Different input and output properties characterize parvalbumin-positive basket and Axo-axonic cells in the hippocampal CA3 subfield
ABSTRACT In the hippocampus, parvalbumin‐expressing basket (BC) and axo‐axonic cells (AAC) show different discharge patterns during distinct network states, but the cellular mechanisms underlying these differences are not well understood. Using whole‐cell patch‐clamp techniques, we investigated the...
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Veröffentlicht in: | Hippocampus 2013-10, Vol.23 (10), p.903-918 |
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description | ABSTRACT
In the hippocampus, parvalbumin‐expressing basket (BC) and axo‐axonic cells (AAC) show different discharge patterns during distinct network states, but the cellular mechanisms underlying these differences are not well understood. Using whole‐cell patch‐clamp techniques, we investigated the single‐cell properties and excitatory synaptic features of anatomically identified BCs and AACs in the CA3 region of mouse hippocampal slices. The results showed that BCs had lower threshold for action potential (AP) generation and lower input resistance, narrower AP and afterhyperpolarization than AACs. In addition, BCs fired with higher frequencies and with more modest accommodation compared with AACs. The kinetic properties of excitatory postsynaptic currents (EPSC), the rectification of AMPA receptor‐mediated currents, the fraction of the NMDA receptor‐mediated component in EPSCs, and the EPSC magnitude necessary to evoke an AP were similar in both cell types. However, smaller excitatory postsynaptic potential and lower intensity fiber stimulation in stratum oriens was necessary to drive firing in BCs. Moreover, the rate of spontaneous EPSCs in BCs was higher than in AACs. Neurolucida analysis revealed that the dendrites of BCs in strata radiatum and oriens were longer and more extensively ramified. Since the density of the excitatory synapses was estimated to be comparable in both cell types, we conclude that the more elaborated dendritic arbor of BCs ensures that they receive a larger number of proximal excitatory inputs. Thus, CA3 pyramidal cells more profoundly innervate BCs than AACs, which could explain, at least in part, their distinct spiking behavior under different hippocampal network activities. © 2013 Wiley Periodicals, Inc. |
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In the hippocampus, parvalbumin‐expressing basket (BC) and axo‐axonic cells (AAC) show different discharge patterns during distinct network states, but the cellular mechanisms underlying these differences are not well understood. Using whole‐cell patch‐clamp techniques, we investigated the single‐cell properties and excitatory synaptic features of anatomically identified BCs and AACs in the CA3 region of mouse hippocampal slices. The results showed that BCs had lower threshold for action potential (AP) generation and lower input resistance, narrower AP and afterhyperpolarization than AACs. In addition, BCs fired with higher frequencies and with more modest accommodation compared with AACs. The kinetic properties of excitatory postsynaptic currents (EPSC), the rectification of AMPA receptor‐mediated currents, the fraction of the NMDA receptor‐mediated component in EPSCs, and the EPSC magnitude necessary to evoke an AP were similar in both cell types. However, smaller excitatory postsynaptic potential and lower intensity fiber stimulation in stratum oriens was necessary to drive firing in BCs. Moreover, the rate of spontaneous EPSCs in BCs was higher than in AACs. Neurolucida analysis revealed that the dendrites of BCs in strata radiatum and oriens were longer and more extensively ramified. Since the density of the excitatory synapses was estimated to be comparable in both cell types, we conclude that the more elaborated dendritic arbor of BCs ensures that they receive a larger number of proximal excitatory inputs. Thus, CA3 pyramidal cells more profoundly innervate BCs than AACs, which could explain, at least in part, their distinct spiking behavior under different hippocampal network activities. © 2013 Wiley Periodicals, Inc.