Pharmacological Mechanisms of Cortical Enhancement Induced by the Repetitive Pairing of Visual/Cholinergic Stimulation
Repetitive visual training paired with electrical activation of cholinergic projections to the primary visual cortex (V1) induces long-term enhancement of cortical processing in response to the visual training stimulus. To better determine the receptor subtypes mediating this effect the selective ph...
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description | Repetitive visual training paired with electrical activation of cholinergic projections to the primary visual cortex (V1) induces long-term enhancement of cortical processing in response to the visual training stimulus. To better determine the receptor subtypes mediating this effect the selective pharmacological blockade of V1 nicotinic (nAChR), M1 and M2 muscarinic (mAChR) or GABAergic A (GABAAR) receptors was performed during the training session and visual evoked potentials (VEPs) were recorded before and after training. The training session consisted of the exposure of awake, adult rats to an orientation-specific 0.12 CPD grating paired with an electrical stimulation of the basal forebrain for a duration of 1 week for 10 minutes per day. Pharmacological agents were infused intracortically during this period. The post-training VEP amplitude was significantly increased compared to the pre-training values for the trained spatial frequency and to adjacent spatial frequencies up to 0.3 CPD, suggesting a long-term increase of V1 sensitivity. This increase was totally blocked by the nAChR antagonist as well as by an M2 mAChR subtype and GABAAR antagonist. Moreover, administration of the M2 mAChR antagonist also significantly decreased the amplitude of the control VEPs, suggesting a suppressive effect on cortical responsiveness. However, the M1 mAChR antagonist blocked the increase of the VEP amplitude only for the high spatial frequency (0.3 CPD), suggesting that M1 role was limited to the spread of the enhancement effect to a higher spatial frequency. More generally, all the drugs used did block the VEP increase at 0.3 CPD. Further, use of each of the aforementioned receptor antagonists blocked training-induced changes in gamma and beta band oscillations. These findings demonstrate that visual training coupled with cholinergic stimulation improved perceptual sensitivity by enhancing cortical responsiveness in V1. This enhancement is mainly mediated by nAChRs, M2 mAChRs and GABAARs. The M1 mAChR subtype appears to be involved in spreading the enhancement of V1 cortical responsiveness to adjacent neurons. |
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To better determine the receptor subtypes mediating this effect the selective pharmacological blockade of V1 nicotinic (nAChR), M1 and M2 muscarinic (mAChR) or GABAergic A (GABAAR) receptors was performed during the training session and visual evoked potentials (VEPs) were recorded before and after training. The training session consisted of the exposure of awake, adult rats to an orientation-specific 0.12 CPD grating paired with an electrical stimulation of the basal forebrain for a duration of 1 week for 10 minutes per day. Pharmacological agents were infused intracortically during this period. The post-training VEP amplitude was significantly increased compared to the pre-training values for the trained spatial frequency and to adjacent spatial frequencies up to 0.3 CPD, suggesting a long-term increase of V1 sensitivity. This increase was totally blocked by the nAChR antagonist as well as by an M2 mAChR subtype and GABAAR antagonist. Moreover, administration of the M2 mAChR antagonist also significantly decreased the amplitude of the control VEPs, suggesting a suppressive effect on cortical responsiveness. However, the M1 mAChR antagonist blocked the increase of the VEP amplitude only for the high spatial frequency (0.3 CPD), suggesting that M1 role was limited to the spread of the enhancement effect to a higher spatial frequency. More generally, all the drugs used did block the VEP increase at 0.3 CPD. Further, use of each of the aforementioned receptor antagonists blocked training-induced changes in gamma and beta band oscillations. These findings demonstrate that visual training coupled with cholinergic stimulation improved perceptual sensitivity by enhancing cortical responsiveness in V1. This enhancement is mainly mediated by nAChRs, M2 mAChRs and GABAARs. The M1 mAChR subtype appears to be involved in spreading the enhancement of V1 cortical responsiveness to adjacent neurons.