Opposing Changes in the Functional Architecture of Large-Scale Networks in Bipolar Mania and Depression

Abstract Objective Manic and depressive phases of bipolar disorder (BD) show opposite symptoms in psychomotor, thought, and affective dimensions. Neuronally, these may depend on distinct patterns of alterations in the functional architecture of brain intrinsic activity. Therefore, the study aimed to...

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Veröffentlicht in:Schizophrenia bulletin 2020-07, Vol.46 (4), p.971-980
Hauptverfasser: Russo, Daniel, Martino, Matteo, Magioncalda, Paola, Inglese, Matilde, Amore, Mario, Northoff, Georg
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container_end_page 980
container_issue 4
container_start_page 971
container_title Schizophrenia bulletin
container_volume 46
creator Russo, Daniel
Martino, Matteo
Magioncalda, Paola
Inglese, Matilde
Amore, Mario
Northoff, Georg
description Abstract Objective Manic and depressive phases of bipolar disorder (BD) show opposite symptoms in psychomotor, thought, and affective dimensions. Neuronally, these may depend on distinct patterns of alterations in the functional architecture of brain intrinsic activity. Therefore, the study aimed to characterize the spatial and temporal changes of resting-state activity in mania and depression, by investigating the regional homogeneity (ReHo) and degree of centrality (DC), in different frequency bands. Methods Using resting-state functional magnetic resonance imaging (fMRI), voxel-wise ReHo and DC were calculated—in the standard frequency band (SFB: 0.01–0.10 Hz), as well as in Slow5 (0.01–0.027 Hz) and Slow4 (0.027–0.073 Hz)—and compared between manic (n = 36), depressed (n = 43), euthymic (n = 29) patients, and healthy controls (n = 112). Finally, clinical correlations were investigated. Results Mania was mainly characterized by decreased ReHo and DC in Slow4 in the medial prefrontal cortex (as part of the default-mode network [DMN]), which in turn correlated with manic symptomatology. Conversely, depression was mainly characterized by decreased ReHo in SFB in the primary sensory-motor cortex (as part of the sensorimotor network [SMN]), which in turn correlated with depressive symptomatology. Conclusions Our data show a functional reconfiguration of the spatiotemporal structure of intrinsic brain activity to occur in BD. Mania might be characterized by a predominance of sensorimotor over associative networks, possibly driven by a deficit of the DMN (reflecting in internal thought deficit). Conversely, depression might be characterized by a predominance of associative over sensorimotor networks, possibly driven by a deficit of the SMN (reflecting in psychomotor inhibition).
doi_str_mv 10.1093/schbul/sbaa004
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Neuronally, these may depend on distinct patterns of alterations in the functional architecture of brain intrinsic activity. Therefore, the study aimed to characterize the spatial and temporal changes of resting-state activity in mania and depression, by investigating the regional homogeneity (ReHo) and degree of centrality (DC), in different frequency bands. Methods Using resting-state functional magnetic resonance imaging (fMRI), voxel-wise ReHo and DC were calculated—in the standard frequency band (SFB: 0.01–0.10 Hz), as well as in Slow5 (0.01–0.027 Hz) and Slow4 (0.027–0.073 Hz)—and compared between manic (n = 36), depressed (n = 43), euthymic (n = 29) patients, and healthy controls (n = 112). Finally, clinical correlations were investigated. Results Mania was mainly characterized by decreased ReHo and DC in Slow4 in the medial prefrontal cortex (as part of the default-mode network [DMN]), which in turn correlated with manic symptomatology. Conversely, depression was mainly characterized by decreased ReHo in SFB in the primary sensory-motor cortex (as part of the sensorimotor network [SMN]), which in turn correlated with depressive symptomatology. Conclusions Our data show a functional reconfiguration of the spatiotemporal structure of intrinsic brain activity to occur in BD. Mania might be characterized by a predominance of sensorimotor over associative networks, possibly driven by a deficit of the DMN (reflecting in internal thought deficit). Conversely, depression might be characterized by a predominance of associative over sensorimotor networks, possibly driven by a deficit of the SMN (reflecting in psychomotor inhibition).