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Stimulus-dependent state transition between synchronized oscillation and randomly repetitive burst in a model cerebellar granular layer
Information processing of the cerebellar granular layer composed of granule and Golgi cells is regarded as an important first step toward the cerebellar computation. Our previous theoretical studies have shown that granule cells can exhibit random alternation between burst and silent modes, which pr...
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Published in: | PLoS computational biology 2011-07, Vol.7 (7), p.e1002087-e1002087 |
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description | Information processing of the cerebellar granular layer composed of granule and Golgi cells is regarded as an important first step toward the cerebellar computation. Our previous theoretical studies have shown that granule cells can exhibit random alternation between burst and silent modes, which provides a basis of population representation of the passage-of-time (POT) from the onset of external input stimuli. On the other hand, another computational study has reported that granule cells can exhibit synchronized oscillation of activity, as consistent with observed oscillation in local field potential recorded from the granular layer while animals keep still. Here we have a question of whether an identical network model can explain these distinct dynamics. In the present study, we carried out computer simulations based on a spiking network model of the granular layer varying two parameters: the strength of a current injected to granule cells and the concentration of Mg²⁺ which controls the conductance of NMDA channels assumed on the Golgi cell dendrites. The simulations showed that cells in the granular layer can switch activity states between synchronized oscillation and random burst-silent alternation depending on the two parameters. For higher Mg²⁺ concentration and a weaker injected current, granule and Golgi cells elicited spikes synchronously (synchronized oscillation state). In contrast, for lower Mg²⁺ concentration and a stronger injected current, those cells showed the random burst-silent alternation (POT-representing state). It is suggested that NMDA channels on the Golgi cell dendrites play an important role for determining how the granular layer works in response to external input. |
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Our previous theoretical studies have shown that granule cells can exhibit random alternation between burst and silent modes, which provides a basis of population representation of the passage-of-time (POT) from the onset of external input stimuli. On the other hand, another computational study has reported that granule cells can exhibit synchronized oscillation of activity, as consistent with observed oscillation in local field potential recorded from the granular layer while animals keep still. Here we have a question of whether an identical network model can explain these distinct dynamics. In the present study, we carried out computer simulations based on a spiking network model of the granular layer varying two parameters: the strength of a current injected to granule cells and the concentration of Mg²⁺ which controls the conductance of NMDA channels assumed on the Golgi cell dendrites. The simulations showed that cells in the granular layer can switch activity states between synchronized oscillation and random burst-silent alternation depending on the two parameters. For higher Mg²⁺ concentration and a weaker injected current, granule and Golgi cells elicited spikes synchronously (synchronized oscillation state). In contrast, for lower Mg²⁺ concentration and a stronger injected current, those cells showed the random burst-silent alternation (POT-representing state). It is suggested that NMDA channels on the Golgi cell dendrites play an important role for determining how the granular layer works in response to external input.</description><identifier>ISSN: 1553-7358</identifier><identifier>ISSN: 1553-734X</identifier><identifier>EISSN: 1553-7358</identifier><identifier>DOI: 10.1371/journal.pcbi.1002087</identifier><identifier>PMID: 21779155</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Action Potentials - physiology ; alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid - metabolism ; Animals ; Biology ; Cerebellar Cortex - cytology ; Cerebellar Cortex - metabolism ; Cerebellar Cortex - physiology ; Computer Simulation ; Dendrites - physiology ; gamma-Aminobutyric Acid - metabolism ; Interneurons ; Magnesium - metabolism ; Models, Neurological ; N-Methylaspartate - metabolism ; Neurons - metabolism ; Neurons - physiology ; Rats ; Rest - physiology ; Studies</subject><ispartof>PLoS computational biology, 2011-07, Vol.7 (7), p.e1002087-e1002087</ispartof><rights>Honda