously along the whole axonal ascending branch and invaded the hillock the activation of which promoted spike back-propagation with marginal delay ( |
| doi_str_mv | 10.1152/jn.90382.2008 |
| format | Article |
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Submitted 20 March 2008;
accepted in final form 19 November 2008
In most neurons, Na + channels in the axon are complemented by others localized in the soma and dendrites to ensure spike back-propagation. However, cerebellar granule cells are neurons with simplified architecture in which the dendrites are short and unbranched and a single thin ascending axon travels toward the molecular layer before bifurcating into parallel fibers. Here we show that in cerebellar granule cells, Na + channels are enriched in the axon, especially in the hillock, but almost absent from soma and dendrites. The impact of this channel distribution on neuronal electroresponsiveness was investigated by multi-compartmental modeling. Numerical simulations indicated that granule cells have a compact electrotonic structure allowing excitatory postsynaptic potentials to diffuse with little attenuation from dendrites to axon. The spike arose almost simultaneously along the whole axonal ascending branch and invaded the hillock the activation of which promoted spike back-propagation with marginal delay (<200 µs) and attenuation (<20 mV) into the somato-dendritic compartment. These properties allow granule cells to perform sub-millisecond coincidence detection of pre- and postsynaptic activity and to rapidly activate Purkinje cells contacted by the axonal ascending branch.
Address for reprint requests and other correspondence: E. D'Angelo, Dept. of Physiological and Pharmacological Sciences, Via Forlanini 6, University of Pavia, I-27100 Pavia, Italy (E-mail dangelo{at}unipv.it )</description><identifier>ISSN: 0022-3077</identifier><identifier>EISSN: 1522-1598</identifier><identifier>DOI: 10.1152/jn.90382.2008</identifier><identifier>PMID: 19073816</identifier><language>eng</language><publisher>United States: Am Phys Soc</publisher><subject>Action Potentials - physiology ; Animals ; Animals, Newborn ; Axons - physiology ; Biophysical Phenomena ; Cerebellum - cytology ; Electric Capacitance ; Electric Stimulation - methods ; Excitatory Amino Acid Agonists - pharmacology ; In Vitro Techniques ; Ion Channel Gating - drug effects ; Ion Channel Gating - physiology ; Membrane Potentials - physiology ; Mice ; Models, Neurological ; N-Methylaspartate - pharmacology ; Neurons - cytology ; Neurons - physiology ; Patch-Clamp Techniques ; Sodium Channels - physiology ; Synaptic Transmission - drug effects ; Synaptic Transmission - physiology</subject><ispartof>Journal of neurophysiology, 2009-02, Vol.101 (2), p.519-532</ispartof><rights>Copyright © 2009, American Physiological Society 2009</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c527t-eb7b92aecdbc9f2d3ea7c36927f95af577cc81177908cfe645cac1b4575e5d623</citedby><cites>FETCH-LOGICAL-c527t-eb7b92aecdbc9f2d3ea7c36927f95af577cc81177908cfe645cac1b4575e5d623</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,781,785,886,3040,27929,27930</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19073816$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Diwakar, Shyam</creatorcontrib><creatorcontrib>Magistretti, Jacopo</creatorcontrib><creatorcontrib>Goldfarb, Mitchell</creatorcontrib><creatorcontrib>Naldi, Giovanni</creatorcontrib><creatorcontrib>D'Angelo, Egidio</creatorcontrib><title>Axonal Na+ Channels Ensure Fast Spike Activation and Back-Propagation in Cerebellar Granule Cells</title><title>Journal of neurophysiology</title><addtitle>J Neurophysiol</addtitle><description>1 Department of Physiological and Pharmacological Sciences, University of Pavia, Pavia, Italy; 2 Consorzio Nazionale Interuniversitario per le Scienze Fisiche della Materia, Pavia Unit, Pavia, Italy; 3 Department of Mathematics, University of Milan, Milan, Italy; 4 and Department of Biological Sciences, Hunter College of City University, New York, New York
Submitted 20 March 2008;
accepted in final form 19 November 2008
In most neurons, Na + channels in the axon are complemented by others localized in the soma and dendrites to ensure spike back-propagation. However, cerebellar granule cells are neurons with simplified architecture in which the dendrites are short and unbranched and a single thin ascending axon travels toward the molecular layer before bifurcating into parallel fibers. Here we show that in cerebellar granule cells, Na + channels are enriched in the axon, especially in the hillock, but almost absent from soma and dendrites. The impact of this channel distribution on neuronal electroresponsiveness was investigated by multi-compartmental modeling. Numerical simulations indicated that granule cells have a compact electrotonic structure allowing excitatory postsynaptic potentials to diffuse with little attenuation from dendrites to axon. The spike arose almost simultaneously along the whole axonal ascending branch and invaded the hillock the activation of which promoted spike back-propagation with marginal delay (<200 µs) and attenuation (<20 mV) into the somato-dendritic compartment. These properties allow granule cells to perform sub-millisecond coincidence detection of pre- and postsynaptic activity and to rapidly activate Purkinje cells contacted by the axonal ascending branch.