</description><identifier>ISSN: 0586-7614</identifier><identifier>EISSN: 1745-1701</identifier><identifier>DOI: 10.1093/schbul/sbaa004</identifier><identifier>PMID: 32047938</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Adult ; Bipolar Disorder - complications ; Bipolar Disorder - diagnostic imaging ; Bipolar Disorder - physiopathology ; Connectome ; Default Mode Network - diagnostic imaging ; Default Mode Network - physiopathology ; Depression - diagnostic imaging ; Depression - etiology ; Depression - physiopathology ; Humans ; Magnetic Resonance Imaging ; Mania - diagnostic imaging ; Mania - etiology ; Mania - physiopathology ; Nerve Net - diagnostic imaging ; Nerve Net - physiopathology ; Prefrontal Cortex - diagnostic imaging ; Prefrontal Cortex - physiopathology ; Regular ; Sensorimotor Cortex - diagnostic imaging ; Sensorimotor Cortex - physiopathology</subject><ispartof>Schizophrenia bulletin, 2020-07, Vol.46 (4), p.971-980</ispartof><rights>The Author(s) 2020. Published by Oxford University Press on behalf of the Maryland Psychiatric Research Center. All rights reserved. For permissions, please email: journals.permissions@oup.com 2020</rights><rights>The Author(s) 2020. Published by Oxford University Press on behalf of the Maryland Psychiatric Research Center. All rights reserved. For permissions, please email: journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c424t-2b8c1d73385c775b62699844023968567dcabc5f14cafcc0f2aa9289105691133</citedby><cites>FETCH-LOGICAL-c424t-2b8c1d73385c775b62699844023968567dcabc5f14cafcc0f2aa9289105691133</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/PMC7342167/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7342167/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,1584,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32047938$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Russo, Daniel</creatorcontrib><creatorcontrib>Martino, Matteo</creatorcontrib><creatorcontrib>Magioncalda, Paola</creatorcontrib><creatorcontrib>Inglese, Matilde</creatorcontrib><creatorcontrib>Amore, Mario</creatorcontrib><creatorcontrib>Northoff, Georg</creatorcontrib><title>Opposing Changes in the Functional Architecture of Large-Scale Networks in Bipolar Mania and Depression</title><title>Schizophrenia bulletin</title><addtitle>Schizophr Bull</addtitle><description>Abstract Objective Manic and depressive phases of bipolar disorder (BD) show opposite symptoms in psychomotor, thought, and affective dimensions. Neuronally, these may depend on distinct patterns of alterations in the functional architecture of brain intrinsic activity. Therefore, the study aimed to characterize the spatial and temporal changes of resting-state activity in mania and depression, by investigating the regional homogeneity (ReHo) and degree of centrality (DC), in different frequency bands. Methods Using resting-state functional magnetic resonance imaging (fMRI), voxel-wise ReHo and DC were calculated—in the standard frequency band (SFB: 0.01–0.10 Hz), as well as in Slow5 (0.01–0.027 Hz) and Slow4 (0.027–0.073 Hz)—and compared between manic (n = 36), depressed (n = 43), euthymic (n = 29) patients, and healthy controls (n = 112). Finally, clinical correlations were investigated. Results Mania was mainly characterized by decreased ReHo and DC in Slow4 in the medial prefrontal cortex (as part of the default-mode network [DMN]), which in turn