The endocannabinoid 2-arachidonoylglycerol negatively regulates habituation by suppressing excitatory recurrent network activity and reducing long-term potentiation in the dentate gyrus
Endocannabinoids are known to mediate retrograde suppression of synaptic transmission, modulate synaptic plasticity, and influence learning and memory. The 2-arachidonoylglycerol (2-AG) produced by diacylglycerol lipase α (DGLα) is regarded as the major endocannabinoid that causes retrograde synapti...
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Veröffentlicht in: | The Journal of neuroscience 2013-02, Vol.33 (8), p.3588-3601 |
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description | Endocannabinoids are known to mediate retrograde suppression of synaptic transmission, modulate synaptic plasticity, and influence learning and memory. The 2-arachidonoylglycerol (2-AG) produced by diacylglycerol lipase α (DGLα) is regarded as the major endocannabinoid that causes retrograde synaptic suppression. To determine how 2-AG signaling influences learning and memory, we subjected DGLα knock-out mice to two learning tasks. We tested the mice using habituation and odor-guided transverse patterning tasks that are known to involve the dentate gyrus and the CA1, respectively, of the hippocampus. We found that DGLα knock-out mice showed significantly faster habituation to an odor and a new environment than wild-type littermates with normal performance in the transverse patterning task. In freely moving animals, long-term potentiation (LTP) induced by theta burst stimulation was significantly larger at perforant path-granule cell synapses in the dentate gyrus of DGLα knock-out mice. Importantly, prior induction of synaptic potentiation at this synapse caused a significant retardation of habituation in DGLα knock-out but not in wild-type littermates. The excitability of granule cells became higher in DGLα knock-out mice after they generated action potentials. Since no differences were found in intrinsic membrane properties and responses to odor stimuli in granule cells, the elevated excitability is considered to result from enhanced activity of an excitatory recurrent network composed of granule cells and mossy cells. These results suggest that retrograde 2-AG signaling negatively regulates habituation by suppressing excitatory recurrent network activity and reducing LTP in the dentate gyrus. |
doi_str_mv | 10.1523/JNEUROSCI.3141-12.2013 |
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The 2-arachidonoylglycerol (2-AG) produced by diacylglycerol lipase α (DGLα) is regarded as the major endocannabinoid that causes retrograde synaptic suppression. To determine how 2-AG signaling influences learning and memory, we subjected DGLα knock-out mice to two learning tasks. We tested the mice using habituation and odor-guided transverse patterning tasks that are known to involve the dentate gyrus and the CA1, respectively, of the hippocampus. We found that DGLα knock-out mice showed significantly faster habituation to an odor and a new environment than wild-type littermates with normal performance in the transverse patterning task. In freely moving animals, long-term potentiation (LTP) induced by theta burst stimulation was significantly larger at perforant path-granule cell synapses in the dentate gyrus of DGLα knock-out mice. Importantly, prior induction of synaptic potentiation at this synapse caused a significant retardation of habituation in DGLα knock-out but not in wild-type littermates. The excitability of granule cells became higher in DGLα knock-out mice after they generated action potentials. Since no differences were found in intrinsic membrane properties and responses to odor stimuli in granule cells, the elevated excitability is considered to result from enhanced activity of an excitatory recurrent network composed of granule cells and mossy cells. These results suggest that retrograde 2-AG signaling negatively regulates habituation by suppressing excitatory recurrent network activity and reducing LTP in the dentate gyrus.