Address for reprint requests and other correspondence: E. D'Angelo, Dept. of Physiological and Pharmacological Sciences, Via Forlanini 6, University of Pavia, I-27100 Pavia, Italy (E-mail dangelo{at}unipv.it )</description><subject>Action Potentials - physiology</subject><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Axons - physiology</subject><subject>Biophysical Phenomena</subject><subject>Cerebellum - cytology</subject><subject>Electric Capacitance</subject><subject>Electric Stimulation - methods</subject><subject>Excitatory Amino Acid Agonists - pharmacology</subject><subject>In Vitro Techniques</subject><subject>Ion Channel Gating - drug effects</subject><subject>Ion Channel Gating - physiology</subject><subject>Membrane Potentials - physiology</subject><subject>Mice</subject><subject>Models, Neurological</subject><subject>N-Methylaspartate - pharmacology</subject><subject>Neurons - cytology</subject><subject>Neurons - physiology</subject><subject>Patch-Clamp Techniques</subject><subject>Sodium Channels - physiology</subject><subject>Synaptic Transmission - drug effects</subject><subject>Synaptic Transmission - physiology</subject><issn>0022-3077</issn><issn>1522-1598</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kcFv0zAUxi0EYmVw5Ip8ggNKsZ06ji9IpVq3SRMgMc6W47w07lw72MlY_3tcWg04cLL1-fe-5_c-hF5TMqeUsw9bP5ekrNmcEVI_QbOssYJyWT9FM0LyvSRCnKEXKW0JIYIT9hydUUlEWdNqhvTyIXjt8Gf9Hq967T24hC98miLgtU4j_jbYO8BLM9p7PdrgsfYt_qTNXfE1hkFvjqL1eAURGnBOR3wZtZ8cZMm59BI967RL8Op0nqPv64vb1VVx8-XyerW8KQxnYiygEY1kGkzbGNmxtgQtTFlJJjrJdceFMKamVAhJatNBteBGG9osuODA24qV5-jj0XeYmh20BvwYtVNDtDsd9ypoq_598bZXm3CvWMUF4Yts8PZkEMOPCdKodjaZw0QewpRUVdV5bVRksDiCJoaUInSPTShRh1DU1qvfoahDKJl_8_fP_tCnFDLw7gj0dtP_tBHU0O-TDS5s9gcvSqhiilOZyfL_5Hpy7hYexlzyWKGGtit_AZ5sqds</recordid><startdate>20090201</startdate><enddate>20090201</enddate><creator>Diwakar, Shyam</creator><creator>Magistretti, Jacopo</creator><creator>Goldfarb, Mitchell</creator><creator>Naldi, Giovanni</creator><creator>D'Angelo, Egidio</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20090201</creationdate><title>Axonal Na+ Channels Ensure Fast Spike Activation and Back-Propagation in Cerebellar Granule Cells</title><author>Diwakar, Shyam ; Magistretti, Jacopo ; Goldfarb, Mitchell ; Naldi, Giovanni ; D'Angelo, Egidio</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c527t-eb7b92aecdbc9f2d3ea7c36927f95af577cc81177908cfe645cac1b4575e5d623</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Action Potentials - physiology</topic><topic>Animals</topic><topic>Animals, Newborn</topic><topic>Axons - physiology</topic><topic>Biophysical Phenomena</topic><topic>Cerebellum - cytology</topic><topic>Electric Capacitance</topic><topic>Electric Stimulation - methods</topic><topic>Excitatory Amino Acid Agonists - pharmacology</topic><topic>In Vitro Techniques</topic><topic>Ion Channel Gating - drug effects</topic><topic>Ion Channel Gating - physiology</topic><topic>Membrane Potentials - physiology</topic><topic>Mice</topic><topic>Models, Neurological</topic><topic>N-Methylaspartate - pharmacology</topic><topic>Neurons - cytology</topic><topic>Neurons - physiology</topic><topic>Patch-Clamp Techniques</topic><topic>Sodium Channels - physiology</topic><topic>Synaptic Transmission - drug effects</topic><topic>Synaptic Transmission - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Diwakar, Shyam</creatorcontrib><creatorcontrib>Magistretti, Jacopo</creatorcontrib><creatorcontrib>Goldfarb, Mitchell</creatorcontrib><creatorcontrib>Naldi, Giovanni</creatorcontrib><creatorcontrib>D'Angelo, Egidio</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>PubMed