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Significance of event related causality (ERC) in eloquent neural networks
Neural activity emerges and propagates swiftly between brain areas. Investigation of these transient large-scale flows requires sophisticated statistical models. We present a method for assessing the statistical confidence of event-related neural propagation. Furthermore, we propose a criterion for...
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Published in: | Neural networks 2022-05, Vol.149, p.204-216 |
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creator | Korzeniewska, Anna Mitsuhashi, Takumi Wang, Yujing Asano, Eishi Franaszczuk, Piotr J. Crone, Nathan E. |
description | Neural activity emerges and propagates swiftly between brain areas. Investigation of these transient large-scale flows requires sophisticated statistical models. We present a method for assessing the statistical confidence of event-related neural propagation. Furthermore, we propose a criterion for statistical model selection, based on both goodness of fit and width of confidence intervals. We show that event-related causality (ERC) with two-dimensional (2D) moving average, is an efficient estimator of task-related neural propagation and that it can be used to determine how different cognitive task demands affect the strength and directionality of neural propagation across human cortical networks. Using electrodes surgically implanted on the surface of the brain for clinical testing prior to epilepsy surgery, we recorded electrocorticographic (ECoG) signals as subjects performed three naming tasks: naming of ambiguous and unambiguous visual objects, and as a contrast, naming to auditory description. ERC revealed robust and statistically significant patterns of high gamma activity propagation, consistent with models of visually and auditorily cued word production. Interestingly, ambiguous visual stimuli elicited more robust propagation from visual to auditory cortices relative to unambiguous stimuli, whereas naming to auditory description elicited propagation in the opposite direction, consistent with recruitment of modalities other than those of the stimulus during object recognition and naming. The new method introduced here is uniquely suitable to both research and clinical applications and can be used to estimate the statistical significance of neural propagation for both cognitive neuroscientific studies and functional brain mapping prior to resective surgery for epilepsy and brain tumors.
•2D moving average provides an efficient smoothing estimator for statistical testing.•The technique has broad applicability to 2D planes of large dimensions.•New criterion for statistical model selection is proposed.•Event-related causality reveals brain interactions consistent with speech models.•The method is uniquely suitable to research and clinical applications. |
doi_str_mv | 10.1016/j.neunet.2022.02.002 |
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•2D moving average provides an efficient smoothing estimator for statistical testing.•The technique has broad applicability to 2D planes of large dimensions.•New criterion for statistical model selection is proposed.•Event-related causality reveals brain interactions consistent with speech models.•The method is uniquely suitable to research and clinical applications.</description><identifier>ISSN: 0893-6080</identifier><identifier>EISSN: 1879-2782</identifier><identifier>DOI: 10.1016/j.neunet.2022.02.002</identifier><identifier>PMID: 35248810</identifier><language>eng</language><publisher>United States: Elsevier Ltd</publisher><subject>Brain ; Brain Mapping - methods ; Electroencephalography - methods ; Epilepsy - surgery ; Granger causality ; Humans ; Information flow ; Multivariate autoregressive model ; Neural networks interactions ; Neural Networks, Computer ; Short-time direct directed transfer function ; Time–frequency analysis</subject><ispartof>Neural networks, 2022-05, Vol.149, p.204-216</ispartof><rights>2022 Elsevier Ltd</rights><rights>Copyright © 2022 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c529t-ee7e7e9e42301712c00d87cd52b57f162cd8406a26d2ccb7d02c282f273eec293</citedby><cites>FETCH-LOGICAL-c529t-ee7e7e9e42301712c00d87cd52b57f162cd8406a26d2ccb7d02c282f273eec293</cites><orcidid>0000-0002-9453-7751 ; 0000-0001-9504-0678</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27923,27924</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35248810$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Korzeniewska, Anna</creatorcontrib><creatorcontrib>Mitsuhashi, Takumi</creatorcontrib><creatorcontrib>Wang, Yujing</creatorcontrib><creatorcontrib>Asano, Eishi</creatorcontrib><creatorcontrib>Franaszczuk, Piotr J.