</description><identifier>ISSN: 1050-9631</identifier><identifier>EISSN: 1098-1063</identifier><identifier>DOI: 10.1002/hipo.22147</identifier><identifier>PMID: 23733415</identifier><identifier>CODEN: HIPPEL</identifier><language>eng</language><publisher>United States: Blackwell Publishing Ltd</publisher><subject>Animals ; Axons - physiology ; CA3 Region, Hippocampal - cytology ; Dendrites - physiology ; dendritic arbor ; EPSC ; EPSP ; Excitatory Postsynaptic Potentials - physiology ; GABAergic Neurons - physiology ; in vitro ; interneuron ; Interneurons - physiology ; Mice ; Mice, Transgenic ; Neurons - physiology ; Parvalbumins ; Patch-Clamp Techniques - instrumentation ; Patch-Clamp Techniques - methods ; Synapses - physiology</subject><ispartof>Hippocampus, 2013-10, Vol.23 (10), p.903-918</ispartof><rights>Copyright © 2013 Wiley Periodicals, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4317-a003bb0c35661966f7e03c47999ae9c48b9cf800a64b9c6d88de94d971cfa7203</citedby><cites>FETCH-LOGICAL-c4317-a003bb0c35661966f7e03c47999ae9c48b9cf800a64b9c6d88de94d971cfa7203</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fhipo.22147$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fhipo.22147$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>315,781,785,1418,27928,27929,45578,45579</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23733415$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Papp, Orsolya I.</creatorcontrib><creatorcontrib>Karlócai, Mária R.</creatorcontrib><creatorcontrib>Tóth, Irén E.</creatorcontrib><creatorcontrib>Freund, Tamás F.</creatorcontrib><creatorcontrib>Hájos, Norbert</creatorcontrib><title>Different input and output properties characterize parvalbumin-positive basket and Axo-axonic cells in the hippocampal CA3 subfield</title><title>Hippocampus</title><addtitle>Hippocampus</addtitle><description>ABSTRACT
In the hippocampus, parvalbumin‐expressing basket (BC) and axo‐axonic cells (AAC) show different discharge patterns during distinct network states, but the cellular mechanisms underlying these differences are not well understood. Using whole‐cell patch‐clamp techniques, we investigated the single‐cell properties and excitatory synaptic features of anatomically identified BCs and AACs in the CA3 region of mouse hippocampal slices. The results showed that BCs had lower threshold for action potential (AP) generation and lower input resistance, narrower AP and afterhyperpolarization than AACs. In addition, BCs fired with higher frequencies and with more modest accommodation compared with AACs. The kinetic properties of excitatory postsynaptic currents (EPSC), the rectification of AMPA receptor‐mediated currents, the fraction of the NMDA receptor‐mediated component in EPSCs, and the EPSC magnitude necessary to evoke an AP were similar in both cell types. However, smaller excitatory postsynaptic potential and lower intensity fiber stimulation in stratum oriens was necessary to drive firing in BCs. Moreover, the rate of spontaneous EPSCs in BCs was higher than in AACs. Neurolucida analysis revealed that the dendrites of BCs in strata radiatum and oriens were longer and more extensively ramified. Since the density of the excitatory synapses was estimated to be comparable in both cell types, we conclude that the more elaborated dendritic arbor of BCs ensures that they receive a larger number of proximal excitatory inputs. Thus, CA3 pyramidal cells more profoundly innervate BCs than AACs, which could explain, at least in part, their distinct spiking behavior under different hippocampal network activities. © 2013 Wiley Periodicals, Inc.</description><subject>Animals</subject><subject>Axons - physiology</subject><subject>CA3 Region, Hippocampal - cytology</subject><subject>Dendrites - physiology</subject><subject>dendritic arbor</subject><subject>EPSC</subject><subject>EPSP</subject><subject>Excitatory Postsynaptic Potentials - physiology</subject><subject>GABAergic Neurons - physiology</subject><subject>in vitro</subject><subject>interneuron</subject><subject>Interneurons - physiology</subject><subject>Mice</subject><subject>Mice, Transgenic</subject><subject>Neurons - physiology</subject><subject>Parvalbumins</subject><subject>Patch-Clamp Techniques - instrumentation</subject><subject>Patch-Clamp Techniques - methods</subject><subject>Synapses - physiology</subject><issn>1050-9631</issn><issn>1098-1063</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kU1v1DAYhCMEoh9w4QcgS1yqSmn9xokdH1dL2VaqaBFfR8tx3mjdJnGwk7Llyh_HIW0PHDh5Ds-Mx54keQP0BCjNTrd2cCdZBrl4luwDlWUKlLPnsy5oKjmDveQghBtKAQpKXyZ7GROM5VDsJ7_f26ZBj_1IbD9MI9F9Tdw0znLwbkA_WgzEbLXXZkRvfyEZtL_TbTV1tk8HF-xo75BUOtziYl_tXKp3rreGGGzbEJPJuEUSew7O6G7QLVmvGAlT1Vhs61fJi0a3AV8_nIfJ1w9nX9bn6eXV5mK9ukxNzkCkmlJWVdSwgnOQnDcCKTO5kFJqlCYvK2maklLN86h4XZY1yryWAkyjRUbZYXK05MaH_ZgwjKqzYW6oe3RTUFBAHm8qMhbRd_-gN27yfWynIGciAxH_O1LHC2W8C8FjowZvO-3vFVA1T6PmadTfaSL89iFyqjqsn9DHLSIAC_DTtnj_nyh1fnF99RiaLh4bRtw9ebS_VVwwUajvHzdqIwuAzbfP6hP7A9PnqVk</recordid><startdate>201310</startdate><enddate>201310</enddate><creator>Papp, Orsolya I.</creator><creator>Karlócai, Mária R.</creator><creator>Tóth, Irén E.</creator><creator>Freund, Tamás F.