</description><identifier>ISSN: 0270-6474</identifier><identifier>ISSN: 1529-2401</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.3141-12.2013</identifier><identifier>PMID: 23426686</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Animals ; Arachidonic Acids - physiology ; Association Learning - physiology ; Dentate Gyrus - physiology ; Endocannabinoids - physiology ; Excitatory Postsynaptic Potentials - physiology ; Female ; Glycerides - physiology ; Habituation, Psychophysiologic - physiology ; Long-Term Potentiation - physiology ; Male ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Nerve Net - physiology ; Neural Inhibition - physiology ; Reaction Time - physiology ; Secondary Prevention</subject><ispartof>The Journal of neuroscience, 2013-02, Vol.33 (8), p.3588-3601</ispartof><rights>Copyright © 2013 the authors 0270-6474/13/333588-14$15.00/0 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c513t-724551520e55aeebea1e8d69426929ae1624a499ab31f798c173ebe5cfeb82383</citedby><cites>FETCH-LOGICAL-c513t-724551520e55aeebea1e8d69426929ae1624a499ab31f798c173ebe5cfeb82383</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/PMC6619537/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6619537/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,725,778,782,883,27911,27912,53778,53780</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23426686$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sugaya, Yuki</creatorcontrib><creatorcontrib>Cagniard, Barbara</creatorcontrib><creatorcontrib>Yamazaki, Maya</creatorcontrib><creatorcontrib>Sakimura, Kenji</creatorcontrib><creatorcontrib>Kano, Masanobu</creatorcontrib><title>The endocannabinoid 2-arachidonoylglycerol negatively regulates habituation by suppressing excitatory recurrent network activity and reducing long-term potentiation in the dentate gyrus</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>Endocannabinoids are known to mediate retrograde suppression of synaptic transmission, modulate synaptic plasticity, and influence learning and memory. The 2-arachidonoylglycerol (2-AG) produced by diacylglycerol lipase α (DGLα) is regarded as the major endocannabinoid that causes retrograde synaptic suppression. To determine how 2-AG signaling influences learning and memory, we subjected DGLα knock-out mice to two learning tasks. We tested the mice using habituation and odor-guided transverse patterning tasks that are known to involve the dentate gyrus and the CA1, respectively, of the hippocampus. We found that DGLα knock-out mice showed significantly faster habituation to an odor and a new environment than wild-type littermates with normal performance in the transverse patterning task. In freely moving animals, long-term potentiation (LTP) induced by theta burst stimulation was significantly larger at perforant path-granule cell synapses in the dentate gyrus of DGLα knock-out mice. Importantly, prior induction of synaptic potentiation at this synapse caused a significant retardation of habituation in DGLα knock-out but not in wild-type littermates. The excitability of granule cells became higher in DGLα knock-out mice after they generated action potentials. Since no differences were found in intrinsic membrane properties and responses to odor stimuli in granule cells, the elevated excitability is considered to result from enhanced activity of an excitatory recurrent network composed of granule cells and mossy cells. These results suggest that retrograde 2-AG signaling negatively regulates habituation by suppressing excitatory recurrent network activity and reducing LTP in the dentate gyrus.</description><subject>Animals</subject><subject>Arachidonic Acids - physiology</subject><subject>Association Learning - physiology</subject><subject>Dentate Gyrus - physiology</subject><subject>Endocannabinoids - physiology</subject><subject>Excitatory Postsynaptic Potentials - physiology</subject><subject>Female</subject><subject>Glycerides - physiology</subject><subject>Habituation, Psychophysiologic - physiology</subject><subject>Long-Term Potentiation - physiology</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Nerve Net - physiology</subject><subject>Neural Inhibition - physiology</subject><subject>Reaction Time - physiology</subject><subject>Secondary Prevention</subject><issn>0270-6474</issn><issn>1529-2401</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFks1u1DAUhSMEokPhFSov2WTwX-zJBgmNWiiqqATt2nKcOxmDxw62U8ij8XY4mjKCFStL957z-dg6VXVB8Jo0lL35-Ony_vPtl-31mhFOakLXFBP2pFqVbVtTjsnTaoWpxLXgkp9VL1L6ijGWmMjn1RllnAqxEavq190eEPg-GO297qwPtke01lGbve2DD7Mb3GwgBoc8DDrbB3AzijBMTmdIaF9MeSrz4FE3ozSNY4SUrB8Q_DQ26xziojdTjOBzgeQfIX5D2hSUzTPSvi_rfjKLxQU_1BniAY0hF7k9gq1HueTsy6RcioY5Tull9WynXYJXj-d5dX91ebf9UN_cvr_evrupTUNYriXlTVM-BUPTaIAONIFNL9ryAS1tNRBBueZtqztGdrLdGCJZUTVmB92Gsg07r94euePUHaA3JUPUTo3RHnScVdBW_bvxdq-G8KCEIG3DZAG8fgTE8H2ClNXBJgPOaQ9hSoqUfII2suX_lzJCiSQcL1RxlJoYUoqwOyUiWC0VUaeKqKUiilC1VKQYL_5-z8n2pxPsN1qYwFg</recordid><startdate>20130220</startdate><enddate>20130220</enddate><creator>Sugaya, Yuki</creator><creator>Cagniard, Barbara</creator><creator>Yamazaki, Maya</creator><creator>Sakimura, Kenji</creator><creator>Kano, Masanobu</creator><general>Society for Neuroscience</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>7TK</scope><scope>5PM</scope></search><sort><creationdate>20130220</creationdate><title>The