Slow gamma rhythms in CA3 are entrained by slow gamma activity in the dentate gyrus
In hippocampal area CA1, slow (∼25-55 Hz) and fast (∼60-100 Hz) gamma rhythms are coupled with different CA1 afferents. CA1 slow gamma is coupled to inputs from CA3, and CA1 fast gamma is coupled to inputs from the medial entorhinal cortex (Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jens...
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Veröffentlicht in: | Journal of neurophysiology 2016-12, Vol.116 (6), p.2594-2603 |
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description | In hippocampal area CA1, slow (∼25-55 Hz) and fast (∼60-100 Hz) gamma rhythms are coupled with different CA1 afferents. CA1 slow gamma is coupled to inputs from CA3, and CA1 fast gamma is coupled to inputs from the medial entorhinal cortex (Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI. Nature 462: 353-357, 2009). CA3 gives rise to highly divergent associational projections, and it is possible that reverberating activity in these connections generates slow gamma rhythms in the hippocampus. However, hippocampal gamma is maximal upstream of CA3, in the dentate gyrus (DG) region (Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G. J Neurosci 15: 47-60, 1995). Thus it is possible that slow gamma in CA3 is driven by inputs from DG, yet few studies have examined slow and fast gamma rhythms in DG recordings. Here we investigated slow and fast gamma rhythms in paired recordings from DG and CA3 in freely moving rats to determine whether slow and fast gamma rhythms in CA3 are entrained by DG. We found that slow gamma rhythms, as opposed to fast gamma rhythms, were particularly prominent in DG. We investigated directional causal influences between DG and CA3 by Granger causality analysis and found that DG slow gamma influences CA3 slow gamma. Moreover, DG place cell spikes were strongly phase-locked to CA3 slow gamma rhythms, suggesting that DG excitatory projections to CA3 may underlie this directional influence. These results indicate that slow gamma rhythms do not originate in CA3 but rather slow gamma activity upstream in DG entrains slow gamma rhythms in CA3. |
doi_str_mv | 10.1152/jn.00499.2016 |
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CA1 slow gamma is coupled to inputs from CA3, and CA1 fast gamma is coupled to inputs from the medial entorhinal cortex (Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI. Nature 462: 353-357, 2009). CA3 gives rise to highly divergent associational projections, and it is possible that reverberating activity in these connections generates slow gamma rhythms in the hippocampus. However, hippocampal gamma is maximal upstream of CA3, in the dentate gyrus (DG) region (Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G. J Neurosci 15: 47-60, 1995). Thus it is possible that slow gamma in CA3 is driven by inputs from DG, yet few studies have examined slow and fast gamma rhythms in DG recordings. Here we investigated slow and fast gamma rhythms in paired recordings from DG and CA3 in freely moving rats to determine whether slow and fast gamma rhythms in CA3 are entrained by DG. We found that slow gamma rhythms, as opposed to fast gamma rhythms, were particularly prominent in DG. We investigated directional causal influences between DG and CA3 by Granger causality analysis and found that DG slow gamma influences CA3 slow gamma. Moreover, DG place cell spikes were strongly phase-locked to CA3 slow gamma rhythms, suggesting that DG excitatory projections to CA3 may underlie this directional influence. These results indicate that slow gamma rhythms do not originate in CA3 but rather slow gamma activity upstream in DG entrains slow gamma rhythms in CA3.</description><identifier>ISSN: 0022-3077</identifier><identifier>EISSN: 1522-1598</identifier><identifier>DOI: 10.1152/jn.00499.2016</identifier><identifier>PMID: 27628206</identifier><language>eng</language><publisher>United States: American Physiological Society</publisher><subject>Action Potentials - physiology ; Analysis of Variance ; Animals ; CA3 Region, Hippocampal - cytology ; CA3 Region, Hippocampal - physiology ; Dentate Gyrus - cytology ; Dentate Gyrus - physiology ; Electric Stimulation ; Electrodes ; Exploratory Behavior - physiology ; Gamma Rhythm - physiology ; Male ; Nerve Net - physiology ; Neural Circuits ; Neural Pathways - physiology ; Neurons - physiology ; Psychomotor Performance - physiology ; Rats ; Rats, Long-Evans ; Spectrum Analysis</subject><ispartof>Journal of neurophysiology, 2016-12, Vol.116 (6), p.2594-2603</ispartof><rights>Copyright © 2016 the American Physiological Society.