correlated with manic symptomatology. Conversely, depression was mainly characterized by decreased ReHo in SFB in the primary sensory-motor cortex (as part of the sensorimotor network [SMN]), which in turn correlated with depressive symptomatology. Conclusions Our data show a functional reconfiguration of the spatiotemporal structure of intrinsic brain activity to occur in BD. Mania might be characterized by a predominance of sensorimotor over associative networks, possibly driven by a deficit of the DMN (reflecting in internal thought deficit). Conversely, depression might be characterized by a predominance of associative over sensorimotor networks, possibly driven by a deficit of the SMN (reflecting in psychomotor inhibition).</description><subject>Adult</subject><subject>Bipolar Disorder - complications</subject><subject>Bipolar Disorder - diagnostic imaging</subject><subject>Bipolar Disorder - physiopathology</subject><subject>Connectome</subject><subject>Default Mode Network - diagnostic imaging</subject><subject>Default Mode Network - physiopathology</subject><subject>Depression - diagnostic imaging</subject><subject>Depression - etiology</subject><subject>Depression - physiopathology</subject><subject>Humans</subject><subject>Magnetic Resonance Imaging</subject><subject>Mania - diagnostic imaging</subject><subject>Mania - etiology</subject><subject>Mania - physiopathology</subject><subject>Nerve Net - diagnostic imaging</subject><subject>Nerve Net - physiopathology</subject><subject>Prefrontal Cortex - diagnostic imaging</subject><subject>Prefrontal Cortex - physiopathology</subject><subject>Regular</subject><subject>Sensorimotor Cortex - diagnostic imaging</subject><subject>Sensorimotor Cortex - physiopathology</subject><issn>0586-7614</issn><issn>1745-1701</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkU1v1DAQhi0Eokvh2mPlIxzS-tvxpVJZKCBt6QE4WxOvk7jN2sFOQPx7UnapyonTHOZ5nxnpReiEkjNKDD8vrm_m4bw0AISIJ2hFtZAV1YQ-RSsia1VpRcURelHKLSFUGMWeoyPOiNCG1yvU3YxjKiF2eN1D7HzBIeKp9_hqjm4KKcKAL7Prw-TdNGePU4s3kDtffXEwePzZTz9TvvsTexvGNEDG1xADYIhb_M6P2ZeyaF6iZy0Mxb86zGP07er91_XHanPz4dP6clM5wcRUsaZ2dKs5r6XTWjaKKWNqIQjjRtVS6a2DxsmWCgetc6RlAIbVhhKpDKWcH6OLvXecm53fOh-nDIMdc9hB_mUTBPvvJobedumH1VwwqvQieH0Q5PR99mWyu1CcHwaIPs3FMi4FlUQLtaBne9TlVEr27cMZSux9O3bfjj20swROHz_3gP-tYwHe7IE0j_-T_QYan5yq</recordid><startdate>20200708</startdate><enddate>20200708</enddate><creator>Russo, Daniel</creator><creator>Martino, Matteo</creator><creator>Magioncalda, Paola</creator><creator>Inglese, Matilde</creator><creator>Amore, Mario</creator><creator>Northoff, Georg</creator><general>Oxford University Press</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>5PM</scope></search><sort><creationdate>20200708</creationdate><title>Opposing Changes in the Functional Architecture of Large-Scale Networks in Bipolar Mania and Depression</title><author>Russo, Daniel ; Martino, Matteo ; Magioncalda, Paola ; Inglese, Matilde ; Amore, Mario ; Northoff, Georg</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c424t-2b8c1d73385c775b62699844023968567dcabc5f14cafcc0f2aa9289105691133</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Adult</topic><topic>Bipolar Disorder - complications</topic><topic>Bipolar Disorder - diagnostic imaging</topic><topic>Bipolar Disorder - physiopathology</topic><topic>Connectome</topic><topic>Default Mode Network - diagnostic imaging</topic><topic>Default Mode Network - physiopathology</topic><topic>Depression - diagnostic imaging</topic><topic>Depression - etiology</topic><topic>Depression - physiopathology</topic><topic>Humans</topic><topic>Magnetic Resonance Imaging</topic><topic>Mania - diagnostic imaging</topic><topic>Mania - etiology</topic><topic>Mania - physiopathology</topic><topic>Nerve Net - diagnostic imaging</topic><topic>Nerve Net - physiopathology</topic><topic>Prefrontal Cortex - diagnostic imaging</topic><topic>Prefrontal Cortex - physiopathology</topic><topic>Regular</topic><topic>Sensorimotor