Loading…

Functional and structural reorganization in brain tumors: a machine learning approach using desynchronized functional oscillations

Neuroimaging studies have allowed for non-invasive mapping of brain networks in brain tumors. Although tumor core and edema are easily identifiable using standard MRI acquisitions, imaging studies often neglect signals, structures, and functions within their presence. Therefore, both functional and...

Full description

Saved in:
Bibliographic Details
Published in:Communications biology 2024-04, Vol.7 (1), p.419-17, Article 419
Main Authors: Falcó-Roget, Joan, Cacciola, Alberto, Sambataro, Fabio, Crimi, Alessandro
Format: Article
Language:English
Subjects:
Citations: Items that this one cites
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by
cites cdi_FETCH-LOGICAL-c492t-2db2dbf84a5206d5c6742ee21768216f3fb4f1f169022456182a09f13b749bab3
container_end_page 17
container_issue 1
container_start_page 419
container_title Communications biology
container_volume 7
creator Falcó-Roget, Joan
Cacciola, Alberto
Sambataro, Fabio
Crimi, Alessandro
description Neuroimaging studies have allowed for non-invasive mapping of brain networks in brain tumors. Although tumor core and edema are easily identifiable using standard MRI acquisitions, imaging studies often neglect signals, structures, and functions within their presence. Therefore, both functional and diffusion signals, as well as their relationship with global patterns of connectivity reorganization, are poorly understood. Here, we explore the functional activity and the structure of white matter fibers considering the contribution of the whole tumor in a surgical context. First, we find intertwined alterations in the frequency domain of local and spatially distributed resting-state functional signals, potentially arising within the tumor. Second, we propose a fiber tracking pipeline capable of using anatomical information while still reconstructing bundles in tumoral and peritumoral tissue. Finally, using machine learning and healthy anatomical information, we predict structural rearrangement after surgery given the preoperative brain network. The generative model also disentangles complex patterns of connectivity reorganization for different types of tumors. Overall, we show the importance of carefully designing studies including MR signals within damaged brain tissues, as they exhibit and relate to non-trivial patterns of both structural and functional (dis-)connections or activity. A multimodal MRI study analyzes how signals within brain tumors shape the organization of brain networks and predict surgical outcomes with simple machine learning methods.
doi_str_mv 10.1038/s42003-024-06119-3
format article
fullrecord <record><control><sourceid>proquest_doaj_</sourceid><recordid>TN_cdi_doaj_primary_oai_doaj_org_article_6b373433f6384deabf87bec4bbe70c51</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><doaj_id>oai_doaj_org_article_6b373433f6384deabf87bec4bbe70c51</doaj_id><sourcerecordid>3034246891</sourcerecordid><originalsourceid>FETCH-LOGICAL-c492t-2db2dbf84a5206d5c6742ee21768216f3fb4f1f169022456182a09f13b749bab3</originalsourceid><addsrcrecordid>eNp9kk1vFCEYx4nR2GbtF_BgSLx4GcvbMODFmKa1TZp4ac8EGNhlMwMrzJjUo5-87E7tiwcTwtvz5_fAwx-A9xh9xoiK08IIQrRBhDWIYywb-gocEyrrhDPy-tn8CJyUskUIYSklp-wtOKKiFUTw7hj8uZijnUKKeoA69rBMebbTnOsyu5TXOobfeh-HIUKTde2neUy5fIEajtpuQnRwcDrHENdQ73Y51U04l_2yd-Uu2k1OFeJ66J9SpWLDMBzA5R144_VQ3MnDuAK3F-c3Z5fN9Y_vV2ffrhvLJJka0pvavGC6JYj3reUdI84R3HFBMPfUG-axx1wiQljLsSAaSY-p6Zg02tAVuFq4fdJbtcth1PlOJR3UYaM-Vuk8BTs4xQ3tKKPUcypY73RN2xlnmTGuQ7bFlfV1Ye1mM7reujjVkr2AvozEsFHr9EthJKUQklTCpwdCTj9nVyY1hmJdLUp0aS6KIsoI40Luk338R7pNc65lPKiobDGp_7oCZFHZnErJzj_eBiO1t4xaLKOqZdTBMorWQx-ev-PxyF-DVAFdBKWG4trlp9z_wd4DV8LPbg</addsrcrecordid><sourcetype>Open Website</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3033951296</pqid></control><display><type>article</type><title>Functional and structural reorganization in brain tumors: a machine learning approach using desynchronized functional oscillations</title><source>PMC (PubMed Central)</source><source>Publicly Available Content (ProQuest)</source><source>Springer Nature - nature.com Journals - Fully Open Access</source><creator>Falcó-Roget, Joan ; Cacciola, Alberto ; Sambataro, Fabio ; Crimi, Alessandro</creator><creatorcontrib>Falcó-Roget, Joan ; Cacciola, Alberto ; Sambataro, Fabio ; Crimi, Alessandro</creatorcontrib><description>Neuroimaging studies have allowed for non-invasive mapping of brain networks in brain tumors. Although tumor core and edema are easily