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0141663</identifier><identifier>PMID: 26513575</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acetylcholine receptors (muscarinic) ; Acetylcholine receptors (nicotinic) ; Animals ; Basal forebrain ; Beta Rhythm - drug effects ; Cholinergic Agents - pharmacology ; Compounds ; Deep Brain Stimulation ; Electrical stimuli ; Electrodes ; Evoked Potentials, Visual ; Experiments ; Forebrain ; Frequency dependence ; GABA Agonists - pharmacology ; GABA Antagonists - pharmacology ; Gamma Rhythm - drug effects ; Male ; Neurons ; Neurosciences ; Orientation ; Orientation behavior ; Oscillations ; Pharmacology ; Photic Stimulation ; Rats ; Receptors ; Receptors, Nicotinic - metabolism ; Rodents ; Sensitivity ; Sensitivity enhancement ; Stimulation ; Training ; Visual cortex ; Visual Cortex - drug effects ; Visual Cortex - physiology ; Visual evoked potentials ; Visual pathways ; Visual stimuli ; γ-Aminobutyric acid A receptors</subject><ispartof>PloS one, 2015-10, Vol.10 (10), p.e0141663-e0141663</ispartof><rights>2015 Kang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://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 Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2015 Kang et al 2015 Kang et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c526t-3e59d8cd4465b8acd18d1e28cb43b059ce3e3bc338f6d202aa6e3b58092b91943</citedby><cites>FETCH-LOGICAL-c526t-3e59d8cd4465b8acd18d1e28cb43b059ce3e3bc338f6d202aa6e3b58092b91943</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/PMC4626033/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4626033/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2100,2926,23865,27923,27924,53790,53792,79371,79372</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26513575$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Dickson, Clayton T</contributor><creatorcontrib>Kang, Jun-Il</creatorcontrib><creatorcontrib>Huppé-Gourgues, Frédéric</creatorcontrib><creatorcontrib>Vaucher, Elvire</creatorcontrib><title>Pharmacological Mechanisms of Cortical Enhancement Induced by the Repetitive Pairing of Visual/Cholinergic Stimulation</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Repetitive visual training paired with electrical activation of cholinergic projections to the primary visual cortex (V1) induces long-term enhancement of cortical processing in response to the visual training stimulus. To better determine the receptor subtypes mediating this effect the selective pharmacological blockade of V1 nicotinic (nAChR), M1 and M2 muscarinic (mAChR) or GABAergic A (GABAAR) receptors was performed during the training session and visual evoked potentials (VEPs) were recorded before and after training. The training session consisted of the exposure of awake, adult rats to an orientation-specific 0.12 CPD grating paired with an electrical stimulation of the basal forebrain for a duration of 1 week for 10 minutes per day. Pharmacological agents were infused intracortically during this period. The post-training VEP amplitude was significantly increased compared to the pre-training values for the trained spatial frequency and to adjacent spatial frequencies up to 0.3 CPD, suggesting a long-term increase of V1 sensitivity. This increase was totally blocked by the nAChR antagonist as well as by an M2 mAChR subtype and GABAAR antagonist. Moreover, administration of the M2 mAChR antagonist also significantly decreased the amplitude of the control VEPs, suggesting a suppressive effect on cortical responsiveness. However, the M1 mAChR antagonist blocked the increase of the VEP amplitude only for the high spatial frequency (0.3 CPD), suggesting that M1 role was limited to the spread of the enhancement effect to a higher spatial frequency. More generally, all the drugs used did block the VEP increase at 0.3 CPD. Further, use of each of the aforementioned receptor antagonists blocked training-induced changes in gamma and beta band oscillations. These findings demonstrate that visual training coupled with cholinergic stimulation improved perceptual sensitivity by enhancing cortical responsiveness in V1. This enhancement is mainly mediated by nAChRs, M2 mAChRs and GABAARs. The M1 mAChR subtype appears to be involved in spreading the enhancement of V1 cortical responsiveness to adjacent neurons.