Functional neuroimaging study in identical twin pairs discordant for regular cigarette smoking
ABSTRACT Despite the tremendous public health and financial burden of cigarette smoking, relatively little is understood about brain mechanisms that subserve smoking behavior. This study investigated the effect of lifetime regular smoking on brain processing in a reward guessing task using functiona...
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Veröffentlicht in: | Addiction biology 2013-01, Vol.18 (1), p.98-108 |
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creator | Lessov-Schlaggar, Christina N. Lepore, Rebecca L. Kristjansson, Sean D. Schlaggar, Bradley L. Barnes, Kelly Anne Petersen, Steven E. Madden, Pamela A. F. Heath, Andrew C. Barch, Deanna M. |
description | ABSTRACT
Despite the tremendous public health and financial burden of cigarette smoking, relatively little is understood about brain mechanisms that subserve smoking behavior. This study investigated the effect of lifetime regular smoking on brain processing in a reward guessing task using functional magnetic resonance imaging and a co‐twin control study design in monozygotic (MZ) twin pairs that maximally controls for genetic and family background factors. Young adult (24–34 years) MZ female twin pairs (n = 15 pairs), discordant for regular smoking defined using Centers for Disease Control criteria as having smoked ≥100 cigarettes in their lifetime, were recruited from an ongoing genetic epidemiological longitudinal study of substance use and psychopathology. We applied hypothesis‐driven region of interest (ROI) and whole‐brain analyses to investigate the effect of regular smoking on reward processing. Reduced response to reward and punishment in regular compared with never‐regular smokers was seen in hypothesis‐driven ROI analysis of bilateral ventral striatum. Whole‐brain analysis identified bilateral reward‐processing regions that showed activation differences in response to winning or losing money but no effect of regular smoking; and frontal/parietal regions, predominantly in the right hemisphere, that showed robust effect of regular smoking but no effect of winning or losing money. Altogether, using a study design that maximally controls for group differences, we found that regular smoking had modest effects on striatal reward processing regions but robust effects on cognitive control/attentional systems. |
doi_str_mv | 10.1111/j.1369-1600.2012.00435.x |
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Despite the tremendous public health and financial burden of cigarette smoking, relatively little is understood about brain mechanisms that subserve smoking behavior. This study investigated the effect of lifetime regular smoking on brain processing in a reward guessing task using functional magnetic resonance imaging and a co‐twin control study design in monozygotic (MZ) twin pairs that maximally controls for genetic and family background factors. Young adult (24–34 years) MZ female twin pairs (n = 15 pairs), discordant for regular smoking defined using Centers for Disease Control criteria as having smoked ≥100 cigarettes in their lifetime, were recruited from an ongoing genetic epidemiological longitudinal study of substance use and psychopathology. We applied hypothesis‐driven region of interest (ROI) and whole‐brain analyses to investigate the effect of regular smoking on reward processing. Reduced response to reward and punishment in regular compared with never‐regular smokers was seen in hypothesis‐driven ROI analysis of bilateral ventral striatum. Whole‐brain analysis identified bilateral reward‐processing regions that showed activation differences in response to winning or losing money but no effect of regular smoking; and frontal/parietal regions, predominantly in the right hemisphere, that showed robust effect of regular smoking but no effect of winning or losing money. Altogether, using a study design that maximally controls for group differences, we found that regular smoking had modest effects on striatal reward processing regions but robust effects on cognitive control/attentional systems.</description><identifier>ISSN: 1355-6215</identifier><identifier>EISSN: 1369-1600</identifier><identifier>DOI: 10.1111/j.1369-1600.2012.00435.x</identifier><identifier>PMID: 22340136</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Addiction ; Adolescent ; Adult ; Analysis of Variance ; Attention ; Basal Ganglia - blood supply ; Basal Ganglia - physiopathology ; Brain - blood supply ; Brain - physiopathology ; Cigarette smoking ; co-twin control ; cognitive control ; discordant ; Diseases in Twins ; Female ; fMRI ; Functional Neuroimaging - methods ; Humans ; Interview, Psychological ; Linear Models ; Magnetic Resonance Imaging - methods ; Oxygen - blood ; Prospective Studies ; Reward ; Smoking - genetics ; Smoking - physiopathology ; Twins, Monozygotic ; Young Adult</subject><ispartof>Addiction biology, 2013-01, Vol.18 (1), p.98-108</ispartof><rights>2012 The Authors, Addiction Biology © 2012 Society for the Study of Addiction</rights><rights>2012 The Authors, Addiction Biology © 2012 Society for the Study of Addiction.