identifiable using standard MRI acquisitions, imaging studies often neglect signals, structures, and functions within their presence. Therefore, both functional and diffusion signals, as well as their relationship with global patterns of connectivity reorganization, are poorly understood. Here, we explore the functional activity and the structure of white matter fibers considering the contribution of the whole tumor in a surgical context. First, we find intertwined alterations in the frequency domain of local and spatially distributed resting-state functional signals, potentially arising within the tumor. Second, we propose a fiber tracking pipeline capable of using anatomical information while still reconstructing bundles in tumoral and peritumoral tissue. Finally, using machine learning and healthy anatomical information, we predict structural rearrangement after surgery given the preoperative brain network. The generative model also disentangles complex patterns of connectivity reorganization for different types of tumors. Overall, we show the importance of carefully designing studies including MR signals within damaged brain tissues, as they exhibit and relate to non-trivial patterns of both structural and functional (dis-)connections or activity. A multimodal MRI study analyzes how signals within brain tumors shape the organization of brain networks and predict surgical outcomes with simple machine learning methods.</description><identifier>ISSN: 2399-3642</identifier><identifier>EISSN: 2399-3642</identifier><identifier>DOI: 10.1038/s42003-024-06119-3</identifier><identifier>PMID: 38582867</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>59 ; 59/36 ; 59/57 ; 631/378 ; 631/67/2321 ; 692/617/375/1345 ; Biomedical and Life Sciences ; Brain - diagnostic imaging ; Brain architecture ; Brain cancer ; Brain mapping ; Brain Mapping - methods ; Brain Neoplasms - diagnostic imaging ; Brain tumors ; Diffusion Tensor Imaging - methods ; Edema ; Humans ; Learning algorithms ; Life Sciences ; Machine Learning ; Magnetic resonance imaging ; Neural networks ; Neuroimaging ; Oscillations ; Structure-function relationships ; Substantia alba ; Synchronization ; Tumors</subject><ispartof>Communications biology, 2024-04, Vol.7 (1), p.419-17, Article 419</ispartof><rights>The Author(s) 2024</rights><rights>2024. The Author(s).</rights><rights>The Author(s) 2024. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c492t-2db2dbf84a5206d5c6742ee21768216f3fb4f1f169022456182a09f13b749bab3</cites><orcidid>0000-0001-5397-6363 ; 0000-0001-9412-4116 ; 0000-0002-9410-6361 ; 0000-0003-2102-416X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10998892/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/3033951296?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,25732,27903,27904,36991,36992,44569,53769,53771</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38582867$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Falcó-Roget, Joan</creatorcontrib><creatorcontrib>Cacciola, Alberto</creatorcontrib><creatorcontrib>Sambataro, Fabio</creatorcontrib><creatorcontrib>Crimi, Alessandro</creatorcontrib><title>Functional and structural reorganization in brain tumors: a machine learning approach using desynchronized functional oscillations</title><title>Communications biology</title><addtitle>Commun Biol</addtitle><addtitle>Commun Biol</addtitle><description>Neuroimaging studies have allowed for non-invasive mapping of brain networks in brain tumors. Although tumor core and edema are easily identifiable using standard MRI acquisitions, imaging studies often neglect signals, structures, and functions within their presence. Therefore, both functional and diffusion signals, as well as their relationship with global patterns of connectivity reorganization, are poorly understood. Here, we explore the functional activity and the structure of white matter fibers considering the contribution of the whole tumor in a surgical context. First, we find intertwined alterations in the frequency domain of local and spatially distributed resting-state functional signals, potentially arising within the tumor. Second, we propose a fiber tracking pipeline capable of using anatomical information while still reconstructing bundles in tumoral and peritumoral tissue. Finally, using machine learning and healthy anatomical information, we predict structural rearrangement after surgery given the preoperative brain network. The generative model also disentangles complex patterns of connectivity reorganization for different types of tumors. Overall, we show the importance of carefully designing studies including MR signals within damaged brain tissues, as they exhibit and relate to non-trivial patterns of both structural and functional (dis-)connections or activity. A multimodal MRI study analyzes how signals within brain tumors shape the organization of brain networks and predict surgical outcomes with simple machine learning methods.