</rights><rights>Copyright © 2016 the American Physiological Society 2016 American Physiological Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c453t-439479131dffb17f07dac584c6e58608ed4a3e3388a59acbd7830f64474578703</citedby><cites>FETCH-LOGICAL-c453t-439479131dffb17f07dac584c6e58608ed4a3e3388a59acbd7830f64474578703</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,776,780,881,3026,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27628206$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hsiao, Yi-Tse</creatorcontrib><creatorcontrib>Zheng, Chenguang</creatorcontrib><creatorcontrib>Colgin, Laura Lee</creatorcontrib><title>Slow gamma rhythms in CA3 are entrained by slow gamma activity in the dentate gyrus</title><title>Journal of neurophysiology</title><addtitle>J Neurophysiol</addtitle><description>In hippocampal area CA1, slow (∼25-55 Hz) and fast (∼60-100 Hz) gamma rhythms are coupled with different CA1 afferents. CA1 slow gamma is coupled to inputs from CA3, and CA1 fast gamma is coupled to inputs from the medial entorhinal cortex (Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI. Nature 462: 353-357, 2009). CA3 gives rise to highly divergent associational projections, and it is possible that reverberating activity in these connections generates slow gamma rhythms in the hippocampus. However, hippocampal gamma is maximal upstream of CA3, in the dentate gyrus (DG) region (Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G. J Neurosci 15: 47-60, 1995). Thus it is possible that slow gamma in CA3 is driven by inputs from DG, yet few studies have examined slow and fast gamma rhythms in DG recordings. Here we investigated slow and fast gamma rhythms in paired recordings from DG and CA3 in freely moving rats to determine whether slow and fast gamma rhythms in CA3 are entrained by DG. We found that slow gamma rhythms, as opposed to fast gamma rhythms, were particularly prominent in DG. We investigated directional causal influences between DG and CA3 by Granger causality analysis and found that DG slow gamma influences CA3 slow gamma. Moreover, DG place cell spikes were strongly phase-locked to CA3 slow gamma rhythms, suggesting that DG excitatory projections to CA3 may underlie this directional influence. These results indicate that slow gamma rhythms do not originate in CA3 but rather slow gamma activity upstream in DG entrains slow gamma rhythms in CA3.</description><subject>Action Potentials - physiology</subject><subject>Analysis of Variance</subject><subject>Animals</subject><subject>CA3 Region, Hippocampal - cytology</subject><subject>CA3 Region, Hippocampal - physiology</subject><subject>Dentate Gyrus - cytology</subject><subject>Dentate Gyrus - physiology</subject><subject>Electric Stimulation</subject><subject>Electrodes</subject><subject>Exploratory Behavior - physiology</subject><subject>Gamma Rhythm - physiology</subject><subject>Male</subject><subject>Nerve Net - physiology</subject><subject>Neural Circuits</subject><subject>Neural Pathways - physiology</subject><subject>Neurons - physiology</subject><subject>Psychomotor Performance - physiology</subject><subject>Rats</subject><subject>Rats, Long-Evans</subject><subject>Spectrum Analysis</subject><issn>0022-3077</issn><issn>1522-1598</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkUlPwzAQhS0EoqVw5Ip85JIy3mLnglRVbFIlDoWz5SROkypLsRNQ_j3pQoHTjGY-vXmah9A1gSkhgt6t6ykAj6IpBRKeoPEwowERkTpFY4ChZyDlCF14vwYAKYCeoxGVIVUUwjFaLsvmC69MVRns8r7NK4-LGs9nDBtnsa1bZ4rapjjusf9FTdIWn0Xbb9k2tzgdQNNavOpd5y_RWWZKb68OdYLeHx_e5s_B4vXpZT5bBAkXrA04i7iMCCNplsVEZiBTkwjFk9AKFYKyKTfMMqaUEZFJ4lQqBlnIueRCKglsgu73upsurmya7MyWeuOKyrheN6bQ_zd1ketV86kFYYxG4SBwexBwzUdnfaurwie2LE1tm85rorhQhAzfGtBgjyau8d7Z7HiGgN4Gode13gWht0EM_M1fb0f65_PsG-zqg7Y</recordid><startdate>20161201</startdate><enddate>20161201</enddate><creator>Hsiao, Yi-Tse</creator><creator>Zheng, Chenguang</creator><creator>Colgin, Laura