Mechanical stiffness and anisotropy measured by MRE during brain development in the minipig
•Anisotropic mechanical properties in the brain are investigated by MR elastography.•Longitudinal changes in brain properties are assessed during brain development.•Multi-excitation wave fields and fiber directions from DTI enable anisotropic MRE. The relationship between brain development and mecha...
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creator | Wang, Shuaihu Guertler, Charlotte A. Okamoto, Ruth J. Johnson, Curtis L. McGarry, Matthew D.J. Bayly, Philip V. |
description | •Anisotropic mechanical properties in the brain are investigated by MR elastography.•Longitudinal changes in brain properties are assessed during brain development.•Multi-excitation wave fields and fiber directions from DTI enable anisotropic MRE.
The relationship between brain development and mechanical properties of brain tissue is important, but remains incompletely understood, in part due to the challenges in measuring these properties longitudinally over time. In addition, white matter, which is composed of aligned, myelinated, axonal fibers, may be mechanically anisotropic. Here we use data from magnetic resonance elastography (MRE) and diffusion tensor imaging (DTI) to estimate anisotropic mechanical properties in six female Yucatan minipigs at ages from 3 to 6 months. Fiber direction was estimated from the principal axis of the diffusion tensor in each voxel. Harmonic shear waves in the brain were excited by three different configurations of a jaw actuator and measured using a motion-sensitive MR imaging sequence. Anisotropic mechanical properties are estimated from displacement field and fiber direction data with a finite element- based, transversely-isotropic nonlinear inversion (TI-NLI) algorithm. TI-NLI finds spatially resolved TI material properties that minimize the error between measured and simulated displacement fields. Maps of anisotropic mechanical properties in the minipig brain were generated for each animal at all four ages. These maps show that white matter is more dissipative and anisotropic than gray matter, and reveal significant effects of brain development on brain stiffness and structural anisotropy. Changes in brain mechanical properties may be a fundamental biophysical signature of brain development. |
doi_str_mv | 10.1016/j.neuroimage.2023.120234 |
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The relationship between brain development and mechanical properties of brain tissue is important, but remains incompletely understood, in part due to the challenges in measuring these properties longitudinally over time. In addition, white matter, which is composed of aligned, myelinated, axonal fibers, may be mechanically anisotropic. Here we use data from magnetic resonance elastography (MRE) and diffusion tensor imaging (DTI) to estimate anisotropic mechanical properties in six female Yucatan minipigs at ages from 3 to 6 months. Fiber direction was estimated from the principal axis of the diffusion tensor in each voxel. Harmonic shear waves in the brain were excited by three different configurations of a jaw actuator and measured using a motion-sensitive MR imaging sequence. Anisotropic mechanical properties are estimated from displacement field and fiber direction data with a finite element- based, transversely-isotropic nonlinear inversion (TI-NLI) algorithm. TI-NLI finds spatially resolved TI material properties that minimize the error between measured and simulated displacement fields. Maps of anisotropic mechanical properties in the minipig brain were generated for each animal at all four ages. These maps show that white matter is more dissipative and anisotropic than gray matter, and reveal significant effects of brain development on brain stiffness and structural anisotropy. Changes in brain mechanical properties may be a fundamental biophysical signature of brain development.</description><identifier>ISSN: 1053-8119</identifier><identifier>EISSN: 1095-9572</identifier><identifier>DOI: 10.1016/j.neuroimage.2023.120234</identifier><identifier>PMID: 37369255</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Anisotropy ; Brain ; Brain - diagnostic imaging ; Brain development ; Brain mapping ; Child development ; Cognition & reasoning ; Diffusion Tensor Imaging ; Elasticity Imaging Techniques - methods ; Estimates ; Female ; Jaw ; Longitudinal studies ; Magnetic resonance elastography ; Magnetic resonance imaging ; Mechanical properties ; Motion detection ; Neuroimaging ; Stiffness ; Substantia alba ; Substantia grisea ; Swine ; Swine, Miniature ; Viscoelasticity</subject><ispartof>NeuroImage (Orlando, Fla.), 2023-08, Vol.277, p.120234-120234, Article 120234</ispartof><rights>2023 The Author(s)</rights><rights>Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved.</rights><rights>2023. The Author(s)</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c508t-9e561176b85144e3d665a2bceaf42deafe74afa5b1ee452792f49878857a1e193</citedby><cites>FETCH-LOGICAL-c508t-9e561176b85144e3d665a2bceaf42deafe74afa5b1ee452792f49878857a1e193</cites><orcidid>0000-0003-4303-0704 ; 0000-0002-3085-3878 ; 0000-0001-6993-3501 ; 0000-0002-7760-131X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1053811923003853$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,860,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37369255$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Shuaihu</creatorcontrib><creatorcontrib>Guertler, Charlotte A.</creatorcontrib><creatorcontrib>Okamoto, Ruth J.</creatorcontrib><creatorcontrib>Johnson, Curtis L.</creatorcontrib><creatorcontrib>McGarry, Matthew D.J.</creatorcontrib><creatorcontrib>Bayly, Philip V.</creatorcontrib><title>Mechanical stiffness and anisotropy measured by MRE during brain development in the minipig</title><title>NeuroImage (Orlando, Fla.)</title><addtitle>Neuroimage</addtitle><description>•Anisotropic mechanical properties in the brain are investigated by MR elastography.•Longitudinal changes in brain properties are assessed during brain development.•Multi-excitation wave fields and fiber directions from DTI enable anisotropic MRE.