</creatorcontrib><creatorcontrib>Crone, Nathan E.</creatorcontrib><title>Significance of event related causality (ERC) in eloquent neural networks</title><title>Neural networks</title><addtitle>Neural Netw</addtitle><description>Neural activity emerges and propagates swiftly between brain areas. Investigation of these transient large-scale flows requires sophisticated statistical models. We present a method for assessing the statistical confidence of event-related neural propagation. Furthermore, we propose a criterion for statistical model selection, based on both goodness of fit and width of confidence intervals. We show that event-related causality (ERC) with two-dimensional (2D) moving average, is an efficient estimator of task-related neural propagation and that it can be used to determine how different cognitive task demands affect the strength and directionality of neural propagation across human cortical networks. Using electrodes surgically implanted on the surface of the brain for clinical testing prior to epilepsy surgery, we recorded electrocorticographic (ECoG) signals as subjects performed three naming tasks: naming of ambiguous and unambiguous visual objects, and as a contrast, naming to auditory description. ERC revealed robust and statistically significant patterns of high gamma activity propagation, consistent with models of visually and auditorily cued word production. Interestingly, ambiguous visual stimuli elicited more robust propagation from visual to auditory cortices relative to unambiguous stimuli, whereas naming to auditory description elicited propagation in the opposite direction, consistent with recruitment of modalities other than those of the stimulus during object recognition and naming. The new method introduced here is uniquely suitable to both research and clinical applications and can be used to estimate the statistical significance of neural propagation for both cognitive neuroscientific studies and functional brain mapping prior to resective surgery for epilepsy and brain tumors.
•2D moving average provides an efficient smoothing estimator for statistical testing.•The technique has broad applicability to 2D planes of large dimensions.•New criterion for statistical model selection is proposed.•Event-related causality reveals brain interactions consistent with speech models.•The method is uniquely suitable to research and clinical applications.</description><subject>Brain</subject><subject>Brain Mapping - methods</subject><subject>Electroencephalography - methods</subject><subject>Epilepsy - surgery</subject><subject>Granger causality</subject><subject>Humans</subject><subject>Information flow</subject><subject>Multivariate autoregressive model</subject><subject>Neural networks interactions</subject><subject>Neural Networks, Computer</subject><subject>Short-time direct directed transfer function</subject><subject>Time–frequency analysis</subject><issn>0893-6080</issn><issn>1879-2782</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp9UctOwzAQtBAISuEPEMoRDinrTRo7FyRUlYeEhMTjbLn2BlzSBOykiL_HVXlekFeag3dnZncYO-Aw4sCLk_moob6hboSAOIJYgBtswKUoUxQSN9kAZJmlBUjYYbshzAGgkHm2zXayMeZSchiwqzv32LjKGd0YStoqoSU1XeKp1h3ZxOg-6Np178nR9HZynLgmobp97Vc9Ud7rOkL31vrnsMe2Kl0H2v_EIXs4n95PLtPrm4urydl1asZYdimRiK-kHDPggqMBsFIYO8bZWFS8QGNlDoXGwqIxM2EBDUqsUGREBstsyE7XvC_9bEHWRCvRhnrxbqH9u2q1U39_GvekHtulKgFLATwSHH0S-NUmoVMLFwzVtW6o7YPCIiukLDHikOXrVuPbEDxV3zIc1CoFNVfrFNQqBQWxAOPY4W-L30NfZ__ZgeKhlo68CsZRTMA6T6ZTtnX_K3wANkKbng</recordid><startdate>20220501</startdate><enddate>20220501</enddate><creator>Korzeniewska, Anna</creator><creator>Mitsuhashi, Takumi</creator><creator>Wang, Yujing</creator><creator>Asano, Eishi</creator><creator>Franaszczuk, Piotr J.</creator><creator>Crone, Nathan E.</creator><general>Elsevier Ltd</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><orcidid>https://orcid.org/0000-0002-9453-7751</orcidid><orcidid>https://orcid.org/0000-0001-9504-0678</orcidid></search><sort><creationdate>20220501</creationdate><title>Significance of event related causality (ERC) in eloquent neural networks</title><author>Korzeniewska, Anna ; Mitsuhashi, Takumi ; Wang, Yujing ; Asano, Eishi ; Franaszczuk, Piotr J. ; Crone, Nathan E.