</description><subject>Acetylcholine receptors (muscarinic)</subject><subject>Acetylcholine receptors (nicotinic)</subject><subject>Animals</subject><subject>Basal forebrain</subject><subject>Beta Rhythm - drug effects</subject><subject>Cholinergic Agents - pharmacology</subject><subject>Compounds</subject><subject>Deep Brain Stimulation</subject><subject>Electrical stimuli</subject><subject>Electrodes</subject><subject>Evoked Potentials, Visual</subject><subject>Experiments</subject><subject>Forebrain</subject><subject>Frequency dependence</subject><subject>GABA Agonists - pharmacology</subject><subject>GABA Antagonists - pharmacology</subject><subject>Gamma Rhythm - drug effects</subject><subject>Male</subject><subject>Neurons</subject><subject>Neurosciences</subject><subject>Orientation</subject><subject>Orientation behavior</subject><subject>Oscillations</subject><subject>Pharmacology</subject><subject>Photic Stimulation</subject><subject>Rats</subject><subject>Receptors</subject><subject>Receptors, Nicotinic - metabolism</subject><subject>Rodents</subject><subject>Sensitivity</subject><subject>Sensitivity enhancement</subject><subject>Stimulation</subject><subject>Training</subject><subject>Visual cortex</subject><subject>Visual Cortex - drug effects</subject><subject>Visual Cortex - physiology</subject><subject>Visual evoked potentials</subject><subject>Visual pathways</subject><subject>Visual stimuli</subject><subject>γ-Aminobutyric acid A receptors</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNptUktv1DAYjBCIPuAfIIjEhctu_U5yQUKrUlYqouJ1tRz7y65Xjr3YyUr99zjdtGoRJ9vjmfkemqJ4g9ES0wpf7MIYvXLLffCwRJhhIeiz4hQ3lCwEQfT5o_tJcZbSDiFOayFeFidEcEx5xU-Lw81WxV7p4MLGauXKr6C3ytvUpzJ05SrE4Q6-9BnV0IMfyrU3owZTtrflsIXyO-xhsIM9QHmjbLR-Myl_2zQqd7HaBmc9xGxe_hhsPzo12OBfFS865RK8ns_z4tfny5-rL4vrb1fr1afrheZEDAsKvDG1NowJ3tZKG1wbDKTWLaMt4o0GCrTVlNadMAQRpUR-8xo1pG1ww-h58e7ou3chyXllSeKK1ISjBk2M9ZFhgtrJfbS9ircyKCvvgBA3Uk07cCBRlpDcDquYYV2N2o43XYU45oRUtFPZ6-NcbWx7MDovKyr3xPTpj7dbuQkHyQQRiNJs8GE2iOHPCGmQvU0anFMewnjsW1RIUJGp7_-h_n86dmTpGFKK0D00g5GcYnSvklOM5ByjLHv7eJAH0X1u6F9dPcdW</recordid><startdate>20151029</startdate><enddate>20151029</enddate><creator>Kang, Jun-Il</creator><creator>Huppé-Gourgues, Frédéric</creator><creator>Vaucher, Elvire</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>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20151029</creationdate><title>Pharmacological Mechanisms of Cortical Enhancement Induced by the Repetitive Pairing of Visual/Cholinergic Stimulation</title><author>Kang, Jun-Il ; Huppé-Gourgues, Frédéric ; Vaucher, Elvire</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c526t-3e59d8cd4465b8acd18d1e28cb43b059ce3e3bc338f6d202aa6e3b58092b91943</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Acetylcholine receptors (muscarinic)</topic><topic>Acetylcholine receptors (nicotinic)</topic><topic>Animals</topic><topic>Basal forebrain</topic><topic>Beta Rhythm - drug effects</topic><topic>Cholinergic Agents - pharmacology</topic><topic>Compounds</topic><topic>Deep Brain Stimulation</topic><topic>Electrical stimuli</topic><topic>Electrodes</topic><topic>Evoked Potentials, Visual</topic><topic>Experiments</topic><topic>Forebrain</topic><topic>Frequency dependence</topic><topic>GABA Agonists - pharmacology</topic><topic>GABA Antagonists - pharmacology</topic><topic>Gamma Rhythm - drug effects</topic><topic>Male</topic><topic>Neurons</topic><topic>Neurosciences</topic><topic>Orientation</topic><topic>Orientation behavior</topic><topic>Oscillations</topic><topic>Pharmacology</topic><topic>Photic Stimulation</topic><topic>Rats</topic><topic>Receptors</topic><topic>Receptors, Nicotinic - metabolism</topic><topic>Rodents</topic><topic>Sensitivity</topic><topic>Sensitivity enhancement</topic><topic>Stimulation</topic><topic>Training</topic><topic>Visual