Levels of Neural Progenitors in the Hippocampus Predict Memory Impairment and Relapse to Drug Seeking as a Function of Excessive Methamphetamine Self-Administration
Methamphetamine affects the hippocampus, a brain region crucial for learning and memory, as well as relapse to drug seeking. Rats self-administered methamphetamine for 1 h twice weekly (intermittent-short-I-ShA), 1 h daily (limited-short-ShA), or 6 h daily (extended-long-LgA) for 22 sessions. After...
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creator | RECINTO, Patrick SAMANT, Anjalirose H GEORGE, Olivier MANDYAM, Chitra D CHAVEZ, Gustavo KIM, Airee YUAN, Clara J SOLEIMAN, Matthew GRANT, Yanabel EDWARDS, Scott WEE, Sunmee KOOB, George F |
description | Methamphetamine affects the hippocampus, a brain region crucial for learning and memory, as well as relapse to drug seeking. Rats self-administered methamphetamine for 1 h twice weekly (intermittent-short-I-ShA), 1 h daily (limited-short-ShA), or 6 h daily (extended-long-LgA) for 22 sessions. After 22 sessions, rats from each access group were withdrawn from self-administration and underwent spatial memory (Y-maze) and working memory (T-maze) tests followed by extinction and reinstatement to methamphetamine seeking or received one intraperitoneal injection of 5-bromo-2'-deoxyuridine (BrdU) to label progenitors in the hippocampal subgranular zone (SGZ) during the synthesis phase. Two-hour-old and 28-day-old surviving BrdU-immunoreactive cells were quantified. I-ShA rats performed better on the Y-maze and had a greater number of 2-h-old SGZ BrdU cells than nondrug controls. LgA rats, but not ShA rats, performed worse on the Y- and T-maze and had a fewer number of 2-h-old SGZ BrdU cells than nondrug and I-ShA rats, suggesting that new hippocampal progenitors, decreased by methamphetamine, were correlated with impairment in the acquisition of new spatial cues. Analyses of addiction-related behaviors after withdrawal and extinction training revealed methamphetamine-primed reinstatement of methamphetamine-seeking behavior in all three groups (I-ShA, ShA, and LgA), and this effect was enhanced in LgA rats compared with I-ShA and ShA rats. Protracted withdrawal from self-administration enhanced the survival of SGZ BrdU cells, and methamphetamine seeking during protracted withdrawal enhanced Fos expression in the dentate gyrus and medial prefrontal cortex in LgA rats to a greater extent than in ShA and I-ShA rats. These results indicate that changes in the levels of the proliferation and survival of hippocampal neural progenitors and neuronal activation of hippocampal granule cells predict the effects of methamphetamine self-administration (limited vs extended access) on cognitive performance and relapse to drug seeking and may contribute to the impairments that perpetuate the addiction cycle. |
doi_str_mv | 10.1038/npp.2011.315 |
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Rats self-administered methamphetamine for 1 h twice weekly (intermittent-short-I-ShA), 1 h daily (limited-short-ShA), or 6 h daily (extended-long-LgA) for 22 sessions. After 22 sessions, rats from each access group were withdrawn from self-administration and underwent spatial memory (Y-maze) and working memory (T-maze) tests followed by extinction and reinstatement to methamphetamine seeking or received one intraperitoneal injection of 5-bromo-2'-deoxyuridine (BrdU) to label progenitors in the hippocampal subgranular zone (SGZ) during the synthesis phase. Two-hour-old and 28-day-old surviving BrdU-immunoreactive cells were quantified. I-ShA rats performed better on the Y-maze and had a greater number of 2-h-old SGZ BrdU cells than nondrug controls. LgA rats, but not ShA rats, performed worse on the Y- and T-maze and had a fewer number of 2-h-old SGZ BrdU cells than nondrug and I-ShA rats, suggesting that new hippocampal progenitors, decreased by methamphetamine, were correlated with impairment in the acquisition of new spatial cues. Analyses of addiction-related behaviors after withdrawal and extinction training revealed methamphetamine-primed reinstatement of methamphetamine-seeking behavior in all three groups (I-ShA, ShA, and LgA), and this effect was enhanced in LgA rats compared with I-ShA and ShA rats. Protracted withdrawal from self-administration enhanced the survival of SGZ BrdU cells, and methamphetamine seeking during protracted withdrawal enhanced Fos expression in the dentate gyrus and medial prefrontal cortex in LgA rats to a greater extent than in ShA and I-ShA rats. These results indicate that changes in the levels of the proliferation and survival of hippocampal neural progenitors and neuronal activation of hippocampal granule cells predict the effects of methamphetamine self-administration (limited vs extended access) on cognitive performance and relapse to drug seeking and may contribute to the impairments that perpetuate the addiction cycle.