Dissociable genetic contributions to error processing: a multimodal neuroimaging study
Neuroimaging studies reliably identify two markers of error commission: the error-related negativity (ERN), an event-related potential, and functional MRI activation of the dorsal anterior cingulate cortex (dACC). While theorized to reflect the same neural process, recent evidence suggests that the...
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| Veröffentlicht in: | PloS one 2014-07, Vol.9 (7), p.e101784-e101784 |
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| creator | Agam, Yigal Vangel, Mark Roffman, Joshua L Gallagher, Patience J Chaponis, Jonathan Haddad, Stephen Goff, Donald C Greenberg, Jennifer L Wilhelm, Sabine Smoller, Jordan W Manoach, Dara S |
| description | Neuroimaging studies reliably identify two markers of error commission: the error-related negativity (ERN), an event-related potential, and functional MRI activation of the dorsal anterior cingulate cortex (dACC). While theorized to reflect the same neural process, recent evidence suggests that the ERN arises from the posterior cingulate cortex not the dACC. Here, we tested the hypothesis that these two error markers also have different genetic mediation.
We measured both error markers in a sample of 92 comprised of healthy individuals and those with diagnoses of schizophrenia, obsessive-compulsive disorder or autism spectrum disorder. Participants performed the same task during functional MRI and simultaneously acquired magnetoencephalography and electroencephalography. We examined the mediation of the error markers by two single nucleotide polymorphisms: dopamine D4 receptor (DRD4) C-521T (rs1800955), which has been associated with the ERN and methylenetetrahydrofolate reductase (MTHFR) C677T (rs1801133), which has been associated with error-related dACC activation. We then compared the effects of each polymorphism on the two error markers modeled as a bivariate response.
We replicated our previous report of a posterior cingulate source of the ERN in healthy participants in the schizophrenia and obsessive-compulsive disorder groups. The effect of genotype on error markers did not differ significantly by diagnostic group. DRD4 C-521T allele load had a significant linear effect on ERN amplitude, but not on dACC activation, and this difference was significant. MTHFR C677T allele load had a significant linear effect on dACC activation but not ERN amplitude, but the difference in effects on the two error markers was not significant.
DRD4 C-521T, but not MTHFR C677T, had a significant differential effect on two canonical error markers. Together with the anatomical dissociation between the ERN and error-related dACC activation, these findings suggest that these error markers have different neural and genetic mediation. |
| doi_str_mv | 10.1371/journal.pone.0101784 |
| format | Article |
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We measured both error markers in a sample of 92 comprised of healthy individuals and those with diagnoses of schizophrenia, obsessive-compulsive disorder or autism spectrum disorder. Participants performed the same task during functional MRI and simultaneously acquired magnetoencephalography and electroencephalography. We examined the mediation of the error markers by two single nucleotide polymorphisms: dopamine D4 receptor (DRD4) C-521T (rs1800955), which has been associated with the ERN and methylenetetrahydrofolate reductase (MTHFR) C677T (rs1801133), which has been associated with error-related dACC activation. We then compared the effects of each polymorphism on the two error markers modeled as a bivariate response.
We replicated our previous report of a posterior cingulate source of the ERN in healthy participants in the schizophrenia and obsessive-compulsive disorder groups. The effect of genotype on error markers did not differ significantly by diagnostic group. DRD4 C-521T allele load had a significant linear effect on ERN amplitude, but not on dACC activation, and this difference was significant. MTHFR C677T allele load had a significant linear effect on dACC activation but not ERN amplitude, but the difference in effects on the two error markers was not significant.