Lee</creator><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>20161201</creationdate><title>Slow gamma rhythms in CA3 are entrained by slow gamma activity in the dentate gyrus</title><author>Hsiao, Yi-Tse ; Zheng, Chenguang ; Colgin, Laura Lee</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c453t-439479131dffb17f07dac584c6e58608ed4a3e3388a59acbd7830f64474578703</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Action Potentials - physiology</topic><topic>Analysis of Variance</topic><topic>Animals</topic><topic>CA3 Region, Hippocampal - cytology</topic><topic>CA3 Region, Hippocampal - physiology</topic><topic>Dentate Gyrus - cytology</topic><topic>Dentate Gyrus - physiology</topic><topic>Electric Stimulation</topic><topic>Electrodes</topic><topic>Exploratory Behavior - physiology</topic><topic>Gamma Rhythm - physiology</topic><topic>Male</topic><topic>Nerve Net - physiology</topic><topic>Neural Circuits</topic><topic>Neural Pathways - physiology</topic><topic>Neurons - physiology</topic><topic>Psychomotor Performance - physiology</topic><topic>Rats</topic><topic>Rats, Long-Evans</topic><topic>Spectrum Analysis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hsiao, Yi-Tse</creatorcontrib><creatorcontrib>Zheng, Chenguang</creatorcontrib><creatorcontrib>Colgin, Laura Lee</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>Hsiao, Yi-Tse</au><au>Zheng, Chenguang</au><au>Colgin, Laura Lee</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Slow gamma rhythms in CA3 are entrained by slow gamma activity in the dentate gyrus</atitle><jtitle>Journal of neurophysiology</jtitle><addtitle>J Neurophysiol</addtitle><date>2016-12-01</date><risdate>2016</risdate><volume>116</volume><issue>6</issue><spage>2594</spage><epage>2603</epage><pages>2594-2603</pages><issn>0022-3077</issn><eissn>1522-1598</eissn><abstract>In hippocampal area CA1, slow (∼25-55 Hz) and fast (∼60-100 Hz) gamma rhythms are coupled with different CA1 afferents. CA1 slow gamma is coupled to inputs from CA3, and CA1 fast gamma is coupled to inputs from the medial entorhinal cortex (Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI. Nature 462: 353-357, 2009). CA3 gives rise to highly divergent associational projections, and it is possible that reverberating activity in these connections generates slow gamma rhythms in the hippocampus. However, hippocampal gamma is maximal upstream of CA3, in the dentate gyrus (DG) region (Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G. J Neurosci 15: 47-60, 1995). Thus it is possible that slow gamma in CA3 is driven by inputs from DG, yet few studies have examined slow and fast gamma rhythms in DG recordings. Here we investigated slow and fast gamma rhythms in paired recordings from DG and CA3 in freely moving rats to determine whether slow and fast gamma rhythms in CA3 are entrained by DG. We found that slow gamma rhythms, as opposed to fast gamma rhythms, were particularly prominent in DG. We investigated directional causal influences between DG and CA3 by Granger causality analysis and found that DG slow gamma influences CA3 slow gamma. Moreover, DG place cell spikes were strongly phase-locked to CA3 slow gamma rhythms, suggesting that DG excitatory projections to CA3 may underlie this directional influence. These results indicate that slow gamma rhythms do not originate in CA3 but rather slow gamma activity upstream in DG entrains slow gamma rhythms in CA3.</abstract><cop>United States</cop><pub>American Physiological Society</pub><pmid>27628206</pmid><doi>10.1152/jn.00499.2016</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Action Potentials - physiology Analysis of Variance Animals CA3 Region, Hippocampal - cytology CA3 Region, Hippocampal - physiology Dentate Gyrus - cytology Dentate Gyrus - physiology Electric Stimulation Electrodes Exploratory Behavior - physiology Gamma Rhythm - physiology Male Nerve Net - physiology Neural Circuits Neural Pathways - physiology Neurons - physiology Psychomotor Performance - physiology Rats Rats, Long-Evans Spectrum Analysis |
title | Slow gamma rhythms in CA3 are entrained by slow gamma activity in the dentate gyrus |
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