Compensatory network changes in the dentate gyrus restore long-term potentiation following ablation of neurogenesis in young-adult mice
It is now well established that neurogenesis in the rodent subgranular zone of the hippocampal dentate gyrus continues throughout adulthood. Neuroblasts born in the dentate subgranular zone migrate into the granule cell layer, where they differentiate into neurons known as dentate granule cells. Sup...
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| creator | Singer, Benjamin H Gamelli, Amy E Fuller, Cynthia L Temme, Stephanie J Parent, Jack M Murphy, Geoffrey G |
| description | It is now well established that neurogenesis in the rodent subgranular zone of the hippocampal dentate gyrus continues throughout adulthood. Neuroblasts born in the dentate subgranular zone migrate into the granule cell layer, where they differentiate into neurons known as dentate granule cells. Suppression of neurogenesis by irradiation or genetic ablation has been shown to disrupt synaptic plasticity in the dentate gyrus and impair some forms of hippocampus-dependent learning and memory. Using a recently developed transgenic mouse model for suppressing neurogenesis, we sought to determine the long-term impact of ablating neurogenesis on synaptic plasticity in young-adult mice. Consistent with previous reports, we found that ablation of neurogenesis resulted in significant deficits in dentate gyrus long-term potentiation (LTP) when examined at a time proximal to the ablation. However, the observed deficits in LTP were not permanent. LTP in the dentate gyrus was restored within 6 wk and this recovery occurred in the complete absence of neurogenesis. The recovery in LTP was accompanied by prominent changes within the dentate gyrus, including an increase in the survival rate of newborn cells that were proliferating just before the ablation and a reduction in inhibitory input to the granule cells of the dentate gyrus. These findings suggest that prolonged suppression of neurogenesis in young-adult mice results in wide-ranging compensatory changes in the structure and dynamics of the dentate gyrus that function to restore plasticity. |
| doi_str_mv | 10.1073/pnas.1015425108 |
| format | Article |
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Neuroblasts born in the dentate subgranular zone migrate into the granule cell layer, where they differentiate into neurons known as dentate granule cells. Suppression of neurogenesis by irradiation or genetic ablation has been shown to disrupt synaptic plasticity in the dentate gyrus and impair some forms of hippocampus-dependent learning and memory. Using a recently developed transgenic mouse model for suppressing neurogenesis, we sought to determine the long-term impact of ablating neurogenesis on synaptic plasticity in young-adult mice. Consistent with previous reports, we found that ablation of neurogenesis resulted in significant deficits in dentate gyrus long-term potentiation (LTP) when examined at a time proximal to the ablation. However, the observed deficits in LTP were not permanent. LTP in the dentate gyrus was restored within 6 wk and this recovery occurred in the complete absence of neurogenesis. The recovery in LTP was accompanied by prominent changes within the dentate gyrus, including an increase in the survival rate of newborn cells that were proliferating just before the ablation and a reduction in inhibitory input to the granule cells of the dentate gyrus. These findings suggest that prolonged suppression of neurogenesis in young-adult mice results in wide-ranging compensatory changes in the structure and dynamics of the dentate gyrus that function to restore plasticity.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1015425108</identifier><identifier>PMID: 21402918</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>adulthood ; Animal cognition ; Animal memory ; Animal models ; Animals ; Antiviral Agents - pharmacology ; Behavioral neuroscience ; Biological Sciences ; Brain ; Cell Differentiation - physiology ; Cell migration ; Cell survival ; Cells ; Dentate gyrus ; Dentate Gyrus - cytology ; Dentate Gyrus - drug effects ; Dentate Gyrus - physiology ; Ganciclovir - pharmacology ; Granule cells ; Hippocampus ; Intermediate Filament Proteins - genetics ; Intermediate Filament Proteins - metabolism ; irradiation ; Kinases ; Learning ; long term effects ; Long term potentiation ; Long-Term Potentiation - physiology ; Memory ; Mice ; Mice, Transgenic ; Neonates ; Nerve Net - physiology ; Nerve Tissue Proteins - genetics ; Nerve Tissue Proteins - metabolism ; Nestin ; Neuroblasts ; Neurogenesis ; Neurogenesis - physiology ; Neurons ; Optical density ; Patch-Clamp Techniques ; Plasticity (synaptic) ; Radiation ; Recovery of function ; Rodents ; survival rate ; Tetanus ; Thymidine Kinase - genetics ; Thymidine Kinase - metabolism ; transgenic animals ; Transgenic mice ; Vesicular Inhibitory Amino Acid Transport Proteins - metabolism</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2011-03, Vol.108 (13), p.5437-5442</ispartof><rights>Copyright © 1993-2008 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Mar 29, 2011</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c588t-44f39f27ccd6b163eb5b8e542dd250385f333df6b6f1651cb2f4cd1c8d9480673</citedby><cites>FETCH-LOGICAL-c588t-44f39f27ccd6b163eb5b8e542dd250385f333df6b6f1651cb2f4cd1c8d9480673</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/108/13.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/41125717$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/41125717$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27903,27904,53769,53771,57995,58228</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21402918$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Singer, Benjamin H</creatorcontrib><creatorcontrib>Gamelli, Amy E</creatorcontrib><creatorcontrib>Fuller, Cynthia L</creatorcontrib><creatorcontrib>Temme, Stephanie J</creatorcontrib><creatorcontrib>Parent, Jack M</creatorcontrib><creatorcontrib>Murphy, Geoffrey G</creatorcontrib><title>Compensatory network changes in the dentate gyrus restore long-term potentiation following ablation of neurogenesis in young-adult mice</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>It is now well established that neurogenesis in the rodent subgranular zone of the hippocampal dentate gyrus continues throughout adulthood. Neuroblasts born in the dentate subgranular zone migrate into the granule cell layer, where they differentiate into neurons known as dentate granule cells. Suppression of neurogenesis by irradiation or genetic ablation has been shown to disrupt synaptic plasticity in the dentate gyrus and impair some forms of hippocampus-dependent learning and memory. Using a recently developed transgenic mouse model for suppressing neurogenesis, we sought to determine the long-term impact of ablating neurogenesis on synaptic plasticity in young-adult mice. Consistent with previous reports, we found that ablation of neurogenesis resulted in significant deficits in dentate gyrus long-term potentiation (LTP) when examined at a time proximal to the ablation. However, the observed deficits in LTP were not permanent. LTP in the dentate gyrus was restored within 6 wk and this recovery occurred in the complete absence of neurogenesis. The recovery in LTP was accompanied by prominent changes within the dentate gyrus, including an increase in the survival rate of newborn cells that were proliferating just before the ablation and a reduction in inhibitory input to the granule cells of the dentate gyrus. These findings suggest that prolonged suppression of neurogenesis in young-adult mice results in wide-ranging compensatory changes in the structure and dynamics of the dentate gyrus that function to restore plasticity.</description><subject>adulthood</subject><subject>Animal cognition</subject><subject>Animal memory</subject><subject>Animal models</subject><subject>Animals</subject><subject>Antiviral Agents - pharmacology</subject><subject>Behavioral neuroscience</subject><subject>Biological Sciences</subject><subject>Brain</subject><subject>Cell Differentiation - physiology</subject><subject>Cell migration</subject><subject>Cell survival</subject><subject>Cells</subject><subject>Dentate gyrus</subject><subject>Dentate Gyrus - cytology</subject><subject>Dentate Gyrus - drug effects</subject><subject>Dentate Gyrus - physiology</subject><subject>Ganciclovir - pharmacology</subject><subject>Granule cells</subject><subject>Hippocampus</subject><subject>Intermediate Filament Proteins - genetics</subject><subject>Intermediate Filament Proteins - metabolism</subject><subject>irradiation</subject><subject>Kinases</subject><subject>Learning</subject><subject>long term effects</subject><subject>Long term potentiation</subject><subject>Long-Term Potentiation - physiology</subject><subject>Memory</subject><subject>Mice</subject><subject>Mice, Transgenic</subject><subject>Neonates</subject><subject>Nerve Net - physiology</subject><subject>Nerve Tissue Proteins - genetics</subject><subject>Nerve Tissue Proteins - metabolism</subject><subject>Nestin</subject><subject>Neuroblasts</subject><subject>Neurogenesis</subject><subject>Neurogenesis - physiology</subject><subject>Neurons</subject><subject>Optical density</subject><subject>Patch-Clamp Techniques</subject><subject>Plasticity (synaptic)</subject><subject>Radiation</subject><subject>Recovery of function</subject><subject>Rodents</subject><subject>survival rate</subject><subject>Tetanus</subject><subject>Thymidine Kinase - genetics</subject><subject>Thymidine Kinase - metabolism</subject><subject>transgenic animals</subject><subject>Transgenic mice</subject><subject>Vesicular Inhibitory Amino Acid Transport Proteins - metabolism</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9ksuO0zAUQCMEYsrAmhVgsYFNGN_4EXuDhCpe0kgsYNaW49hpSmIXO2HUL-C3cWhpgQUrW_a5R_dVFI8BvwJck6ud1ynfgNGKARZ3ihVgCSWnEt8tVhhXdSloRS-KByltMcaSCXy_uKiA4kqCWBU_1mHcWZ_0FOIeeTvdhvgVmY32nU2o92jaWNRaP-nJom4f54SiTRm2aAi-KycbR7QLUyZ6PfXBIxeGIdz2vkO6GQ5PwWXzHENnvU39L-0-zDlat_MwobE39mFxz-kh2UfH87K4eff2y_pDef3p_cf1m-vSMCGmklJHpKtqY1reACe2YY2wufq2rRgmgjlCSOt4wx1wBqapHDUtGNFKKjCvyWXx-uDdzc1oW5PzjnpQu9iPOu5V0L36-8f3G9WF74pgLoFDFrw4CmL4NudWqLFPxg6D9jbMSQkmqeScLuTL_5J5bLXMNLCMPv8H3YY5-twIJTjGAmqMM3R1gEwMKUXrTlkDVss2qGUb1HkbcsTTP4s98b_Hn4FnR2CJPOuEAqIYJUu_nhyI7TL0E0IBKlZDfTY4HZTuYp_UzecKQ84aZCUpIz8B3OfROg</recordid><startdate>20110329</startdate><enddate>20110329</enddate><creator>Singer, Benjamin H</creator><creator>Gamelli, Amy E</creator><creator>Fuller, Cynthia L</creator><creator>Temme, Stephanie J</creator><creator>Parent, Jack M</creator><creator>Murphy, Geoffrey G</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20110329</creationdate><title>Compensatory network changes in the dentate gyrus restore long-term potentiation following ablation of neurogenesis in young-adult mice</title><author>Singer, Benjamin H ; 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Neuroblasts born in the dentate subgranular zone migrate into the granule cell layer, where they differentiate into neurons known as dentate granule cells. Suppression of neurogenesis by irradiation or genetic ablation has been shown to disrupt synaptic plasticity in the dentate gyrus and impair some forms of hippocampus-dependent learning and memory. Using a recently developed transgenic mouse model for suppressing neurogenesis, we sought to determine the long-term impact of ablating neurogenesis on synaptic plasticity in young-adult mice. Consistent with previous reports, we found that ablation of neurogenesis resulted in significant deficits in dentate gyrus long-term potentiation (LTP) when examined at a time proximal to the ablation. However, the observed deficits in LTP were not permanent. LTP in the dentate gyrus was restored within 6 wk and this recovery occurred in the complete absence of neurogenesis. The recovery in LTP was accompanied by prominent changes within the dentate gyrus, including an increase in the survival rate of newborn cells that were proliferating just before the ablation and a reduction in inhibitory input to the granule cells of the dentate gyrus. These findings suggest that prolonged suppression of neurogenesis in young-adult mice results in wide-ranging compensatory changes in the structure and dynamics of the dentate gyrus that function to restore plasticity.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>21402918</pmid><doi>10.1073/pnas.1015425108</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | adulthood Animal cognition Animal memory Animal models Animals Antiviral Agents - pharmacology Behavioral neuroscience Biological Sciences Brain Cell Differentiation - physiology Cell migration Cell survival Cells Dentate gyrus Dentate Gyrus - cytology Dentate Gyrus - drug effects Dentate Gyrus - physiology Ganciclovir - pharmacology Granule cells Hippocampus Intermediate Filament Proteins - genetics Intermediate Filament Proteins - metabolism irradiation Kinases Learning long term effects Long term potentiation Long-Term Potentiation - physiology Memory Mice Mice, Transgenic Neonates Nerve Net - physiology Nerve Tissue Proteins - genetics Nerve Tissue Proteins - metabolism Nestin Neuroblasts Neurogenesis Neurogenesis - physiology Neurons Optical density Patch-Clamp Techniques Plasticity (synaptic) Radiation Recovery of function Rodents survival rate Tetanus Thymidine Kinase - genetics Thymidine Kinase - metabolism transgenic animals Transgenic mice Vesicular Inhibitory Amino Acid Transport Proteins - metabolism |
| title | Compensatory network changes in the dentate gyrus restore long-term potentiation following ablation of neurogenesis in young-adult mice |
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