DRD4 C-521T, but not MTHFR C677T, had a significant differential effect on two canonical error markers. Together with the anatomical dissociation between the ERN and error-related dACC activation, these findings suggest that these error markers have different neural and genetic mediation.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0101784</identifier><identifier>PMID: 25010186</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Activation ; Adult ; Alleles ; Autism ; Biology and Life Sciences ; Bivariate analysis ; Brain research ; Child Development Disorders, Pervasive - diagnosis ; Child Development Disorders, Pervasive - genetics ; Child Development Disorders, Pervasive - physiopathology ; Chromosomes ; Cortex (cingulate) ; Diagnostic systems ; Dissociation ; DNA methylation ; Dopamine ; Dopamine D4 receptors ; Dopamine receptors ; EEG ; Electroencephalography ; Error analysis ; Evoked Potentials - genetics ; Female ; Functional magnetic resonance imaging ; Genetic research ; Genetics ; Genotype ; Genotypes ; Gyrus Cinguli - physiopathology ; Humans ; Hypotheses ; Magnetic Resonance Imaging ; Magnetoencephalography ; Male ; Markers ; Measurement methods ; Mediation ; Medical imaging ; Medical schools ; Mental disorders ; Methylenetetrahydrofolate reductase ; Methylenetetrahydrofolate Reductase (NADPH2) - genetics ; Mismatch negativity ; Multimodal Imaging ; Multivariate Analysis ; Neuroimaging ; Neurology ; Neurosciences ; NMR ; Nuclear magnetic resonance ; Obsessive compulsive disorder ; Obsessive-Compulsive Disorder - diagnosis ; Obsessive-Compulsive Disorder - genetics ; Obsessive-Compulsive Disorder - physiopathology ; Polymorphism ; Polymorphism, Single Nucleotide ; Psychiatry ; Receptors, Dopamine D4 - genetics ; Saccades - genetics ; Saccades - physiology ; Schizophrenia ; Schizophrenia - diagnosis ; Schizophrenia - genetics ; Schizophrenia - physiopathology ; Single nucleotide polymorphisms ; Single-nucleotide polymorphism ; Studies</subject><ispartof>PloS one, 2014-07, Vol.9 (7), p.e101784-e101784</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Agam 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>2014 Agam et al 2014 Agam et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-bbed4916212986bd9a8a4068f7bdb7ab571a54a264071cad8f586a438be741623</citedby><cites>FETCH-LOGICAL-c758t-bbed4916212986bd9a8a4068f7bdb7ab571a54a264071cad8f586a438be741623</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/PMC4092014/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4092014/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79342,79343</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25010186$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Agam, Yigal</creatorcontrib><creatorcontrib>Vangel, Mark</creatorcontrib><creatorcontrib>Roffman, Joshua L</creatorcontrib><creatorcontrib>Gallagher, Patience J</creatorcontrib><creatorcontrib>Chaponis, Jonathan</creatorcontrib><creatorcontrib>Haddad, Stephen</creatorcontrib><creatorcontrib>Goff, Donald C</creatorcontrib><creatorcontrib>Greenberg, Jennifer L</creatorcontrib><creatorcontrib>Wilhelm, Sabine</creatorcontrib><creatorcontrib>Smoller, Jordan W</creatorcontrib><creatorcontrib>Manoach, Dara S</creatorcontrib><title>Dissociable genetic contributions to error processing: a multimodal neuroimaging study</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Neuroimaging studies reliably identify two markers of error commission: the error-related negativity (ERN), an event-related potential, and functional MRI activation of the dorsal anterior cingulate cortex (dACC). While theorized to reflect the same neural process, recent evidence suggests that the ERN arises from the posterior cingulate cortex not the dACC. Here, we tested the hypothesis that these two error markers also have different genetic mediation.
We measured both error markers in a sample of 92 comprised of healthy individuals and those with diagnoses of schizophrenia, obsessive-compulsive disorder or autism spectrum disorder. Participants performed the same task during functional MRI and simultaneously acquired magnetoencephalography and electroencephalography. We examined the mediation of the error markers by two single nucleotide polymorphisms: dopamine D4 receptor (DRD4) C-521T (rs1800955), which has been associated with the ERN and methylenetetrahydrofolate reductase (MTHFR) C677T (rs1801133), which has been associated with error-related dACC activation. We then compared the effects of each polymorphism on the two error markers modeled as a bivariate response.
