Amelioration of oxidative stress-induced phenotype loss of parvalbumin interneurons might contribute to the beneficial effects of environmental enrichment in a rat model of post-traumatic stress disorder
•NOX2 activation leads to ROS overproduction in a rat model of PTSD.•Excessive oxidative stress elicits phenotype loss of PV interneurons.•Phenotype loss of PV interneurons might contribute to abnormal behaviors in this PTSD model.•EE reverses all these abnormalities in this PTSD model. Post-traumat...
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description | •NOX2 activation leads to ROS overproduction in a rat model of PTSD.•Excessive oxidative stress elicits phenotype loss of PV interneurons.•Phenotype loss of PV interneurons might contribute to abnormal behaviors in this PTSD model.•EE reverses all these abnormalities in this PTSD model.
Post-traumatic stress disorder (PTSD) is a common psychiatric disease following exposure to a severe traumatic event or physiological stress, which is characterized by anxiety- and depression-like behaviors and cognitive impairment. However, the underlying mechanisms remain elusive. Parvalbumin (PV) interneurons that are susceptible to oxidative stress are a subset of inhibitory GABAergic neurons regulating the excitability of pyramidal neurons, while dysfunction of PV interneurons is casually linked to many mental disorders including PTSD. We therefore hypothesized that environmental enrichment (EE), a method of enhanced cognitive, sensory and motor stimulation, can reverse the behavioral impairments by normalizing PV interneurons in a rat model of PTSD induced by inescapable foot shocks (IFS). Behavioral changes were determined by the open field, elevated plus maze, fear conditioning, and Morris water maze tests. The levels of nicotinamide adenosine dinucleotide phosphate (NADPH) oxidase 2 (NOX2), NOX4, PV, glutamic acid decarboxylase 67 (GAD-67), and 8-hydroxy-2-deoxyguanosine (8-OH-dG) in the hippocampus and prefrontal cortex were determined. Our results showed that in this PTSD model, rats displayed the anxiety-like behavior, enhanced fear learning behavior, and hippocampus- dependent spatial memory deficit, which were accompanied by the up-regulation of NOX2, 8-OH-dG, and down-regulation of PV and GAD-67. Notably, EE reversed all these abnormalities. These results suggest that restoration of PV interneurons by inhibiting oxidative stress in the hippocampus and prefrontal cortex might represent a mechanism through which EE reverses the behavioral impairments in a rat model of PTSD induced by IFS. |
doi_str_mv | 10.1016/j.bbr.2016.06.016 |
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Post-traumatic stress disorder (PTSD) is a common psychiatric disease following exposure to a severe traumatic event or physiological stress, which is characterized by anxiety- and depression-like behaviors and cognitive impairment. However, the underlying mechanisms remain elusive. Parvalbumin (PV) interneurons that are susceptible to oxidative stress are a subset of inhibitory GABAergic neurons regulating the excitability of pyramidal neurons, while dysfunction of PV interneurons is casually linked to many mental disorders including PTSD. We therefore hypothesized that environmental enrichment (EE), a method of enhanced cognitive, sensory and motor stimulation, can reverse the behavioral impairments by normalizing PV interneurons in a rat model of PTSD induced by inescapable foot shocks (IFS). Behavioral changes were determined by the open field, elevated plus maze, fear conditioning, and Morris water maze tests. The levels of nicotinamide adenosine dinucleotide phosphate (NADPH) oxidase 2 (NOX2), NOX4, PV, glutamic acid decarboxylase 67 (GAD-67), and 8-hydroxy-2-deoxyguanosine (8-OH-dG) in the hippocampus and prefrontal cortex were determined. Our results showed that in this PTSD model, rats displayed the anxiety-like behavior, enhanced fear learning behavior, and hippocampus- dependent spatial memory deficit, which were accompanied by the up-regulation of NOX2, 8-OH-dG, and down-regulation of PV and GAD-67. Notably, EE reversed all these abnormalities. These results suggest that restoration of PV interneurons by inhibiting oxidative stress in the hippocampus and prefrontal cortex might represent a mechanism through which EE reverses the behavioral impairments in a rat model of PTSD induced by IFS.