</rights><rights>2013 Society for the Study of Addiction</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5725-28c046378152b73d6c95ba8083ffbc72909f0b99c31c67fda1a06d243e28d9eb3</citedby><cites>FETCH-LOGICAL-c5725-28c046378152b73d6c95ba8083ffbc72909f0b99c31c67fda1a06d243e28d9eb3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fj.1369-1600.2012.00435.x$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fj.1369-1600.2012.00435.x$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22340136$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lessov-Schlaggar, Christina N.</creatorcontrib><creatorcontrib>Lepore, Rebecca L.</creatorcontrib><creatorcontrib>Kristjansson, Sean D.</creatorcontrib><creatorcontrib>Schlaggar, Bradley L.</creatorcontrib><creatorcontrib>Barnes, Kelly Anne</creatorcontrib><creatorcontrib>Petersen, Steven E.</creatorcontrib><creatorcontrib>Madden, Pamela A. F.</creatorcontrib><creatorcontrib>Heath, Andrew C.</creatorcontrib><creatorcontrib>Barch, Deanna M.</creatorcontrib><title>Functional neuroimaging study in identical twin pairs discordant for regular cigarette smoking</title><title>Addiction biology</title><addtitle>Addict Biol</addtitle><description>ABSTRACT
Despite the tremendous public health and financial burden of cigarette smoking, relatively little is understood about brain mechanisms that subserve smoking behavior. This study investigated the effect of lifetime regular smoking on brain processing in a reward guessing task using functional magnetic resonance imaging and a co‐twin control study design in monozygotic (MZ) twin pairs that maximally controls for genetic and family background factors. Young adult (24–34 years) MZ female twin pairs (n = 15 pairs), discordant for regular smoking defined using Centers for Disease Control criteria as having smoked ≥100 cigarettes in their lifetime, were recruited from an ongoing genetic epidemiological longitudinal study of substance use and psychopathology. We applied hypothesis‐driven region of interest (ROI) and whole‐brain analyses to investigate the effect of regular smoking on reward processing. Reduced response to reward and punishment in regular compared with never‐regular smokers was seen in hypothesis‐driven ROI analysis of bilateral ventral striatum. Whole‐brain analysis identified bilateral reward‐processing regions that showed activation differences in response to winning or losing money but no effect of regular smoking; and frontal/parietal regions, predominantly in the right hemisphere, that showed robust effect of regular smoking but no effect of winning or losing money. Altogether, using a study design that maximally controls for group differences, we found that regular smoking had modest effects on striatal reward processing regions but robust effects on cognitive control/attentional systems.</description><subject>Addiction</subject><subject>Adolescent</subject><subject>Adult</subject><subject>Analysis of Variance</subject><subject>Attention</subject><subject>Basal Ganglia - blood supply</subject><subject>Basal Ganglia - physiopathology</subject><subject>Brain - blood supply</subject><subject>Brain - physiopathology</subject><subject>Cigarette smoking</subject><subject>co-twin control</subject><subject>cognitive control</subject><subject>discordant</subject><subject>Diseases in Twins</subject><subject>Female</subject><subject>fMRI</subject><subject>Functional Neuroimaging - methods</subject><subject>Humans</subject><subject>Interview, Psychological</subject><subject>Linear Models</subject><subject>Magnetic Resonance Imaging - methods</subject><subject>Oxygen - blood</subject><subject>Prospective Studies</subject><subject>Reward</subject><subject>Smoking - genetics</subject><subject>Smoking - physiopathology</subject><subject>Twins, Monozygotic</subject><subject>Young Adult</subject><issn>1355-6215</issn><issn>1369-1600</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkUtv1DAUhSMEog_4C8gSGzZJ_YjtWEJIfbdSBRsQiAVXjuMETzPxYCd05t_X6ZQRsKo3tnW_c66vT5YhgguS1tGiIEyonAiMC4oJLTAuGS_Wz7L9XeH5fOY8F5TwvewgxgVOpOTsZbZHKStxIvezHxfTYEbnB92jwU7Bu6Xu3NChOE7NBrkBucYOozOpPt6l60q7EFHjovGh0cOIWh9QsN3U64CM63Sw42hRXPrbZPMqe9HqPtrXj_th9uXi_PPpVX7z6fL69PgmN1xSntPK4FIwWRFOa8kaYRSvdYUr1ra1kVRh1eJaKcOIEbJtNNFYNLRkllaNsjU7zD5sfVdTvbSNSU8OuodVSOOEDXjt4N_K4H5C538DKyWWTCWDd48Gwf-abBxhmUa0fa8H66cIpFRUpIbkCSiVjBDOKU7o2__QhZ9C-uvZULDUuXwwrLaUCT7GYNvduwmGOW9YwBwrzLHCnDc85A3rJH3z99w74Z-AE_B-C9y53m6ebAzHZyfpkOT5Vu7iaNc7uQ63ICSTHL5-vIRK8TP-7bsCxu4B7nvIqw</recordid><startdate>201301</startdate><enddate>201301</enddate><creator>Lessov-Schlaggar, Christina N.</creator><creator>Lepore, Rebecca L.</creator><creator>Kristjansson, Sean D.</creator><creator>Schlaggar, Bradley L.</creator><creator>Barnes, Kelly Anne</creator><creator>Petersen, Steven E.</creator><creator>Madden, Pamela A. F.</creator><creator>Heath, Andrew C.</creator><creator>Barch, Deanna M.