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c529t-ee7e7e9e42301712c00d87cd52b57f162cd8406a26d2ccb7d02c282f273eec293</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Brain</topic><topic>Brain Mapping - methods</topic><topic>Electroencephalography - methods</topic><topic>Epilepsy - surgery</topic><topic>Granger causality</topic><topic>Humans</topic><topic>Information flow</topic><topic>Multivariate autoregressive model</topic><topic>Neural networks interactions</topic><topic>Neural Networks, Computer</topic><topic>Short-time direct directed transfer function</topic><topic>Time–frequency analysis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Korzeniewska, Anna</creatorcontrib><creatorcontrib>Mitsuhashi, Takumi</creatorcontrib><creatorcontrib>Wang, Yujing</creatorcontrib><creatorcontrib>Asano, Eishi</creatorcontrib><creatorcontrib>Franaszczuk, Piotr J.</creatorcontrib><creatorcontrib>Crone, Nathan E.</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>Neural networks</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Korzeniewska, Anna</au><au>Mitsuhashi, Takumi</au><au>Wang, Yujing</au><au>Asano, Eishi</au><au>Franaszczuk, Piotr J.</au><au>Crone, Nathan E.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Significance of event related causality (ERC) in eloquent neural networks</atitle><jtitle>Neural networks</jtitle><addtitle>Neural Netw</addtitle><date>2022-05-01</date><risdate>2022</risdate><volume>149</volume><spage>204</spage><epage>216</epage><pages>204-216</pages><issn>0893-6080</issn><eissn>1879-2782</eissn><abstract>Neural activity emerges and propagates swiftly between brain areas. Investigation of these transient large-scale flows requires sophisticated statistical models. We present a method for assessing the statistical confidence of event-related neural propagation. Furthermore, we propose a criterion for statistical model selection, based on both goodness of fit and width of confidence intervals. We show that event-related causality (ERC) with two-dimensional (2D) moving average, is an efficient estimator of task-related neural propagation and that it can be used to determine how different cognitive task demands affect the strength and directionality of neural propagation across human cortical networks. Using electrodes surgically implanted on the surface of the brain for clinical testing prior to epilepsy surgery, we recorded electrocorticographic (ECoG) signals as subjects performed three naming tasks: naming of ambiguous and unambiguous visual objects, and as a contrast, naming to auditory description. ERC revealed robust and statistically significant patterns of high gamma activity propagation, consistent with models of visually and auditorily cued word production. Interestingly, ambiguous visual stimuli elicited more robust propagation from visual to auditory cortices relative to unambiguous stimuli, whereas naming to auditory description elicited propagation in the opposite direction, consistent with recruitment of modalities other than those of the stimulus during object recognition and naming. The new method introduced here is uniquely suitable to both research and clinical applications and can be used to estimate the statistical significance of neural propagation for both cognitive neuroscientific studies and functional brain mapping prior to resective surgery for epilepsy and brain tumors.
•2D moving average provides an efficient smoothing estimator for statistical testing.•The technique has broad applicability to 2D planes of large dimensions.•New criterion for statistical model selection is proposed.•Event-related causality reveals brain interactions consistent with speech models.•The method is uniquely suitable to research and clinical applications.</abstract><cop>United States</cop><pub>Elsevier Ltd</pub><pmid>35248810</pmid><doi>10.1016/j.neunet.2022.02.002</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-9453-7751</orcidid><orcidid>https://orcid.org/0000-0001-9504-0678</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Brain Brain Mapping - methods Electroencephalography - methods Epilepsy - surgery Granger causality Humans Information flow Multivariate autoregressive model Neural networks interactions Neural Networks, Computer Short-time direct directed transfer function Time–frequency analysis |
title | Significance of event related causality (ERC) in eloquent neural networks |
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