The relationship between brain development and mechanical properties of brain tissue is important, but remains incompletely understood, in part due to the challenges in measuring these properties longitudinally over time. In addition, white matter, which is composed of aligned, myelinated, axonal fibers, may be mechanically anisotropic. Here we use data from magnetic resonance elastography (MRE) and diffusion tensor imaging (DTI) to estimate anisotropic mechanical properties in six female Yucatan minipigs at ages from 3 to 6 months. Fiber direction was estimated from the principal axis of the diffusion tensor in each voxel. Harmonic shear waves in the brain were excited by three different configurations of a jaw actuator and measured using a motion-sensitive MR imaging sequence. Anisotropic mechanical properties are estimated from displacement field and fiber direction data with a finite element- based, transversely-isotropic nonlinear inversion (TI-NLI) algorithm. TI-NLI finds spatially resolved TI material properties that minimize the error between measured and simulated displacement fields. Maps of anisotropic mechanical properties in the minipig brain were generated for each animal at all four ages. These maps show that white matter is more dissipative and anisotropic than gray matter, and reveal significant effects of brain development on brain stiffness and structural anisotropy. Changes in brain mechanical properties may be a fundamental biophysical signature of brain development.</description><subject>Animals</subject><subject>Anisotropy</subject><subject>Brain</subject><subject>Brain - diagnostic imaging</subject><subject>Brain development</subject><subject>Brain mapping</subject><subject>Child development</subject><subject>Cognition & reasoning</subject><subject>Diffusion Tensor Imaging</subject><subject>Elasticity Imaging Techniques - methods</subject><subject>Estimates</subject><subject>Female</subject><subject>Jaw</subject><subject>Longitudinal studies</subject><subject>Magnetic resonance elastography</subject><subject>Magnetic resonance imaging</subject><subject>Mechanical properties</subject><subject>Motion detection</subject><subject>Neuroimaging</subject><subject>Stiffness</subject><subject>Substantia alba</subject><subject>Substantia grisea</subject><subject>Swine</subject><subject>Swine, Miniature</subject><subject>Viscoelasticity</subject><issn>1053-8119</issn><issn>1095-9572</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNqFUU1v1DAQtRCIlsJfQJa4cMnijzi2TwiqllZqhYTgxMFynMmuV4kd7GSl_fc42lI-Lhw8Hstv3sy8hxCmZEMJbd7tNwGWFP1ot7BhhPENXWP9BJ1TokWlhWRP11zwSlGqz9CLnPeEEE1r9RydcckbzYQ4R9_vwe1s8M4OOM--7wPkjG3oyvE5zilORzyCzUuCDrdHfP_lCndL8mGL22R9wB0cYIjTCGHG5TnvAI8--MlvX6JnvR0yvHq4L9C366uvlzfV3edPt5cf7ioniJorDaKhVDatErSugXdNIyxrHdi-Zl2JIGvbW9FSgFowqVlfayWVEtJSoJpfoPcn3mlpR-hcmSTZwUyp6JOOJlpv_v4Jfme28WAoJUUd3hSGtw8MKf5YIM9m9NnBMNgAccmGKU4ayRqyNnvzD3QflxTKfitKSy4VFwWlTiiXYs4J-sdpKDGrhWZvfltoVvPMycJS-vrPbR4Lf3lWAB9PACiaHjwkk52H4KDzCdxsuuj_3-Un4_-zcQ</recordid><startdate>20230815</startdate><enddate>20230815</enddate><creator>Wang, Shuaihu</creator><creator>Guertler, Charlotte A.</creator><creator>Okamoto, Ruth J.</creator><creator>Johnson, Curtis L.</creator><creator>McGarry, Matthew D.J.</creator><creator>Bayly, Philip V.</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><scope>6I.</scope><scope>AAFTH</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>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</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>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4303-0704</orcidid><orcidid>https://orcid.org/0000-0002-3085-3878</orcidid><orcidid>https://orcid.org/0000-0001-6993-3501</orcidid><orcidid>https://orcid.org/0000-0002-7760-131X</orcidid></search><sort><creationdate>20230815</creationdate><title>Mechanical stiffness and anisotropy measured by MRE during brain development in the minipig</title><author>Wang, Shuaihu ; Guertler, Charlotte A. ; Okamoto, Ruth J. ; Johnson, Curtis L. ; McGarry, Matthew D.J. ; Bayly, Philip V.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c508t-9e561176b85144e3d665a2bceaf42deafe74afa5b1ee452792f49878857a1e193</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Animals</topic><topic>Anisotropy</topic><topic>Brain</topic><topic>Brain - diagnostic imaging</topic><topic>Brain development</topic><topic>Brain mapping</topic><topic>Child development</topic><topic>Cognition & reasoning</topic><topic>Diffusion Tensor Imaging</topic><topic>Elasticity Imaging Techniques - methods</topic><topic>Estimates</topic><topic>Female</topic><topic>Jaw</topic><topic>Longitudinal studies</topic><topic>Magnetic resonance elastography</topic><topic>Magnetic resonance imaging</topic><topic>Mechanical properties</topic><topic>Motion detection</topic><topic>Neuroimaging</topic><topic>Stiffness</topic><topic>Substantia alba</topic><topic>Substantia grisea</topic><topic>Swine</topic><topic>Swine, Miniature</topic><topic>Viscoelasticity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Shuaihu</creatorcontrib><creatorcontrib>Guertler, Charlotte A.