</description><subject>59</subject><subject>59/36</subject><subject>59/57</subject><subject>631/378</subject><subject>631/67/2321</subject><subject>692/617/375/1345</subject><subject>Biomedical and Life Sciences</subject><subject>Brain - diagnostic imaging</subject><subject>Brain architecture</subject><subject>Brain cancer</subject><subject>Brain mapping</subject><subject>Brain Mapping - methods</subject><subject>Brain Neoplasms - diagnostic imaging</subject><subject>Brain tumors</subject><subject>Diffusion Tensor Imaging - methods</subject><subject>Edema</subject><subject>Humans</subject><subject>Learning algorithms</subject><subject>Life Sciences</subject><subject>Machine Learning</subject><subject>Magnetic resonance imaging</subject><subject>Neural networks</subject><subject>Neuroimaging</subject><subject>Oscillations</subject><subject>Structure-function relationships</subject><subject>Substantia alba</subject><subject>Synchronization</subject><subject>Tumors</subject><issn>2399-3642</issn><issn>2399-3642</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNp9kk1vFCEYx4nR2GbtF_BgSLx4GcvbMODFmKa1TZp4ac8EGNhlMwMrzJjUo5-87E7tiwcTwtvz5_fAwx-A9xh9xoiK08IIQrRBhDWIYywb-gocEyrrhDPy-tn8CJyUskUIYSklp-wtOKKiFUTw7hj8uZijnUKKeoA69rBMebbTnOsyu5TXOobfeh-HIUKTde2neUy5fIEajtpuQnRwcDrHENdQ73Y51U04l_2yd-Uu2k1OFeJ66J9SpWLDMBzA5R144_VQ3MnDuAK3F-c3Z5fN9Y_vV2ffrhvLJJka0pvavGC6JYj3reUdI84R3HFBMPfUG-axx1wiQljLsSAaSY-p6Zg02tAVuFq4fdJbtcth1PlOJR3UYaM-Vuk8BTs4xQ3tKKPUcypY73RN2xlnmTGuQ7bFlfV1Ye1mM7reujjVkr2AvozEsFHr9EthJKUQklTCpwdCTj9nVyY1hmJdLUp0aS6KIsoI40Luk338R7pNc65lPKiobDGp_7oCZFHZnErJzj_eBiO1t4xaLKOqZdTBMorWQx-ev-PxyF-DVAFdBKWG4trlp9z_wd4DV8LPbg</recordid><startdate>20240406</startdate><enddate>20240406</enddate><creator>Falcó-Roget, Joan</creator><creator>Cacciola, Alberto</creator><creator>Sambataro, Fabio</creator><creator>Crimi, Alessandro</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><general>Nature Portfolio</general><scope>C6C</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>3V.</scope><scope>7XB</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>LK8</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-5397-6363</orcidid><orcidid>https://orcid.org/0000-0001-9412-4116</orcidid><orcidid>https://orcid.org/0000-0002-9410-6361</orcidid><orcidid>https://orcid.org/0000-0003-2102-416X</orcidid></search><sort><creationdate>20240406</creationdate><title>Functional and structural reorganization in brain tumors: a machine learning approach using desynchronized functional oscillations</title><author>Falcó-Roget, Joan ; Cacciola, Alberto ; Sambataro, Fabio ; Crimi, Alessandro</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c492t-2db2dbf84a5206d5c6742ee21768216f3fb4f1f169022456182a09f13b749bab3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>59</topic><topic>59/36</topic><topic>59/57</topic><topic>631/378</topic><topic>631/67/2321</topic><topic>692/617/375/1345</topic><topic>Biomedical and Life Sciences</topic><topic>Brain - diagnostic imaging</topic><topic>Brain architecture</topic><topic>Brain cancer</topic><topic>Brain mapping</topic><topic>Brain Mapping - methods</topic><topic>Brain Neoplasms - diagnostic imaging</topic><topic>Brain tumors</topic><topic>Diffusion Tensor Imaging - methods</topic><topic>Edema</topic><topic>Humans</topic><topic>Learning algorithms</topic><topic>Life Sciences</topic><topic>Machine Learning</topic><topic>Magnetic resonance imaging</topic><topic>Neural networks</topic><topic>Neuroimaging</topic><topic>Oscillations</topic><topic>Structure-function relationships</topic><topic>Substantia alba</topic><topic>Synchronization</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Falcó-Roget, Joan</creatorcontrib><creatorcontrib>Cacciola, Alberto</creatorcontrib><creatorcontrib>Sambataro, Fabio</creatorcontrib><creatorcontrib>Crimi, Alessandro</creatorcontrib><collection>Springer Open Access</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>ProQuest Central (purchase pre-March 2016)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>Biological Sciences</collection><collection>Science Database</collection><collection>Biological Science Database</collection><collection>Publicly Available Content (ProQuest)</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 Basic</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Communications biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Falcó-Roget, Joan</au><au>Cacciola, Alberto</au><au>Sambataro, Fabio</au><au>Crimi, Alessandro</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Functional and structural reorganization in brain tumors: a machine learning approach using desynchronized functional oscillations</atitle><jtitle>Communications biology</jtitle><stitle>Commun Biol</stitle><addtitle>Commun Biol</addtitle><date>2024-04-06</date><risdate>2024</risdate><volume>7</volume><issue>1</issue><spage>419</spage><epage>17</epage><pages>419-17</pages><artnum>419</artnum><issn>2399-3642</issn><eissn>2399-3642</eissn><abstract>Neuroimaging studies have allowed for non-invasive mapping of brain networks in brain tumors. Although tumor core and edema are easily identifiable using standard MRI acquisitions, imaging studies often neglect signals, structures, and functions within their presence. Therefore, both functional and diffusion signals, as well as their relationship with global patterns of connectivity reorganization, are poorly understood. Here, we explore the functional activity and the structure of white matter fibers considering the contribution of the whole tumor in a surgical context. First, we find intertwined alterations in the frequency domain of local and spatially distributed resting-state functional signals, potentially arising within the tumor. Second, we propose a fiber tracking pipeline capable of using anatomical information while still reconstructing bundles in tumoral and peritumoral tissue. Finally, using machine learning and healthy anatomical information, we predict structural rearrangement after surgery given the preoperative brain network. The generative model also disentangles complex patterns of connectivity reorganization for different types of tumors. Overall, we show the importance of carefully designing studies including MR signals within damaged brain tissues, as they exhibit and relate to non-trivial patterns of both structural and functional (dis-)connections or activity. A multimodal MRI study analyzes how signals within brain tumors shape the organization of brain networks and predict surgical outcomes with simple machine learning methods.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>38582867</pmid><doi>10.1038/s42003-024-06119-3</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0001-5397-6363</orcidid><orcidid>https://orcid.org/0000-0001-9412-4116</orcidid><orcidid>https://orcid.org/0000-0002-9410-6361</orcidid><orcidid>https://orcid.org/0000-0003-2102-416X</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 2399-3642
ispartof Communications biology, 2024-04, Vol.7 (1), p.419-17, Article 419
issn 2399-3642
2399-3642
language eng
recordid cdi_doaj_primary_oai_doaj_org_article_6b373433f6384deabf87bec4bbe70c51
source PMC (PubMed Central); Publicly Available Content (ProQuest); Springer Nature - nature.com Journals - Fully Open Access
subjects 59
59/36
59/57
631/378
631/67/2321
692/617/375/1345
Biomedical and Life Sciences
Brain - diagnostic imaging
Brain architecture
Brain cancer
Brain mapping
Brain Mapping - methods
Brain Neoplasms - diagnostic imaging
Brain tumors
Diffusion Tensor Imaging - methods
Edema
Humans
Learning algorithms
Life Sciences
Machine Learning
Magnetic resonance imaging
Neural networks
Neuroimaging
Oscillations
Structure-function relationships
Substantia alba
Synchronization
Tumors
title Functional and structural reorganization in brain tumors: a machine learning approach using desynchronized functional oscillations
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-26T02%3A45%3A12IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_doaj_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Functional%20and%20structural%20reorganization%20in%20brain%20tumors:%20a%20machine%20learning%20approach%20using%20desynchronized%20functional%20oscillations&rft.jtitle=Communications%20biology&rft.au=Falc%C3%B3-Roget,%20Joan&rft.date=2024-04-06&rft.volume=7&rft.issue=1&rft.spage=419&rft.epage=17&rft.pages=419-17&rft.artnum=419&rft.issn=2399-3642&rft.eissn=2399-3642&rft_id=info:doi/10.1038/s42003-024-06119-3&rft_dat=%3Cproquest_doaj_%3E3034246891%3C/proquest_doaj_%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c492t-2db2dbf84a5206d5c6742ee21768216f3fb4f1f169022456182a09f13b749bab3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=3033951296&rft_id=info:pmid/38582867&rfr_iscdi=true