We replicated our previous report of a posterior cingulate source of the ERN in healthy participants in the schizophrenia and obsessive-compulsive disorder groups. The effect of genotype on error markers did not differ significantly by diagnostic group. DRD4 C-521T allele load had a significant linear effect on ERN amplitude, but not on dACC activation, and this difference was significant. MTHFR C677T allele load had a significant linear effect on dACC activation but not ERN amplitude, but the difference in effects on the two error markers was not significant.
DRD4 C-521T, but not MTHFR C677T, had a significant differential effect on two canonical error markers. Together with the anatomical dissociation between the ERN and error-related dACC activation, these findings suggest that these error markers have different neural and genetic mediation.</description><subject>Activation</subject><subject>Adult</subject><subject>Alleles</subject><subject>Autism</subject><subject>Biology and Life Sciences</subject><subject>Bivariate analysis</subject><subject>Brain research</subject><subject>Child Development Disorders, Pervasive - diagnosis</subject><subject>Child Development Disorders, Pervasive - genetics</subject><subject>Child Development Disorders, Pervasive - physiopathology</subject><subject>Chromosomes</subject><subject>Cortex (cingulate)</subject><subject>Diagnostic systems</subject><subject>Dissociation</subject><subject>DNA methylation</subject><subject>Dopamine</subject><subject>Dopamine D4 receptors</subject><subject>Dopamine receptors</subject><subject>EEG</subject><subject>Electroencephalography</subject><subject>Error analysis</subject><subject>Evoked Potentials - genetics</subject><subject>Female</subject><subject>Functional magnetic resonance imaging</subject><subject>Genetic research</subject><subject>Genetics</subject><subject>Genotype</subject><subject>Genotypes</subject><subject>Gyrus Cinguli - physiopathology</subject><subject>Humans</subject><subject>Hypotheses</subject><subject>Magnetic Resonance Imaging</subject><subject>Magnetoencephalography</subject><subject>Male</subject><subject>Markers</subject><subject>Measurement methods</subject><subject>Mediation</subject><subject>Medical imaging</subject><subject>Medical schools</subject><subject>Mental disorders</subject><subject>Methylenetetrahydrofolate reductase</subject><subject>Methylenetetrahydrofolate Reductase (NADPH2) - genetics</subject><subject>Mismatch negativity</subject><subject>Multimodal Imaging</subject><subject>Multivariate Analysis</subject><subject>Neuroimaging</subject><subject>Neurology</subject><subject>Neurosciences</subject><subject>NMR</subject><subject>Nuclear magnetic resonance</subject><subject>Obsessive compulsive disorder</subject><subject>Obsessive-Compulsive Disorder - diagnosis</subject><subject>Obsessive-Compulsive Disorder - genetics</subject><subject>Obsessive-Compulsive Disorder - physiopathology</subject><subject>Polymorphism</subject><subject>Polymorphism, Single Nucleotide</subject><subject>Psychiatry</subject><subject>Receptors, Dopamine D4 - genetics</subject><subject>Saccades - genetics</subject><subject>Saccades - physiology</subject><subject>Schizophrenia</subject><subject>Schizophrenia - diagnosis</subject><subject>Schizophrenia - genetics</subject><subject>Schizophrenia - physiopathology</subject><subject>Single nucleotide polymorphisms</subject><subject>Single-nucleotide polymorphism</subject><subject>Studies</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNkl1r1TAYx4sobk6_gWhBEL04x6RJk9QLYcy3A4OBL7sNSfq0JyNtzpJW3Lc39XTjVHYhvUhJfs__eftn2XOM1phw_O7Kj6FXbr3zPawRRpgL-iA7xhUpVqxA5OHB_1H2JMYrhEoiGHucHRXlFCDYcXb50cbojVXaQd5CD4M1ufH9EKweB-v7mA8-hxB8yHfBG4jR9u37XOXd6Abb-Vq5vIcxeNupNj3lcRjrm6fZo0a5CM_m8yT7-fnTj7Ovq_OLL5uz0_OV4aUYVlpDTSvMClxUgum6UkJRxETDda250iXHqqSqYBRxbFQtmlIwRYnQwGkKIyfZy73uzvko55FEiUtKCecU0URs9kTt1ZXchVRmuJFeWfn3wodWqpCadiC10QIajBqWkuJGa0OrqsaFrmpeFRVKWh_mbKPuoDaQxqTcQnT50tutbP0vSVFVIDwV82YWCP56hDjIzkYDzqke_LivmxPGKUnoq3_Q-7ubqValBmzf-JTXTKLylKYFE4bQpLW-h0pfDZ1Ny4bGpvtFwNtFwGQI-D20aoxRbr5_-3_24nLJvj5gt6DcsI3e7Y22BOkeNMHHGKC5GzJGcrL_7TTkZH852z-FvThc0F3Qrd_JH2NVADk</recordid><startdate>20140710</startdate><enddate>20140710</enddate><creator>Agam, Yigal</creator><creator>Vangel, Mark</creator><creator>Roffman, Joshua