</description><identifier>ISSN: 0166-4328</identifier><identifier>EISSN: 1872-7549</identifier><identifier>DOI: 10.1016/j.bbr.2016.06.016</identifier><identifier>PMID: 27297027</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Animals ; Anxiety ; Conditioning, Classical ; Deoxyguanosine - analogs & derivatives ; Deoxyguanosine - metabolism ; Disease Models, Animal ; Electroshock ; Environment ; Environmental enrichment ; Fear ; GABAergic Neurons - metabolism ; Glutamate Decarboxylase - metabolism ; Hippocampus - metabolism ; Interneurons - metabolism ; Male ; Maze Learning ; NADP - metabolism ; NADPH Oxidase 2 - metabolism ; NADPH Oxidase 4 - metabolism ; Oxidative Stress ; Parvalbumin ; Parvalbumins - metabolism ; Phenotype ; Post-traumatic stress disorder ; Prefrontal Cortex - metabolism ; Rats ; Rats, Sprague-Dawley ; Reactive Oxygen Species ; Spatial Memory ; Stress Disorders, Post-Traumatic - metabolism ; Stress Disorders, Post-Traumatic - prevention & control ; Stress Disorders, Post-Traumatic - psychology</subject><ispartof>Behavioural brain research, 2016-10, Vol.312, p.84-92</ispartof><rights>2016 Elsevier B.V.</rights><rights>Copyright © 2016 Elsevier B.V. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c419t-489fdc96d6275f850b622e12ae070d36e4443573dbb586469b06b66d07e1616e3</citedby><cites>FETCH-LOGICAL-c419t-489fdc96d6275f850b622e12ae070d36e4443573dbb586469b06b66d07e1616e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.bbr.2016.06.016$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27297027$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sun, Xiao R.</creatorcontrib><creatorcontrib>Zhang, Hui</creatorcontrib><creatorcontrib>Zhao, Hong T.</creatorcontrib><creatorcontrib>Ji, Mu H.</creatorcontrib><creatorcontrib>Li, Hui H.</creatorcontrib><creatorcontrib>Wu, Jing</creatorcontrib><creatorcontrib>Li, Kuan Y.</creatorcontrib><creatorcontrib>Yang, Jian J.</creatorcontrib><title>Amelioration of oxidative stress-induced phenotype loss of parvalbumin interneurons might contribute to the beneficial effects of environmental enrichment in a rat model of post-traumatic stress disorder</title><title>Behavioural brain research</title><addtitle>Behav Brain Res</addtitle><description>•NOX2 activation leads to ROS overproduction in a rat model of PTSD.•Excessive oxidative stress elicits phenotype loss of PV interneurons.•Phenotype loss of PV interneurons might contribute to abnormal behaviors in this PTSD model.•EE reverses all these abnormalities in this PTSD model.
Post-traumatic stress disorder (PTSD) is a common psychiatric disease following exposure to a severe traumatic event or physiological stress, which is characterized by anxiety- and depression-like behaviors and cognitive impairment. However, the underlying mechanisms remain elusive. Parvalbumin (PV) interneurons that are susceptible to oxidative stress are a subset of inhibitory GABAergic neurons regulating the excitability of pyramidal neurons, while dysfunction of PV interneurons is casually linked to many mental disorders including PTSD. We therefore hypothesized that environmental enrichment (EE), a method of enhanced cognitive, sensory and motor stimulation, can reverse the behavioral impairments by normalizing PV interneurons in a rat model of PTSD induced by inescapable foot shocks (IFS). Behavioral changes were determined by the open field, elevated plus maze, fear conditioning, and Morris water maze tests. The levels of nicotinamide adenosine dinucleotide phosphate (NADPH) oxidase 2 (NOX2), NOX4, PV, glutamic acid decarboxylase 67 (GAD-67), and 8-hydroxy-2-deoxyguanosine (8-OH-dG) in the hippocampus and prefrontal cortex were determined. Our results showed that in this PTSD model, rats displayed the anxiety-like behavior, enhanced fear learning behavior, and hippocampus- dependent spatial memory deficit, which were accompanied by the up-regulation of NOX2, 8-OH-dG, and down-regulation of PV and GAD-67. Notably, EE reversed all these abnormalities. These results suggest that restoration of PV interneurons by inhibiting oxidative stress in the hippocampus and prefrontal cortex might represent a mechanism through which EE reverses the behavioral impairments in a rat model of PTSD induced by IFS.