Central (Full Participant titles)</collection><jtitle>Journal of neurophysiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Diwakar, Shyam</au><au>Magistretti, Jacopo</au><au>Goldfarb, Mitchell</au><au>Naldi, Giovanni</au><au>D'Angelo, Egidio</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Axonal Na+ Channels Ensure Fast Spike Activation and Back-Propagation in Cerebellar Granule Cells</atitle><jtitle>Journal of neurophysiology</jtitle><addtitle>J Neurophysiol</addtitle><date>2009-02-01</date><risdate>2009</risdate><volume>101</volume><issue>2</issue><spage>519</spage><epage>532</epage><pages>519-532</pages><issn>0022-3077</issn><eissn>1522-1598</eissn><abstract>1 Department of Physiological and Pharmacological Sciences, University of Pavia, Pavia, Italy; 2 Consorzio Nazionale Interuniversitario per le Scienze Fisiche della Materia, Pavia Unit, Pavia, Italy; 3 Department of Mathematics, University of Milan, Milan, Italy; 4 and Department of Biological Sciences, Hunter College of City University, New York, New York
Submitted 20 March 2008;
accepted in final form 19 November 2008
In most neurons, Na + channels in the axon are complemented by others localized in the soma and dendrites to ensure spike back-propagation. However, cerebellar granule cells are neurons with simplified architecture in which the dendrites are short and unbranched and a single thin ascending axon travels toward the molecular layer before bifurcating into parallel fibers. Here we show that in cerebellar granule cells, Na + channels are enriched in the axon, especially in the hillock, but almost absent from soma and dendrites. The impact of this channel distribution on neuronal electroresponsiveness was investigated by multi-compartmental modeling. Numerical simulations indicated that granule cells have a compact electrotonic structure allowing excitatory postsynaptic potentials to diffuse with little attenuation from dendrites to axon. The spike arose almost simultaneously along the whole axonal ascending branch and invaded the hillock the activation of which promoted spike back-propagation with marginal delay (<200 µs) and attenuation (<20 mV) into the somato-dendritic compartment. These properties allow granule cells to perform sub-millisecond coincidence detection of pre- and postsynaptic activity and to rapidly activate Purkinje cells contacted by the axonal ascending branch.
Address for reprint requests and other correspondence: E. D'Angelo, Dept. of Physiological and Pharmacological Sciences, Via Forlanini 6, University of Pavia, I-27100 Pavia, Italy (E-mail dangelo{at}unipv.it )</abstract><cop>United States</cop><pub>Am Phys Soc</pub><pmid>19073816</pmid><doi>10.1152/jn.90382.2008</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; American Physiological Society; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection |
| subjects | Action Potentials - physiology Animals Animals, Newborn Axons - physiology Biophysical Phenomena Cerebellum - cytology Electric Capacitance Electric Stimulation - methods Excitatory Amino Acid Agonists - pharmacology In Vitro Techniques Ion Channel Gating - drug effects Ion Channel Gating - physiology Membrane Potentials - physiology Mice Models, Neurological N-Methylaspartate - pharmacology Neurons - cytology Neurons - physiology Patch-Clamp Techniques Sodium Channels - physiology Synaptic Transmission - drug effects Synaptic Transmission - physiology |
| title | Axonal Na+ Channels Ensure Fast Spike Activation and Back-Propagation in Cerebellar Granule Cells |
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