cortex</topic><topic>Visual Cortex - drug effects</topic><topic>Visual Cortex - physiology</topic><topic>Visual evoked potentials</topic><topic>Visual pathways</topic><topic>Visual stimuli</topic><topic>γ-Aminobutyric acid A receptors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kang, Jun-Il</creatorcontrib><creatorcontrib>Huppé-Gourgues, Frédéric</creatorcontrib><creatorcontrib>Vaucher, Elvire</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kang, Jun-Il</au><au>Huppé-Gourgues, Frédéric</au><au>Vaucher, Elvire</au><au>Dickson, Clayton T</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pharmacological Mechanisms of Cortical Enhancement Induced by the Repetitive Pairing of Visual/Cholinergic Stimulation</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-10-29</date><risdate>2015</risdate><volume>10</volume><issue>10</issue><spage>e0141663</spage><epage>e0141663</epage><pages>e0141663-e0141663</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Repetitive visual training paired with electrical activation of cholinergic projections to the primary visual cortex (V1) induces long-term enhancement of cortical processing in response to the visual training stimulus. To better determine the receptor subtypes mediating this effect the selective pharmacological blockade of V1 nicotinic (nAChR), M1 and M2 muscarinic (mAChR) or GABAergic A (GABAAR) receptors was performed during the training session and visual evoked potentials (VEPs) were recorded before and after training. The training session consisted of the exposure of awake, adult rats to an orientation-specific 0.12 CPD grating paired with an electrical stimulation of the basal forebrain for a duration of 1 week for 10 minutes per day. Pharmacological agents were infused intracortically during this period. The post-training VEP amplitude was significantly increased compared to the pre-training values for the trained spatial frequency and to adjacent spatial frequencies up to 0.3 CPD, suggesting a long-term increase of V1 sensitivity. This increase was totally blocked by the nAChR antagonist as well as by an M2 mAChR subtype and GABAAR antagonist. Moreover, administration of the M2 mAChR antagonist also significantly decreased the amplitude of the control VEPs, suggesting a suppressive effect on cortical responsiveness. However, the M1 mAChR antagonist blocked the increase of the VEP amplitude only for the high spatial frequency (0.3 CPD), suggesting that M1 role was limited to the spread of the enhancement effect to a higher spatial frequency. More generally, all the drugs used did block the VEP increase at 0.3 CPD. Further, use of each of the aforementioned receptor antagonists blocked training-induced changes in gamma and beta band oscillations. These findings demonstrate that visual training coupled with cholinergic stimulation improved perceptual sensitivity by enhancing cortical responsiveness in V1. This enhancement is mainly mediated by nAChRs, M2 mAChRs and GABAARs. The M1 mAChR subtype appears to be involved in spreading the enhancement of V1 cortical responsiveness to adjacent neurons.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>26513575</pmid><doi>10.1371/journal.pone.0141663</doi><oa>free_for_read</oa></addata></record> |
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subjects | Acetylcholine receptors (muscarinic) Acetylcholine receptors (nicotinic) Animals Basal forebrain Beta Rhythm - drug effects Cholinergic Agents - pharmacology Compounds Deep Brain Stimulation Electrical stimuli Electrodes Evoked Potentials, Visual Experiments Forebrain Frequency dependence GABA Agonists - pharmacology GABA Antagonists - pharmacology Gamma Rhythm - drug effects Male Neurons Neurosciences Orientation Orientation behavior Oscillations Pharmacology Photic Stimulation Rats Receptors Receptors, Nicotinic - metabolism Rodents Sensitivity Sensitivity enhancement Stimulation Training Visual cortex Visual Cortex - drug effects Visual Cortex - physiology Visual evoked potentials Visual pathways Visual stimuli γ-Aminobutyric acid A receptors |
title | Pharmacological Mechanisms of Cortical Enhancement Induced by the Repetitive Pairing of Visual/Cholinergic Stimulation |
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