</creator><creator>Hájos, Norbert</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</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>7QG</scope><scope>7TK</scope><scope>K9.</scope><scope>7X8</scope></search><sort><creationdate>201310</creationdate><title>Different input and output properties characterize parvalbumin-positive basket and Axo-axonic cells in the hippocampal CA3 subfield</title><author>Papp, Orsolya I. ; Karlócai, Mária R. ; Tóth, Irén E. ; Freund, Tamás F. ; Hájos, Norbert</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4317-a003bb0c35661966f7e03c47999ae9c48b9cf800a64b9c6d88de94d971cfa7203</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Axons - physiology</topic><topic>CA3 Region, Hippocampal - cytology</topic><topic>Dendrites - physiology</topic><topic>dendritic arbor</topic><topic>EPSC</topic><topic>EPSP</topic><topic>Excitatory Postsynaptic Potentials - physiology</topic><topic>GABAergic Neurons - physiology</topic><topic>in vitro</topic><topic>interneuron</topic><topic>Interneurons - physiology</topic><topic>Mice</topic><topic>Mice, Transgenic</topic><topic>Neurons - physiology</topic><topic>Parvalbumins</topic><topic>Patch-Clamp Techniques - instrumentation</topic><topic>Patch-Clamp Techniques - methods</topic><topic>Synapses - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Papp, Orsolya I.</creatorcontrib><creatorcontrib>Karlócai, Mária R.</creatorcontrib><creatorcontrib>Tóth, Irén E.</creatorcontrib><creatorcontrib>Freund, Tamás F.</creatorcontrib><creatorcontrib>Hájos, Norbert</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Hippocampus</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Papp, Orsolya I.</au><au>Karlócai, Mária R.</au><au>Tóth, Irén E.</au><au>Freund, Tamás F.</au><au>Hájos, Norbert</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Different input and output properties characterize parvalbumin-positive basket and Axo-axonic cells in the hippocampal CA3 subfield</atitle><jtitle>Hippocampus</jtitle><addtitle>Hippocampus</addtitle><date>2013-10</date><risdate>2013</risdate><volume>23</volume><issue>10</issue><spage>903</spage><epage>918</epage><pages>903-918</pages><issn>1050-9631</issn><eissn>1098-1063</eissn><coden>HIPPEL</coden><abstract>ABSTRACT
In the hippocampus, parvalbumin‐expressing basket (BC) and axo‐axonic cells (AAC) show different discharge patterns during distinct network states, but the cellular mechanisms underlying these differences are not well understood. Using whole‐cell patch‐clamp techniques, we investigated the single‐cell properties and excitatory synaptic features of anatomically identified BCs and AACs in the CA3 region of mouse hippocampal slices. The results showed that BCs had lower threshold for action potential (AP) generation and lower input resistance, narrower AP and afterhyperpolarization than AACs. In addition, BCs fired with higher frequencies and with more modest accommodation compared with AACs. The kinetic properties of excitatory postsynaptic currents (EPSC), the rectification of AMPA receptor‐mediated currents, the fraction of the NMDA receptor‐mediated component in EPSCs, and the EPSC magnitude necessary to evoke an AP were similar in both cell types. However, smaller excitatory postsynaptic potential and lower intensity fiber stimulation in stratum oriens was necessary to drive firing in BCs. Moreover, the rate of spontaneous EPSCs in BCs was higher than in AACs. Neurolucida analysis revealed that the dendrites of BCs in strata radiatum and oriens were longer and more extensively ramified. Since the density of the excitatory synapses was estimated to be comparable in both cell types, we conclude that the more elaborated dendritic arbor of BCs ensures that they receive a larger number of proximal excitatory inputs. Thus, CA3 pyramidal cells more profoundly innervate BCs than AACs, which could explain, at least in part, their distinct spiking behavior under different hippocampal network activities. © 2013 Wiley Periodicals, Inc.</abstract><cop>United States</cop><pub>Blackwell Publishing Ltd</pub><pmid>23733415</pmid><doi>10.1002/hipo.22147</doi><tpages>16</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Axons - physiology CA3 Region, Hippocampal - cytology Dendrites - physiology dendritic arbor EPSC EPSP Excitatory Postsynaptic Potentials - physiology GABAergic Neurons - physiology in vitro interneuron Interneurons - physiology Mice Mice, Transgenic Neurons - physiology Parvalbumins Patch-Clamp Techniques - instrumentation Patch-Clamp Techniques - methods Synapses - physiology |
title | Different input and output properties characterize parvalbumin-positive basket and Axo-axonic cells in the hippocampal CA3 subfield |
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