Cortex - diagnostic imaging</topic><topic>Sensorimotor Cortex - physiopathology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Russo, Daniel</creatorcontrib><creatorcontrib>Martino, Matteo</creatorcontrib><creatorcontrib>Magioncalda, Paola</creatorcontrib><creatorcontrib>Inglese, Matilde</creatorcontrib><creatorcontrib>Amore, Mario</creatorcontrib><creatorcontrib>Northoff, Georg</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>PubMed Central (Full Participant titles)</collection><jtitle>Schizophrenia bulletin</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Russo, Daniel</au><au>Martino, Matteo</au><au>Magioncalda, Paola</au><au>Inglese, Matilde</au><au>Amore, Mario</au><au>Northoff, Georg</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Opposing Changes in the Functional Architecture of Large-Scale Networks in Bipolar Mania and Depression</atitle><jtitle>Schizophrenia bulletin</jtitle><addtitle>Schizophr Bull</addtitle><date>2020-07-08</date><risdate>2020</risdate><volume>46</volume><issue>4</issue><spage>971</spage><epage>980</epage><pages>971-980</pages><issn>0586-7614</issn><eissn>1745-1701</eissn><abstract>Abstract Objective Manic and depressive phases of bipolar disorder (BD) show opposite symptoms in psychomotor, thought, and affective dimensions. Neuronally, these may depend on distinct patterns of alterations in the functional architecture of brain intrinsic activity. Therefore, the study aimed to characterize the spatial and temporal changes of resting-state activity in mania and depression, by investigating the regional homogeneity (ReHo) and degree of centrality (DC), in different frequency bands. Methods Using resting-state functional magnetic resonance imaging (fMRI), voxel-wise ReHo and DC were calculated—in the standard frequency band (SFB: 0.01–0.10 Hz), as well as in Slow5 (0.01–0.027 Hz) and Slow4 (0.027–0.073 Hz)—and compared between manic (n = 36), depressed (n = 43), euthymic (n = 29) patients, and healthy controls (n = 112). Finally, clinical correlations were investigated. Results Mania was mainly characterized by decreased ReHo and DC in Slow4 in the medial prefrontal cortex (as part of the default-mode network [DMN]), which in turn correlated with manic symptomatology. Conversely, depression was mainly characterized by decreased ReHo in SFB in the primary sensory-motor cortex (as part of the sensorimotor network [SMN]), which in turn correlated with depressive symptomatology. Conclusions Our data show a functional reconfiguration of the spatiotemporal structure of intrinsic brain activity to occur in BD. Mania might be characterized by a predominance of sensorimotor over associative networks, possibly driven by a deficit of the DMN (reflecting in internal thought deficit). Conversely, depression might be characterized by a predominance of associative over sensorimotor networks, possibly driven by a deficit of the SMN (reflecting in psychomotor inhibition).</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>32047938</pmid><doi>10.1093/schbul/sbaa004</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record>
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subjects Adult
Bipolar Disorder - complications
Bipolar Disorder - diagnostic imaging
Bipolar Disorder - physiopathology
Connectome
Default Mode Network - diagnostic imaging
Default Mode Network - physiopathology
Depression - diagnostic imaging
Depression - etiology
Depression - physiopathology
Humans
Magnetic Resonance Imaging
Mania - diagnostic imaging
Mania - etiology
Mania - physiopathology
Nerve Net - diagnostic imaging
Nerve Net - physiopathology
Prefrontal Cortex - diagnostic imaging
Prefrontal Cortex - physiopathology
Regular
Sensorimotor Cortex - diagnostic imaging
Sensorimotor Cortex - physiopathology
title Opposing Changes in the Functional Architecture of Large-Scale Networks in Bipolar Mania and Depression
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