et al. 2011</rights><rights>2011 Honda et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Honda T, Yamazaki T, Tanaka S, Nagao S, Nishino T (2011) Stimulus-Dependent State Transition between Synchronized Oscillation and Randomly Repetitive Burst in a Model Cerebellar Granular Layer. PLoS Comput Biol 7(7): e1002087. doi:10.1371/journal.pcbi.1002087</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c563t-8187bd23fa5fbf950bf4c0e3396dd33a097d5e1547bc14824d0718a04cc2949c3</citedby><cites>FETCH-LOGICAL-c563t-8187bd23fa5fbf950bf4c0e3396dd33a097d5e1547bc14824d0718a04cc2949c3</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/PMC3136428/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3136428/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,36990,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21779155$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Honda, Takeru</creatorcontrib><creatorcontrib>Yamazaki, Tadashi</creatorcontrib><creatorcontrib>Tanaka, Shigeru</creatorcontrib><creatorcontrib>Nagao, Soichi</creatorcontrib><creatorcontrib>Nishino, Tetsuro</creatorcontrib><title>Stimulus-dependent state transition between synchronized oscillation and randomly repetitive burst in a model cerebellar granular layer</title><title>PLoS computational biology</title><addtitle>PLoS Comput Biol</addtitle><description>Information processing of the cerebellar granular layer composed of granule and Golgi cells is regarded as an important first step toward the cerebellar computation. Our previous theoretical studies have shown that granule cells can exhibit random alternation between burst and silent modes, which provides a basis of population representation of the passage-of-time (POT) from the onset of external input stimuli. On the other hand, another computational study has reported that granule cells can exhibit synchronized oscillation of activity, as consistent with observed oscillation in local field potential recorded from the granular layer while animals keep still. Here we have a question of whether an identical network model can explain these distinct dynamics. In the present study, we carried out computer simulations based on a spiking network model of the granular layer varying two parameters: the strength of a current injected to granule cells and the concentration of Mg²⁺ which controls the conductance of NMDA channels assumed on the Golgi cell dendrites. The simulations showed that cells in the granular layer can switch activity states between synchronized oscillation and random burst-silent alternation depending on the two parameters. For higher Mg²⁺ concentration and a weaker injected current, granule and Golgi cells elicited spikes synchronously (synchronized oscillation state). In contrast, for lower Mg²⁺ concentration and a stronger injected current, those cells showed the random burst-silent alternation (POT-representing state). It is suggested that NMDA channels on the Golgi cell dendrites play an important role for determining how the granular layer works in response to external input.</description><subject>Action Potentials - physiology</subject><subject>alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid - metabolism</subject><subject>Animals</subject><subject>Biology</subject><subject>Cerebellar Cortex - cytology</subject><subject>Cerebellar Cortex - metabolism</subject><subject>Cerebellar Cortex - physiology</subject><subject>Computer Simulation</subject><subject>Dendrites - physiology</subject><subject>gamma-Aminobutyric Acid - metabolism</subject><subject>Interneurons</subject><subject>Magnesium - metabolism</subject><subject>Models, Neurological</subject><subject>N-Methylaspartate - metabolism</subject><subject>Neurons - metabolism</subject><subject>Neurons - physiology</subject><subject>Rats</subject><subject>Rest - physiology</subject><subject>Studies</subject><issn>1553-7358</issn><issn>1553-734X</issn><issn>1553-7358</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNpVUl1vFCEUnRiNrav_wChvPs0KAwzMi4lp_GjSxAf1mTBwZ8uGgRWYNusf8G_LdrdNG0i44Z5z7uVymuYtwWtCBfm4jUsK2q93ZnRrgnGHpXjWnBPOaSsol88fxWfNq5y3GNdw6F82Zx0RYqjZ8-bfz-LmxS-5tbCDYCEUlIsugErSIbviYkAjlFuAgPI-mOsUg_sLFsVsnPf6DqCDRRVu4-z3KFWhUok3gMYl5YJcBaA5WvDIQIIRKi2hTSUsh8DrPaTXzYtJ-wxvTueq-f31y6-L7-3Vj2-XF5-vWsN7WlpJpBhtRyfNp3EaOB4nZjBQOvTWUqrxICwHwpkYDWGyYxYLIjVmxnQDGwxdNe-PujsfszrNMCtC65KE1r1qLo8IG_VW7ZKbddqrqJ26u4hpo3QqznhQRAKnmFgA0jNm-4EPfKRD12sJVhJRtT6dqi3jDNbU6Sbtn4g-zQR3rTbxRtV2etbJKvDhJJDinwVyUbPL5jDAAHHJSgopu65-akWyI9KkmHOC6aEKwepgmPvHqoNh1MkwlfbucYcPpHuH0P88lsMd</recordid><startdate>20110701</startdate><enddate>20110701</enddate><creator>Honda, Takeru</creator><creator>Yamazaki, Tadashi</creator><creator>Tanaka, Shigeru</creator><creator>Nagao, Soichi</creator><creator>Nishino, Tetsuro</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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><scope>DOA</scope></search><sort><creationdate>20110701</creationdate><title>Stimulus-dependent