</description><subject>Animals</subject><subject>Anxiety</subject><subject>Conditioning, Classical</subject><subject>Deoxyguanosine - analogs & derivatives</subject><subject>Deoxyguanosine - metabolism</subject><subject>Disease Models, Animal</subject><subject>Electroshock</subject><subject>Environment</subject><subject>Environmental enrichment</subject><subject>Fear</subject><subject>GABAergic Neurons - metabolism</subject><subject>Glutamate Decarboxylase - metabolism</subject><subject>Hippocampus - metabolism</subject><subject>Interneurons - metabolism</subject><subject>Male</subject><subject>Maze Learning</subject><subject>NADP - metabolism</subject><subject>NADPH Oxidase 2 - metabolism</subject><subject>NADPH Oxidase 4 - metabolism</subject><subject>Oxidative Stress</subject><subject>Parvalbumin</subject><subject>Parvalbumins - metabolism</subject><subject>Phenotype</subject><subject>Post-traumatic stress disorder</subject><subject>Prefrontal Cortex - metabolism</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Reactive Oxygen Species</subject><subject>Spatial Memory</subject><subject>Stress Disorders, Post-Traumatic - metabolism</subject><subject>Stress Disorders, Post-Traumatic - prevention & control</subject><subject>Stress Disorders, Post-Traumatic - psychology</subject><issn>0166-4328</issn><issn>1872-7549</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNUcuO1DAQtBCIHRY-gAvykUsG23HsRJxWq-UhrcQFzpYfHcajxA62M2K_kZ_C2Rk4IqSW7LarqltVCL2mZE8JFe-Oe2PSntXrntSi4gna0V6yRnZ8eIp29UU0vGX9FXqR85EQwklHn6MrJtkgCZM79OtmhsnHpIuPAccRx5_e1eYEOJcEOTc-uNWCw8sBQiwPC-Ap5rxBF51OejLr7AP2oUAKsKYYMp7990PBNoaSvFkL4BJxOQA2EGD01usJwziCLY8yEE6-0mYIZfsIydvD1lRNrHHdDM_RwfQ4MebSlKTXua5oLxti53NMDtJL9GzUU4ZXl_Mafftw9_X2U3P_5ePn25v7xnI6lIb3w-jsIJxgshv7jhjBGFCmgUjiWgGc87aTrTOm6wUXgyHCCOGIBCqogPYavT3rLin-WCEXNftsYZp0gLhmRXtK-0EOTP4HlPSCtIPgFUrPUJuqvwlGtSQ_6_SgKFFb3Oqoatxqi1uRWlRUzpuL_GpmcH8Zf_KtgPdnAFQ_Th6SytZDqHn6VP1XLvp_yP8GKj_AXQ</recordid><startdate>20161001</startdate><enddate>20161001</enddate><creator>Sun, Xiao R.</creator><creator>Zhang, Hui</creator><creator>Zhao, Hong T.</creator><creator>Ji, Mu H.</creator><creator>Li, Hui H.</creator><creator>Wu, Jing</creator><creator>Li, Kuan Y.</creator><creator>Yang, Jian J.</creator><general>Elsevier B.V</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>7QG</scope><scope>7TK</scope></search><sort><creationdate>20161001</creationdate><title>Amelioration of oxidative stress-induced phenotype loss of parvalbumin interneurons might contribute to the beneficial effects of environmental enrichment in a rat model of post-traumatic stress disorder</title><author>Sun, Xiao R. ; Zhang, Hui ; Zhao, Hong T. ; Ji, Mu H. ; Li, Hui H. ; Wu, Jing ; Li, Kuan Y. ; Yang, Jian J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c419t-489fdc96d6275f850b622e12ae070d36e4443573dbb586469b06b66d07e1616e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Animals</topic><topic>Anxiety</topic><topic>Conditioning, Classical</topic><topic>Deoxyguanosine - analogs & derivatives</topic><topic>Deoxyguanosine - metabolism</topic><topic>Disease Models, Animal</topic><topic>Electroshock</topic><topic>Environment</topic><topic>Environmental enrichment</topic><topic>Fear</topic><topic>GABAergic Neurons - metabolism</topic><topic>Glutamate Decarboxylase - metabolism</topic><topic>Hippocampus - metabolism</topic><topic>Interneurons - metabolism</topic><topic>Male</topic><topic>Maze Learning</topic><topic>NADP - metabolism</topic><topic>NADPH Oxidase 2 - metabolism</topic><topic>NADPH Oxidase 4 - metabolism</topic><topic>Oxidative Stress</topic><topic>Parvalbumin</topic><topic>Parvalbumins - metabolism</topic><topic>Phenotype</topic><topic>Post-traumatic stress disorder</topic><topic>Prefrontal Cortex - metabolism</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>Reactive Oxygen Species</topic><topic>Spatial Memory</topic><topic>Stress Disorders, Post-Traumatic - metabolism</topic><topic>Stress Disorders, Post-Traumatic - prevention & control</topic><topic>Stress Disorders, Post-Traumatic - psychology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sun, Xiao R.</creatorcontrib><creatorcontrib>Zhang, Hui</creatorcontrib><creatorcontrib>Zhao, Hong T.</creatorcontrib><creatorcontrib>Ji, Mu H.