</description><identifier>ISSN: 0893-133X</identifier><identifier>EISSN: 1740-634X</identifier><identifier>DOI: 10.1038/npp.2011.315</identifier><identifier>PMID: 22205547</identifier><identifier>CODEN: NEROEW</identifier><language>eng</language><publisher>Basingstoke: Nature Publishing Group</publisher><subject>Addictions ; Addictive behaviors ; Adult and adolescent clinical studies ; Adult Stem Cells - drug effects ; Adult Stem Cells - physiology ; Analysis of Variance ; Animals ; Behavior ; Behavior, Addictive - chemically induced ; Behavior, Addictive - psychology ; Biological and medical sciences ; Bromodeoxyuridine - metabolism ; Caspase 3 - metabolism ; Central Nervous System Stimulants - administration & dosage ; Conditioning, Operant - drug effects ; Conditioning, Operant - physiology ; Drug addiction ; Drug withdrawal ; Extinction, Psychological - drug effects ; Extinction, Psychological - physiology ; Hippocampus - cytology ; Hypotheses ; Ki-67 Antigen - metabolism ; Male ; Maze Learning - drug effects ; Maze Learning - physiology ; Medical sciences ; Memory ; Memory Disorders - chemically induced ; Memory Disorders - pathology ; Memory, Short-Term - drug effects ; Memory, Short-Term - physiology ; Methamphetamine ; Methamphetamine - administration & dosage ; Neurobiology ; Neurogenesis ; Neurogenesis - drug effects ; Neurogenesis - physiology ; Neuropharmacology ; Neurosciences ; Original ; Pharmacology. Drug treatments ; Proto-Oncogene Proteins c-fos - metabolism ; Psychoanaleptics: cns stimulant, antidepressant agent, nootropic agent, mood stabilizer ; Psychoanaleptics: cns stimulant, antidepressant agent, nootropic agent, mood stabilizer..., (alzheimer disease) ; Psychology. Psychoanalysis. Psychiatry ; Psychopathology. Psychiatry ; Psychopharmacology ; Rats ; Rats, Wistar ; Reinforcement Schedule ; Self Administration ; Space Perception - drug effects ; Time Factors</subject><ispartof>Neuropsychopharmacology (New York, N.Y.), 2012-04, Vol.37 (5), p.1275-1287</ispartof><rights>2015 INIST-CNRS</rights><rights>Copyright Nature Publishing Group Apr 2012</rights><rights>Copyright © 2012 American College of Neuropsychopharmacology 2012 American College of Neuropsychopharmacology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c472t-13f54b42d4e24fd96c7542aef4fac4e79a8596327943465013d7442127fb65363</citedby><cites>FETCH-LOGICAL-c472t-13f54b42d4e24fd96c7542aef4fac4e79a8596327943465013d7442127fb65363</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/PMC3306889/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3306889/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=25789462$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22205547$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>RECINTO, Patrick</creatorcontrib><creatorcontrib>SAMANT, Anjalirose H</creatorcontrib><creatorcontrib>GEORGE, Olivier</creatorcontrib><creatorcontrib>MANDYAM, Chitra D</creatorcontrib><creatorcontrib>CHAVEZ, Gustavo</creatorcontrib><creatorcontrib>KIM, Airee</creatorcontrib><creatorcontrib>YUAN, Clara J</creatorcontrib><creatorcontrib>SOLEIMAN, Matthew</creatorcontrib><creatorcontrib>GRANT, Yanabel</creatorcontrib><creatorcontrib>EDWARDS, Scott</creatorcontrib><creatorcontrib>WEE, Sunmee</creatorcontrib><creatorcontrib>KOOB, George F</creatorcontrib><title>Levels of Neural Progenitors in the Hippocampus Predict Memory Impairment and Relapse to Drug Seeking as a Function of Excessive Methamphetamine Self-Administration</title><title>Neuropsychopharmacology (New York, N.Y.)</title><addtitle>Neuropsychopharmacology</addtitle><description>Methamphetamine affects the hippocampus, a brain region crucial for learning and memory, as well as relapse to drug seeking. Rats self-administered methamphetamine for 1 h twice weekly (intermittent-short-I-ShA), 1 h daily (limited-short-ShA), or 6 h daily (extended-long-LgA) for 22 sessions. After 22 sessions, rats from each access group were withdrawn from self-administration and underwent spatial memory (Y-maze) and working memory (T-maze) tests followed by extinction and reinstatement to methamphetamine seeking or received one intraperitoneal injection of 5-bromo-2'-deoxyuridine (BrdU) to label progenitors in the hippocampal subgranular zone (SGZ) during the synthesis phase. Two-hour-old and 28-day-old surviving BrdU-immunoreactive cells were quantified. I-ShA rats performed better on the Y-maze and had a greater number of 2-h-old SGZ BrdU cells than nondrug controls. LgA rats, but not ShA rats, performed worse on the Y- and