Selective reduction of AMPA currents onto hippocampal interneurons impairs network oscillatory activity
Reduction of excitatory currents onto GABAergic interneurons in the forebrain results in impaired spatial working memory and altered oscillatory network patterns in the hippocampus. Whether this phenotype is caused by an alteration in hippocampal interneurons is not known because most studies employ...
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| description | Reduction of excitatory currents onto GABAergic interneurons in the forebrain results in impaired spatial working memory and altered oscillatory network patterns in the hippocampus. Whether this phenotype is caused by an alteration in hippocampal interneurons is not known because most studies employed genetic manipulations affecting several brain regions. Here we performed viral injections in genetically modified mice to ablate the GluA4 subunit of the AMPA receptor in the hippocampus (GluA4(HC-/-) mice), thereby selectively reducing AMPA receptor-mediated currents onto a subgroup of hippocampal interneurons expressing GluA4. This regionally selective manipulation led to a strong spatial working memory deficit while leaving reference memory unaffected. Ripples (125-250 Hz) in the CA1 region of GluA4(HC-/-) mice had larger amplitude, slower frequency and reduced rate of occurrence. These changes were associated with an increased firing rate of pyramidal cells during ripples. The spatial selectivity of hippocampal pyramidal cells was comparable to that of controls in many respects when assessed during open field exploration and zigzag maze running. However, GluA4 ablation caused altered modulation of firing rate by theta oscillations in both interneurons and pyramidal cells. Moreover, the correlation between the theta firing phase of pyramidal cells and position was weaker in GluA4(HC-/-) mice. These results establish the involvement of AMPA receptor-mediated currents onto hippocampal interneurons for ripples and theta oscillations, and highlight potential cellular and network alterations that could account for the altered working memory performance. |
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Whether this phenotype is caused by an alteration in hippocampal interneurons is not known because most studies employed genetic manipulations affecting several brain regions. Here we performed viral injections in genetically modified mice to ablate the GluA4 subunit of the AMPA receptor in the hippocampus (GluA4(HC-/-) mice), thereby selectively reducing AMPA receptor-mediated currents onto a subgroup of hippocampal interneurons expressing GluA4. This regionally selective manipulation led to a strong spatial working memory deficit while leaving reference memory unaffected. Ripples (125-250 Hz) in the CA1 region of GluA4(HC-/-) mice had larger amplitude, slower frequency and reduced rate of occurrence. These changes were associated with an increased firing rate of pyramidal cells during ripples. The spatial selectivity of hippocampal pyramidal cells was comparable to that of controls in many respects when assessed during open field exploration and zigzag maze running. However, GluA4 ablation caused altered modulation of firing rate by theta oscillations in both interneurons and pyramidal cells. Moreover, the correlation between the theta firing phase of pyramidal cells and position was weaker in GluA4(HC-/-) mice. These results establish the involvement of AMPA receptor-mediated currents onto hippocampal interneurons for ripples and theta oscillations, and highlight potential cellular and network alterations that could account for the altered working memory performance.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0037318</identifier><identifier>PMID: 22675480</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Ablation ; Action Potentials - physiology ; alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid - metabolism ; Animals ; Biology ; Brain ; CA1 Region, Hippocampal - physiology ; Cancer ; Cellular communication ; Chickens ; Cognitive ability ; Exploration ; Exploratory Behavior ; Firing ; Firing rate ; Forebrain ; GABA ; Gene Deletion ; Genetic engineering ; Genetic modification ; Genetically modified organisms ; Hippocampus ; Hippocampus - physiology ; House mouse ; Interneurons ; Interneurons - physiology ; Ion Channel Gating - physiology ; Maze Learning ; Medical research ; Memory ; Memory, Short-Term - physiology ; Mice ; Nerve Net - physiology ; Neurobiology ; Neurosciences ; Oscillations ; Pyramidal cells ; Pyramidal Cells - physiology ; Receptors, AMPA - deficiency ; Receptors, AMPA - metabolism ; Recipes ; Reduction ; Ripples ; Rodents ; Selectivity ; Short term memory ; Spatial memory ; Theta rhythms ; Viruses ; α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid ; α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors ; γ-Aminobutyric acid</subject><ispartof>PloS one, 2012-06, Vol.7 (6), p.e37318</ispartof><rights>COPYRIGHT 2012 Public Library of Science</rights><rights>2012 Caputi et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Whether this phenotype is caused by an alteration in hippocampal interneurons is not known because most studies employed genetic manipulations affecting several brain regions. Here we performed viral injections in genetically modified mice to ablate the GluA4 subunit of the AMPA receptor in the hippocampus (GluA4(HC-/-) mice), thereby selectively reducing AMPA receptor-mediated currents onto a subgroup of hippocampal interneurons expressing GluA4. This regionally selective manipulation led to a strong spatial working memory deficit while leaving reference memory unaffected. Ripples (125-250 Hz) in the CA1 region of GluA4(HC-/-) mice had larger amplitude, slower frequency and reduced rate of occurrence. These changes were associated with an increased firing rate of pyramidal cells during ripples. The spatial selectivity of hippocampal pyramidal cells was comparable to that of controls in many respects when assessed during open field exploration and zigzag maze running. However, GluA4 ablation caused altered modulation of firing rate by theta oscillations in both interneurons and pyramidal cells. Moreover, the correlation between the theta firing phase of pyramidal cells and position was weaker in GluA4(HC-/-) mice. 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Whether this phenotype is caused by an alteration in hippocampal interneurons is not known because most studies employed genetic manipulations affecting several brain regions. Here we performed viral injections in genetically modified mice to ablate the GluA4 subunit of the AMPA receptor in the hippocampus (GluA4(HC-/-) mice), thereby selectively reducing AMPA receptor-mediated currents onto a subgroup of hippocampal interneurons expressing GluA4. This regionally selective manipulation led to a strong spatial working memory deficit while leaving reference memory unaffected. Ripples (125-250 Hz) in the CA1 region of GluA4(HC-/-) mice had larger amplitude, slower frequency and reduced rate of occurrence. These changes were associated with an increased firing rate of pyramidal cells during ripples. The spatial selectivity of hippocampal pyramidal cells was comparable to that of controls in many respects when assessed during open field exploration and zigzag maze running. However, GluA4 ablation caused altered modulation of firing rate by theta oscillations in both interneurons and pyramidal cells. Moreover, the correlation between the theta firing phase of pyramidal cells and position was weaker in GluA4(HC-/-) mice. These results establish the involvement of AMPA receptor-mediated currents onto hippocampal interneurons for ripples and theta oscillations, and highlight potential cellular and network alterations that could account for the altered working memory performance.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>22675480</pmid><doi>10.1371/journal.pone.0037318</doi><tpages>e37318</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Ablation Action Potentials - physiology alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid - metabolism Animals Biology Brain CA1 Region, Hippocampal - physiology Cancer Cellular communication Chickens Cognitive ability Exploration Exploratory Behavior Firing Firing rate Forebrain GABA Gene Deletion Genetic engineering Genetic modification Genetically modified organisms Hippocampus Hippocampus - physiology House mouse Interneurons Interneurons - physiology Ion Channel Gating - physiology Maze Learning Medical research Memory Memory, Short-Term - physiology Mice Nerve Net - physiology Neurobiology Neurosciences Oscillations Pyramidal cells Pyramidal Cells - physiology Receptors, AMPA - deficiency Receptors, AMPA - metabolism Recipes Reduction Ripples Rodents Selectivity Short term memory Spatial memory Theta rhythms Viruses α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors γ-Aminobutyric acid |
| title | Selective reduction of AMPA currents onto hippocampal interneurons impairs network oscillatory activity |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-31T04%3A33%3A36IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Selective%20reduction%20of%20AMPA%20currents%20onto%20hippocampal%20interneurons%20impairs%20network%20oscillatory%20activity&rft.jtitle=PloS%20one&rft.au=Caputi,%20Antonio&rft.date=2012-06-04&rft.volume=7&rft.issue=6&rft.spage=e37318&rft.pages=e37318-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0037318&rft_dat=%3Cgale_plos_%3EA477116615%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1325002830&rft_id=info:pmid/22675480&rft_galeid=A477116615&rft_doaj_id=oai_doaj_org_article_a2fa1ecb610f4b97b12869f46b842748&rfr_iscdi=true |