</creatorcontrib><creatorcontrib>Li, Hui H.</creatorcontrib><creatorcontrib>Wu, Jing</creatorcontrib><creatorcontrib>Li, Kuan Y.</creatorcontrib><creatorcontrib>Yang, Jian J.</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>Animal Behavior Abstracts</collection><collection>Neurosciences Abstracts</collection><jtitle>Behavioural brain research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sun, Xiao R.</au><au>Zhang, Hui</au><au>Zhao, Hong T.</au><au>Ji, Mu H.</au><au>Li, Hui H.</au><au>Wu, Jing</au><au>Li, Kuan Y.</au><au>Yang, Jian J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Amelioration of oxidative stress-induced phenotype loss of parvalbumin interneurons might contribute to the beneficial effects of environmental enrichment in a rat model of post-traumatic stress disorder</atitle><jtitle>Behavioural brain research</jtitle><addtitle>Behav Brain Res</addtitle><date>2016-10-01</date><risdate>2016</risdate><volume>312</volume><spage>84</spage><epage>92</epage><pages>84-92</pages><issn>0166-4328</issn><eissn>1872-7549</eissn><abstract>•NOX2 activation leads to ROS overproduction in a rat model of PTSD.•Excessive oxidative stress elicits phenotype loss of PV interneurons.•Phenotype loss of PV interneurons might contribute to abnormal behaviors in this PTSD model.•EE reverses all these abnormalities in this PTSD model.
Post-traumatic stress disorder (PTSD) is a common psychiatric disease following exposure to a severe traumatic event or physiological stress, which is characterized by anxiety- and depression-like behaviors and cognitive impairment. However, the underlying mechanisms remain elusive. Parvalbumin (PV) interneurons that are susceptible to oxidative stress are a subset of inhibitory GABAergic neurons regulating the excitability of pyramidal neurons, while dysfunction of PV interneurons is casually linked to many mental disorders including PTSD. We therefore hypothesized that environmental enrichment (EE), a method of enhanced cognitive, sensory and motor stimulation, can reverse the behavioral impairments by normalizing PV interneurons in a rat model of PTSD induced by inescapable foot shocks (IFS). Behavioral changes were determined by the open field, elevated plus maze, fear conditioning, and Morris water maze tests. The levels of nicotinamide adenosine dinucleotide phosphate (NADPH) oxidase 2 (NOX2), NOX4, PV, glutamic acid decarboxylase 67 (GAD-67), and 8-hydroxy-2-deoxyguanosine (8-OH-dG) in the hippocampus and prefrontal cortex were determined. Our results showed that in this PTSD model, rats displayed the anxiety-like behavior, enhanced fear learning behavior, and hippocampus- dependent spatial memory deficit, which were accompanied by the up-regulation of NOX2, 8-OH-dG, and down-regulation of PV and GAD-67. Notably, EE reversed all these abnormalities. These results suggest that restoration of PV interneurons by inhibiting oxidative stress in the hippocampus and prefrontal cortex might represent a mechanism through which EE reverses the behavioral impairments in a rat model of PTSD induced by IFS.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>27297027</pmid><doi>10.1016/j.bbr.2016.06.016</doi><tpages>9</tpages></addata></record> |
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subjects | Animals Anxiety Conditioning, Classical Deoxyguanosine - analogs & derivatives Deoxyguanosine - metabolism Disease Models, Animal Electroshock Environment Environmental enrichment Fear GABAergic Neurons - metabolism Glutamate Decarboxylase - metabolism Hippocampus - metabolism Interneurons - metabolism Male Maze Learning NADP - metabolism NADPH Oxidase 2 - metabolism NADPH Oxidase 4 - metabolism Oxidative Stress Parvalbumin Parvalbumins - metabolism Phenotype Post-traumatic stress disorder Prefrontal Cortex - metabolism Rats Rats, Sprague-Dawley Reactive Oxygen Species Spatial Memory Stress Disorders, Post-Traumatic - metabolism Stress Disorders, Post-Traumatic - prevention & control Stress Disorders, Post-Traumatic - psychology |
title | Amelioration of oxidative stress-induced phenotype loss of parvalbumin interneurons might contribute to the beneficial effects of environmental enrichment in a rat model of post-traumatic stress disorder |
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