T-maze and had a fewer number of 2-h-old SGZ BrdU cells than nondrug and I-ShA rats, suggesting that new hippocampal progenitors, decreased by methamphetamine, were correlated with impairment in the acquisition of new spatial cues. Analyses of addiction-related behaviors after withdrawal and extinction training revealed methamphetamine-primed reinstatement of methamphetamine-seeking behavior in all three groups (I-ShA, ShA, and LgA), and this effect was enhanced in LgA rats compared with I-ShA and ShA rats. Protracted withdrawal from self-administration enhanced the survival of SGZ BrdU cells, and methamphetamine seeking during protracted withdrawal enhanced Fos expression in the dentate gyrus and medial prefrontal cortex in LgA rats to a greater extent than in ShA and I-ShA rats. These results indicate that changes in the levels of the proliferation and survival of hippocampal neural progenitors and neuronal activation of hippocampal granule cells predict the effects of methamphetamine self-administration (limited vs extended access) on cognitive performance and relapse to drug seeking and may contribute to the impairments that perpetuate the addiction cycle.</description><subject>Addictions</subject><subject>Addictive behaviors</subject><subject>Adult and adolescent clinical studies</subject><subject>Adult Stem Cells - drug effects</subject><subject>Adult Stem Cells - physiology</subject><subject>Analysis of Variance</subject><subject>Animals</subject><subject>Behavior</subject><subject>Behavior, Addictive - chemically induced</subject><subject>Behavior, Addictive - psychology</subject><subject>Biological and medical sciences</subject><subject>Bromodeoxyuridine - metabolism</subject><subject>Caspase 3 - metabolism</subject><subject>Central Nervous System Stimulants - administration & dosage</subject><subject>Conditioning, Operant - drug effects</subject><subject>Conditioning, Operant - physiology</subject><subject>Drug addiction</subject><subject>Drug withdrawal</subject><subject>Extinction, Psychological - drug effects</subject><subject>Extinction, Psychological - physiology</subject><subject>Hippocampus - cytology</subject><subject>Hypotheses</subject><subject>Ki-67 Antigen - metabolism</subject><subject>Male</subject><subject>Maze Learning - drug effects</subject><subject>Maze Learning - physiology</subject><subject>Medical sciences</subject><subject>Memory</subject><subject>Memory Disorders - chemically induced</subject><subject>Memory Disorders - pathology</subject><subject>Memory, Short-Term - drug effects</subject><subject>Memory, Short-Term - physiology</subject><subject>Methamphetamine</subject><subject>Methamphetamine - administration & dosage</subject><subject>Neurobiology</subject><subject>Neurogenesis</subject><subject>Neurogenesis - drug effects</subject><subject>Neurogenesis - physiology</subject><subject>Neuropharmacology</subject><subject>Neurosciences</subject><subject>Original</subject><subject>Pharmacology. 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Psychiatry</topic><topic>Psychopharmacology</topic><topic>Rats</topic><topic>Rats, Wistar</topic><topic>Reinforcement Schedule</topic><topic>Self Administration</topic><topic>Space Perception - drug effects</topic><topic>Time Factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>RECINTO, Patrick</creatorcontrib><creatorcontrib>SAMANT, Anjalirose H</creatorcontrib><creatorcontrib>GEORGE, Olivier</creatorcontrib><creatorcontrib>MANDYAM, Chitra D</creatorcontrib><creatorcontrib>CHAVEZ, Gustavo</creatorcontrib><creatorcontrib>KIM, Airee</creatorcontrib><creatorcontrib>YUAN, Clara J</creatorcontrib><creatorcontrib>SOLEIMAN, Matthew</creatorcontrib><creatorcontrib>GRANT, Yanabel</creatorcontrib><creatorcontrib>EDWARDS, Scott</creatorcontrib><creatorcontrib>WEE, Sunmee</creatorcontrib><creatorcontrib>KOOB, George F</creatorcontrib><collection>Pascal-Francis</collection><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>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>ProQuest SciTech 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>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Psychology Database</collection><collection>Biological Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Neuropsychopharmacology (New York, N.Y.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>RECINTO, Patrick</au><au>SAMANT, Anjalirose H</au><au>GEORGE, Olivier</au><au>MANDYAM, Chitra D</au><au>CHAVEZ, Gustavo</au><au>KIM, Airee</au><au>YUAN, Clara J</au><au>SOLEIMAN, Matthew</au><au>GRANT, Yanabel</au><au>EDWARDS, Scott</au><au>WEE, Sunmee</au><au>KOOB, George F</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Levels of Neural Progenitors in the Hippocampus Predict Memory Impairment and Relapse to Drug Seeking as a Function of Excessive Methamphetamine Self-Administration</atitle><jtitle>Neuropsychopharmacology (New York, N.Y.)