L</creator><creator>Gallagher, Patience J</creator><creator>Chaponis, Jonathan</creator><creator>Haddad, Stephen</creator><creator>Goff, Donald C</creator><creator>Greenberg, Jennifer L</creator><creator>Wilhelm, Sabine</creator><creator>Smoller, Jordan W</creator><creator>Manoach, Dara S</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>IOV</scope><scope>ISR</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>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20140710</creationdate><title>Dissociable genetic contributions to error processing: a multimodal neuroimaging study</title><author>Agam, Yigal ; Vangel, Mark ; Roffman, Joshua L ; Gallagher, Patience J ; Chaponis, Jonathan ; Haddad, Stephen ; Goff, Donald C ; Greenberg, Jennifer L ; Wilhelm, Sabine ; Smoller, Jordan W ; Manoach, Dara S</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c758t-bbed4916212986bd9a8a4068f7bdb7ab571a54a264071cad8f586a438be741623</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Activation</topic><topic>Adult</topic><topic>Alleles</topic><topic>Autism</topic><topic>Biology and Life Sciences</topic><topic>Bivariate analysis</topic><topic>Brain research</topic><topic>Child Development Disorders, Pervasive - diagnosis</topic><topic>Child Development Disorders, Pervasive - genetics</topic><topic>Child Development Disorders, Pervasive - physiopathology</topic><topic>Chromosomes</topic><topic>Cortex (cingulate)</topic><topic>Diagnostic systems</topic><topic>Dissociation</topic><topic>DNA methylation</topic><topic>Dopamine</topic><topic>Dopamine D4 receptors</topic><topic>Dopamine receptors</topic><topic>EEG</topic><topic>Electroencephalography</topic><topic>Error analysis</topic><topic>Evoked Potentials - genetics</topic><topic>Female</topic><topic>Functional magnetic resonance imaging</topic><topic>Genetic research</topic><topic>Genetics</topic><topic>Genotype</topic><topic>Genotypes</topic><topic>Gyrus Cinguli - physiopathology</topic><topic>Humans</topic><topic>Hypotheses</topic><topic>Magnetic Resonance Imaging</topic><topic>Magnetoencephalography</topic><topic>Male</topic><topic>Markers</topic><topic>Measurement methods</topic><topic>Mediation</topic><topic>Medical imaging</topic><topic>Medical schools</topic><topic>Mental disorders</topic><topic>Methylenetetrahydrofolate reductase</topic><topic>Methylenetetrahydrofolate Reductase (NADPH2) - 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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>Agam, Yigal</au><au>Vangel, Mark</au><au>Roffman, Joshua L</au><au>Gallagher, Patience J</au><au>Chaponis, Jonathan</au><au>Haddad, Stephen</au><au>Goff, Donald C</au><au>Greenberg, Jennifer L</au><au>Wilhelm, Sabine</au><au>Smoller, Jordan W</au><au>Manoach, Dara S</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dissociable genetic contributions to error processing: a multimodal neuroimaging study</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-07-10</date><risdate>2014</risdate><volume>9</volume><issue>7</issue><spage>e101784</spage><epage>e101784</epage><pages>e101784-e101784</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Neuroimaging studies reliably identify two markers of error commission: the error-related negativity (ERN), an event-related potential, and functional MRI activation of the dorsal anterior cingulate cortex (dACC). While theorized to reflect the same neural process, recent evidence suggests that the ERN arises from the posterior cingulate cortex not the dACC. Here, we tested the hypothesis that these two error markers also have different genetic mediation.