state transition between synchronized oscillation and randomly repetitive burst in a model cerebellar granular layer</title><author>Honda, Takeru ; Yamazaki, Tadashi ; Tanaka, Shigeru ; Nagao, Soichi ; Nishino, Tetsuro</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c563t-8187bd23fa5fbf950bf4c0e3396dd33a097d5e1547bc14824d0718a04cc2949c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Action Potentials - physiology</topic><topic>alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid - metabolism</topic><topic>Animals</topic><topic>Biology</topic><topic>Cerebellar Cortex - cytology</topic><topic>Cerebellar Cortex - metabolism</topic><topic>Cerebellar Cortex - physiology</topic><topic>Computer Simulation</topic><topic>Dendrites - physiology</topic><topic>gamma-Aminobutyric Acid - metabolism</topic><topic>Interneurons</topic><topic>Magnesium - metabolism</topic><topic>Models, Neurological</topic><topic>N-Methylaspartate - metabolism</topic><topic>Neurons - metabolism</topic><topic>Neurons - physiology</topic><topic>Rats</topic><topic>Rest - physiology</topic><topic>Studies</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Honda, Takeru</creatorcontrib><creatorcontrib>Yamazaki, Tadashi</creatorcontrib><creatorcontrib>Tanaka, Shigeru</creatorcontrib><creatorcontrib>Nagao, Soichi</creatorcontrib><creatorcontrib>Nishino, Tetsuro</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><collection>Directory of Open Access Journals</collection><jtitle>PLoS computational biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Honda, Takeru</au><au>Yamazaki, Tadashi</au><au>Tanaka, Shigeru</au><au>Nagao, Soichi</au><au>Nishino, Tetsuro</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Stimulus-dependent state transition between synchronized oscillation and randomly repetitive burst in a model cerebellar granular layer</atitle><jtitle>PLoS computational biology</jtitle><addtitle>PLoS Comput Biol</addtitle><date>2011-07-01</date><risdate>2011</risdate><volume>7</volume><issue>7</issue><spage>e1002087</spage><epage>e1002087</epage><pages>e1002087-e1002087</pages><issn>1553-7358</issn><issn>1553-734X</issn><eissn>1553-7358</eissn><abstract>Information processing of the cerebellar granular layer composed of granule and Golgi cells is regarded as an important first step toward the cerebellar computation. Our previous theoretical studies have shown that granule cells can exhibit random alternation between burst and silent modes, which provides a basis of population representation of the passage-of-time (POT) from the onset of external input stimuli. On the other hand, another computational study has reported that granule cells can exhibit synchronized oscillation of activity, as consistent with observed oscillation in local field potential recorded from the granular layer while animals keep still. Here we have a question of whether an identical network model can explain these distinct dynamics. In the present study, we carried out computer simulations based on a spiking network model of the granular layer varying two parameters: the strength of a current injected to granule cells and the concentration of Mg²⁺ which controls the conductance of NMDA channels assumed on the Golgi cell dendrites. The simulations showed that cells in the granular layer can switch activity states between synchronized oscillation and random burst-silent alternation depending on the two parameters. For higher Mg²⁺ concentration and a weaker injected current, granule and Golgi cells elicited spikes synchronously (synchronized oscillation state). In contrast, for lower Mg²⁺ concentration and a stronger injected current, those cells showed the random burst-silent alternation (POT-representing state). It is suggested that NMDA channels on the Golgi cell dendrites play an important role for determining how the granular layer works in response to external input.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>21779155</pmid><doi>10.1371/journal.pcbi.1002087</doi><oa>free_for_read</oa></addata></record> |
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subjects | Action Potentials - physiology alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid - metabolism Animals Biology Cerebellar Cortex - cytology Cerebellar Cortex - metabolism Cerebellar Cortex - physiology Computer Simulation Dendrites - physiology gamma-Aminobutyric Acid - metabolism Interneurons Magnesium - metabolism Models, Neurological N-Methylaspartate - metabolism Neurons - metabolism Neurons - physiology Rats Rest - physiology Studies |
title | Stimulus-dependent state transition between synchronized oscillation and randomly repetitive burst in a model cerebellar granular layer |
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