</jtitle><addtitle>Neuropsychopharmacology</addtitle><date>2012-04-01</date><risdate>2012</risdate><volume>37</volume><issue>5</issue><spage>1275</spage><epage>1287</epage><pages>1275-1287</pages><issn>0893-133X</issn><eissn>1740-634X</eissn><coden>NEROEW</coden><abstract>Methamphetamine affects the hippocampus, a brain region crucial for learning and memory, as well as relapse to drug seeking. Rats self-administered methamphetamine for 1 h twice weekly (intermittent-short-I-ShA), 1 h daily (limited-short-ShA), or 6 h daily (extended-long-LgA) for 22 sessions. After 22 sessions, rats from each access group were withdrawn from self-administration and underwent spatial memory (Y-maze) and working memory (T-maze) tests followed by extinction and reinstatement to methamphetamine seeking or received one intraperitoneal injection of 5-bromo-2'-deoxyuridine (BrdU) to label progenitors in the hippocampal subgranular zone (SGZ) during the synthesis phase. Two-hour-old and 28-day-old surviving BrdU-immunoreactive cells were quantified. I-ShA rats performed better on the Y-maze and had a greater number of 2-h-old SGZ BrdU cells than nondrug controls. LgA rats, but not ShA rats, performed worse on the Y- and T-maze and had a fewer number of 2-h-old SGZ BrdU cells than nondrug and I-ShA rats, suggesting that new hippocampal progenitors, decreased by methamphetamine, were correlated with impairment in the acquisition of new spatial cues. Analyses of addiction-related behaviors after withdrawal and extinction training revealed methamphetamine-primed reinstatement of methamphetamine-seeking behavior in all three groups (I-ShA, ShA, and LgA), and this effect was enhanced in LgA rats compared with I-ShA and ShA rats. Protracted withdrawal from self-administration enhanced the survival of SGZ BrdU cells, and methamphetamine seeking during protracted withdrawal enhanced Fos expression in the dentate gyrus and medial prefrontal cortex in LgA rats to a greater extent than in ShA and I-ShA rats. These results indicate that changes in the levels of the proliferation and survival of hippocampal neural progenitors and neuronal activation of hippocampal granule cells predict the effects of methamphetamine self-administration (limited vs extended access) on cognitive performance and relapse to drug seeking and may contribute to the impairments that perpetuate the addiction cycle.</abstract><cop>Basingstoke</cop><pub>Nature Publishing Group</pub><pmid>22205547</pmid><doi>10.1038/npp.2011.315</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 0893-133X |
ispartof | Neuropsychopharmacology (New York, N.Y.), 2012-04, Vol.37 (5), p.1275-1287 |
issn | 0893-133X 1740-634X |
language | eng |
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source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; SpringerLink Journals - AutoHoldings |
subjects | Addictions Addictive behaviors Adult and adolescent clinical studies Adult Stem Cells - drug effects Adult Stem Cells - physiology Analysis of Variance Animals Behavior Behavior, Addictive - chemically induced Behavior, Addictive - psychology Biological and medical sciences Bromodeoxyuridine - metabolism Caspase 3 - metabolism Central Nervous System Stimulants - administration & dosage Conditioning, Operant - drug effects Conditioning, Operant - physiology Drug addiction Drug withdrawal Extinction, Psychological - drug effects Extinction, Psychological - physiology Hippocampus - cytology Hypotheses Ki-67 Antigen - metabolism Male Maze Learning - drug effects Maze Learning - physiology Medical sciences Memory Memory Disorders - chemically induced Memory Disorders - pathology Memory, Short-Term - drug effects Memory, Short-Term - physiology Methamphetamine Methamphetamine - administration & dosage Neurobiology Neurogenesis Neurogenesis - drug effects Neurogenesis - physiology Neuropharmacology Neurosciences Original Pharmacology. Drug treatments Proto-Oncogene Proteins c-fos - metabolism Psychoanaleptics: cns stimulant, antidepressant agent, nootropic agent, mood stabilizer Psychoanaleptics: cns stimulant, antidepressant agent, nootropic agent, mood stabilizer..., (alzheimer disease) Psychology. Psychoanalysis. Psychiatry Psychopathology. Psychiatry Psychopharmacology Rats Rats, Wistar Reinforcement Schedule Self Administration Space Perception - drug effects Time Factors |
title | Levels of Neural Progenitors in the Hippocampus Predict Memory Impairment and Relapse to Drug Seeking as a Function of Excessive Methamphetamine Self-Administration |
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