endocannabinoid 2-arachidonoylglycerol negatively regulates habituation by suppressing excitatory recurrent network activity and reducing long-term potentiation in the dentate gyrus</title><author>Sugaya, Yuki ; Cagniard, Barbara ; Yamazaki, Maya ; Sakimura, Kenji ; Kano, Masanobu</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c513t-724551520e55aeebea1e8d69426929ae1624a499ab31f798c173ebe5cfeb82383</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Arachidonic Acids - physiology</topic><topic>Association Learning - physiology</topic><topic>Dentate Gyrus - physiology</topic><topic>Endocannabinoids - physiology</topic><topic>Excitatory Postsynaptic Potentials - physiology</topic><topic>Female</topic><topic>Glycerides - physiology</topic><topic>Habituation, Psychophysiologic - physiology</topic><topic>Long-Term Potentiation - physiology</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Nerve Net - physiology</topic><topic>Neural Inhibition - physiology</topic><topic>Reaction Time - physiology</topic><topic>Secondary Prevention</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sugaya, Yuki</creatorcontrib><creatorcontrib>Cagniard, Barbara</creatorcontrib><creatorcontrib>Yamazaki, Maya</creatorcontrib><creatorcontrib>Sakimura, Kenji</creatorcontrib><creatorcontrib>Kano, Masanobu</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>Neurosciences Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sugaya, Yuki</au><au>Cagniard, Barbara</au><au>Yamazaki, Maya</au><au>Sakimura, Kenji</au><au>Kano, Masanobu</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The endocannabinoid 2-arachidonoylglycerol negatively regulates habituation by suppressing excitatory recurrent network activity and reducing long-term potentiation in the dentate gyrus</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2013-02-20</date><risdate>2013</risdate><volume>33</volume><issue>8</issue><spage>3588</spage><epage>3601</epage><pages>3588-3601</pages><issn>0270-6474</issn><issn>1529-2401</issn><eissn>1529-2401</eissn><abstract>Endocannabinoids are known to mediate retrograde suppression of synaptic transmission, modulate synaptic plasticity, and influence learning and memory. The 2-arachidonoylglycerol (2-AG) produced by diacylglycerol lipase α (DGLα) is regarded as the major endocannabinoid that causes retrograde synaptic suppression. To determine how 2-AG signaling influences learning and memory, we subjected DGLα knock-out mice to two learning tasks. We tested the mice using habituation and odor-guided transverse patterning tasks that are known to involve the dentate gyrus and the CA1, respectively, of the hippocampus. We found that DGLα knock-out mice showed significantly faster habituation to an odor and a new environment than wild-type littermates with normal performance in the transverse patterning task. In freely moving animals, long-term potentiation (LTP) induced by theta burst stimulation was significantly larger at perforant path-granule cell synapses in the dentate gyrus of DGLα knock-out mice. Importantly, prior induction of synaptic potentiation at this synapse caused a significant retardation of habituation in DGLα knock-out but not in wild-type littermates. The excitability of granule cells became higher in DGLα knock-out mice after they generated action potentials. Since no differences were found in intrinsic membrane properties and responses to odor stimuli in granule cells, the elevated excitability is considered to result from enhanced activity of an excitatory recurrent network composed of granule cells and mossy cells. These results suggest that retrograde 2-AG signaling negatively regulates habituation by suppressing excitatory recurrent network activity and reducing LTP in the dentate gyrus.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>23426686</pmid><doi>10.1523/JNEUROSCI.3141-12.2013</doi><tpages>14</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Arachidonic Acids - physiology Association Learning - physiology Dentate Gyrus - physiology Endocannabinoids - physiology Excitatory Postsynaptic Potentials - physiology Female Glycerides - physiology Habituation, Psychophysiologic - physiology Long-Term Potentiation - physiology Male Mice Mice, Inbred C57BL Mice, Knockout Nerve Net - physiology Neural Inhibition - physiology Reaction Time - physiology Secondary Prevention |
title | The endocannabinoid 2-arachidonoylglycerol negatively regulates habituation by suppressing excitatory recurrent network activity and reducing long-term potentiation in the dentate gyrus |
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