We measured both error markers in a sample of 92 comprised of healthy individuals and those with diagnoses of schizophrenia, obsessive-compulsive disorder or autism spectrum disorder. Participants performed the same task during functional MRI and simultaneously acquired magnetoencephalography and electroencephalography. We examined the mediation of the error markers by two single nucleotide polymorphisms: dopamine D4 receptor (DRD4) C-521T (rs1800955), which has been associated with the ERN and methylenetetrahydrofolate reductase (MTHFR) C677T (rs1801133), which has been associated with error-related dACC activation. We then compared the effects of each polymorphism on the two error markers modeled as a bivariate response.
We replicated our previous report of a posterior cingulate source of the ERN in healthy participants in the schizophrenia and obsessive-compulsive disorder groups. The effect of genotype on error markers did not differ significantly by diagnostic group. DRD4 C-521T allele load had a significant linear effect on ERN amplitude, but not on dACC activation, and this difference was significant. MTHFR C677T allele load had a significant linear effect on dACC activation but not ERN amplitude, but the difference in effects on the two error markers was not significant.
DRD4 C-521T, but not MTHFR C677T, had a significant differential effect on two canonical error markers. Together with the anatomical dissociation between the ERN and error-related dACC activation, these findings suggest that these error markers have different neural and genetic mediation.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25010186</pmid><doi>10.1371/journal.pone.0101784</doi><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2014-07, Vol.9 (7), p.e101784-e101784 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1544377404 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Activation Adult Alleles Autism Biology and Life Sciences Bivariate analysis Brain research Child Development Disorders, Pervasive - diagnosis Child Development Disorders, Pervasive - genetics Child Development Disorders, Pervasive - physiopathology Chromosomes Cortex (cingulate) Diagnostic systems Dissociation DNA methylation Dopamine Dopamine D4 receptors Dopamine receptors EEG Electroencephalography Error analysis Evoked Potentials - genetics Female Functional magnetic resonance imaging Genetic research Genetics Genotype Genotypes Gyrus Cinguli - physiopathology Humans Hypotheses Magnetic Resonance Imaging Magnetoencephalography Male Markers Measurement methods Mediation Medical imaging Medical schools Mental disorders Methylenetetrahydrofolate reductase Methylenetetrahydrofolate Reductase (NADPH2) - genetics Mismatch negativity Multimodal Imaging Multivariate Analysis Neuroimaging Neurology Neurosciences NMR Nuclear magnetic resonance Obsessive compulsive disorder Obsessive-Compulsive Disorder - diagnosis Obsessive-Compulsive Disorder - genetics Obsessive-Compulsive Disorder - physiopathology Polymorphism Polymorphism, Single Nucleotide Psychiatry Receptors, Dopamine D4 - genetics Saccades - genetics Saccades - physiology Schizophrenia Schizophrenia - diagnosis Schizophrenia - genetics Schizophrenia - physiopathology Single nucleotide polymorphisms Single-nucleotide polymorphism Studies |
| title | Dissociable genetic contributions to error processing: a multimodal neuroimaging study |
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