</creatorcontrib><creatorcontrib>Okamoto, Ruth J.</creatorcontrib><creatorcontrib>Johnson, Curtis L.</creatorcontrib><creatorcontrib>McGarry, Matthew D.J.</creatorcontrib><creatorcontrib>Bayly, Philip V.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect: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>Neurosciences Abstracts</collection><collection>ProQuest Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central UK/Ireland</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>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>PML(ProQuest Medical Library)</collection><collection>Psychology Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</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 One Psychology</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>NeuroImage (Orlando, Fla.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Shuaihu</au><au>Guertler, Charlotte A.</au><au>Okamoto, Ruth J.</au><au>Johnson, Curtis L.</au><au>McGarry, Matthew D.J.</au><au>Bayly, Philip V.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mechanical stiffness and anisotropy measured by MRE during brain development in the minipig</atitle><jtitle>NeuroImage (Orlando, Fla.)</jtitle><addtitle>Neuroimage</addtitle><date>2023-08-15</date><risdate>2023</risdate><volume>277</volume><spage>120234</spage><epage>120234</epage><pages>120234-120234</pages><artnum>120234</artnum><issn>1053-8119</issn><eissn>1095-9572</eissn><abstract>•Anisotropic mechanical properties in the brain are investigated by MR elastography.•Longitudinal changes in brain properties are assessed during brain development.•Multi-excitation wave fields and fiber directions from DTI enable anisotropic MRE.
The relationship between brain development and mechanical properties of brain tissue is important, but remains incompletely understood, in part due to the challenges in measuring these properties longitudinally over time. In addition, white matter, which is composed of aligned, myelinated, axonal fibers, may be mechanically anisotropic. Here we use data from magnetic resonance elastography (MRE) and diffusion tensor imaging (DTI) to estimate anisotropic mechanical properties in six female Yucatan minipigs at ages from 3 to 6 months. Fiber direction was estimated from the principal axis of the diffusion tensor in each voxel. Harmonic shear waves in the brain were excited by three different configurations of a jaw actuator and measured using a motion-sensitive MR imaging sequence. Anisotropic mechanical properties are estimated from displacement field and fiber direction data with a finite element- based, transversely-isotropic nonlinear inversion (TI-NLI) algorithm. TI-NLI finds spatially resolved TI material properties that minimize the error between measured and simulated displacement fields. Maps of anisotropic mechanical properties in the minipig brain were generated for each animal at all four ages. These maps show that white matter is more dissipative and anisotropic than gray matter, and reveal significant effects of brain development on brain stiffness and structural anisotropy. Changes in brain mechanical properties may be a fundamental biophysical signature of brain development.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>37369255</pmid><doi>10.1016/j.neuroimage.2023.120234</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0003-4303-0704</orcidid><orcidid>https://orcid.org/0000-0002-3085-3878</orcidid><orcidid>https://orcid.org/0000-0001-6993-3501</orcidid><orcidid>https://orcid.org/0000-0002-7760-131X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Anisotropy Brain Brain - diagnostic imaging Brain development Brain mapping Child development Cognition & reasoning Diffusion Tensor Imaging Elasticity Imaging Techniques - methods Estimates Female Jaw Longitudinal studies Magnetic resonance elastography Magnetic resonance imaging Mechanical properties Motion detection Neuroimaging Stiffness Substantia alba Substantia grisea Swine Swine, Miniature Viscoelasticity |
title | Mechanical stiffness and anisotropy measured by MRE during brain development in the minipig |
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