</creator><general>Blackwell Publishing Ltd</general><general>John Wiley & Sons, Inc</general><scope>BSCLL</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>7T5</scope><scope>7TM</scope><scope>H94</scope><scope>7X8</scope><scope>7TK</scope><scope>5PM</scope></search><sort><creationdate>201301</creationdate><title>Functional neuroimaging study in identical twin pairs discordant for regular cigarette smoking</title><author>Lessov-Schlaggar, Christina N. ; Lepore, Rebecca L. ; Kristjansson, Sean D. ; Schlaggar, Bradley L. ; Barnes, Kelly Anne ; Petersen, Steven E. ; Madden, Pamela A. F. ; Heath, Andrew C. ; Barch, Deanna M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5725-28c046378152b73d6c95ba8083ffbc72909f0b99c31c67fda1a06d243e28d9eb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Addiction</topic><topic>Adolescent</topic><topic>Adult</topic><topic>Analysis of Variance</topic><topic>Attention</topic><topic>Basal Ganglia - blood supply</topic><topic>Basal Ganglia - physiopathology</topic><topic>Brain - blood supply</topic><topic>Brain - physiopathology</topic><topic>Cigarette smoking</topic><topic>co-twin control</topic><topic>cognitive control</topic><topic>discordant</topic><topic>Diseases in Twins</topic><topic>Female</topic><topic>fMRI</topic><topic>Functional Neuroimaging - methods</topic><topic>Humans</topic><topic>Interview, Psychological</topic><topic>Linear Models</topic><topic>Magnetic Resonance Imaging - methods</topic><topic>Oxygen - blood</topic><topic>Prospective Studies</topic><topic>Reward</topic><topic>Smoking - genetics</topic><topic>Smoking - physiopathology</topic><topic>Twins, Monozygotic</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lessov-Schlaggar, Christina N.</creatorcontrib><creatorcontrib>Lepore, Rebecca L.</creatorcontrib><creatorcontrib>Kristjansson, Sean D.</creatorcontrib><creatorcontrib>Schlaggar, Bradley L.</creatorcontrib><creatorcontrib>Barnes, Kelly Anne</creatorcontrib><creatorcontrib>Petersen, Steven E.</creatorcontrib><creatorcontrib>Madden, Pamela A. F.</creatorcontrib><creatorcontrib>Heath, Andrew C.</creatorcontrib><creatorcontrib>Barch, Deanna M.</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Immunology Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Neurosciences Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Addiction biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lessov-Schlaggar, Christina N.</au><au>Lepore, Rebecca L.</au><au>Kristjansson, Sean D.</au><au>Schlaggar, Bradley L.</au><au>Barnes, Kelly Anne</au><au>Petersen, Steven E.</au><au>Madden, Pamela A. F.</au><au>Heath, Andrew C.</au><au>Barch, Deanna M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional neuroimaging study in identical twin pairs discordant for regular cigarette smoking</atitle><jtitle>Addiction biology</jtitle><addtitle>Addict Biol</addtitle><date>2013-01</date><risdate>2013</risdate><volume>18</volume><issue>1</issue><spage>98</spage><epage>108</epage><pages>98-108</pages><issn>1355-6215</issn><eissn>1369-1600</eissn><abstract>ABSTRACT
Despite the tremendous public health and financial burden of cigarette smoking, relatively little is understood about brain mechanisms that subserve smoking behavior. This study investigated the effect of lifetime regular smoking on brain processing in a reward guessing task using functional magnetic resonance imaging and a co‐twin control study design in monozygotic (MZ) twin pairs that maximally controls for genetic and family background factors. Young adult (24–34 years) MZ female twin pairs (n = 15 pairs), discordant for regular smoking defined using Centers for Disease Control criteria as having smoked ≥100 cigarettes in their lifetime, were recruited from an ongoing genetic epidemiological longitudinal study of substance use and psychopathology. We applied hypothesis‐driven region of interest (ROI) and whole‐brain analyses to investigate the effect of regular smoking on reward processing. Reduced response to reward and punishment in regular compared with never‐regular smokers was seen in hypothesis‐driven ROI analysis of bilateral ventral striatum. Whole‐brain analysis identified bilateral reward‐processing regions that showed activation differences in response to winning or losing money but no effect of regular smoking; and frontal/parietal regions, predominantly in the right hemisphere, that showed robust effect of regular smoking but no effect of winning or losing money. Altogether, using a study design that maximally controls for group differences, we found that regular smoking had modest effects on striatal reward processing regions but robust effects on cognitive control/attentional systems.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><pmid>22340136</pmid><doi>10.1111/j.1369-1600.2012.00435.x</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Addiction Adolescent Adult Analysis of Variance Attention Basal Ganglia - blood supply Basal Ganglia - physiopathology Brain - blood supply Brain - physiopathology Cigarette smoking co-twin control cognitive control discordant Diseases in Twins Female fMRI Functional Neuroimaging - methods Humans Interview, Psychological Linear Models Magnetic Resonance Imaging - methods Oxygen - blood Prospective Studies Reward Smoking - genetics Smoking - physiopathology Twins, Monozygotic Young Adult |
title | Functional neuroimaging study in identical twin pairs discordant for regular cigarette smoking |
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