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Brain Structure and Function

Erschienen in:

17.09.2018 | Original Article

Whole mouse brain structural connectomics using magnetic resonance histology

verfasst von: Nian Wang, Robert J. Anderson, Alexandra Badea, Gary Cofer, Russell Dibb, Yi Qi, G. Allan Johnson

Erschienen in: Brain Structure and Function | Ausgabe 9/2018

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Abstract

Diffusion tensor histology holds great promise for quantitative characterization of structural connectivity in mouse models of neurological and psychiatric conditions. There has been extensive study in both the clinical and preclinical domains on the complex tradeoffs between the spatial resolution, the number of samples in diffusion q-space, scan time, and the reliability of the resultant data. We describe here a method for accelerating the acquisition of diffusion MRI data to support quantitative connectivity measurements in the whole mouse brain using compressed sensing (CS). The use of CS allows substantial increase in spatial resolution and/or reduction in scan time. Compared to the fully sampled results at the same scan time, the subtle anatomical details of the brain, such as cortical layers, dentate gyrus, and cerebellum, were better visualized using CS due to the higher spatial resolution. Compared to the fully sampled results at the same spatial resolution, the scalar diffusion metrics, including fractional anisotropy (FA) and mean diffusivity (MD), showed consistently low error across the whole brain (< 6.0%) even with 8.0 times acceleration. The node properties of connectivity (strength, cluster coefficient, eigenvector centrality, and local efficiency) demonstrated correlation of better than 95.0% between accelerated and fully sampled connectomes. The acceleration will enable routine application of this technology to a wide range of mouse models of neurologic diseases.

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Adcock B, Hansen A, Roman B, Teschke G (2014) Generalized sampling: stable reconstructions, inverse problems and compressed sensing over the continuum. Adv Image Electron Phys 182:187–279. https://doi.org/10.1016/B978-0-12-800146-2.00004-7 CrossRef

Baldoli C, Scola E, Della Rosa PA, Pontesilli S, Longaretti R, Poloniato A, Scotti R, Blasi V, Cirillo S, Iadanza A, Rovelli R, Barera G, Scifo P (2015) Maturation of preterm newborn brains: a fMRI-DTI study of auditory processing of linguistic stimuli and white matter development. Brain Struct Funct 220(6):3733–3751. https://doi.org/10.1007/s00429-014-0887-5 CrossRefPubMed

Bargmann CI, Marder E (2013) From the connectome to brain function. Nat Methods 10(6):483–490CrossRef

Barth M, Breuer F, Koopmans PJ, Norris DG, Poser BA (2016) Simultaneous multislice (SMS) imaging techniques. Magn Reson Med 75(1):63–81. https://doi.org/10.1002/mrm.25897 CrossRef

Bilgic B, Ye H, Wald LL, Setsompop K (2017) Simultaneous time interleaved multislice (STIMS) for rapid susceptibility weighted acquisition. Neuroimage 155:577–586. https://doi.org/10.1016/j.neuroimage.2017.04.036 CrossRefPubMedPubMedCentral

Boretius S, Michaelis T, Tammer R, Ashery-Padan R, Frahm J, Stoykova A (2009) In vivo MRI of altered brain anatomy and fiber connectivity in adult pax6 deficient mice. Cereb Cortex 19(12):2838–2847. https://doi.org/10.1093/cercor/bhp057 CrossRefPubMed

Bozzali M, Parker GJ, Serra L, Embleton K, Gili T, Perri R, Caltagirone C, Cercignani M (2011) Anatomical connectivity mapping: a new tool to assess brain disconnection in Alzheimer’s disease. Neuroimage 54(3):2045–2051. https://doi.org/10.1016/j.neuroimage.2010.08.069 CrossRefPubMed

Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10(3):186–198. https://doi.org/10.1038/nrn2575 CrossRefPubMed

Calabrese E, Badea A, Cofer G, Qi Y, Johnson GA (2015) A diffusion MRI tractography connectome of the mouse brain and comparison with neuronal tracer data. Cereb Cortex 25(11):4628–4637. https://doi.org/10.1093/cercor/bhv121 CrossRefPubMedPubMedCentral

Chang HC, Sundman M, Petit L, Guhaniyogi S, Chu ML, Petty C, Song AW, Chen NK (2015) Human brain diffusion tensor imaging at submillimeter isotropic resolution on a 3 T clinical MRI scanner. Neuroimage 118:667–675. https://doi.org/10.1016/j.neuroimage.2015.06.016 CrossRefPubMedPubMedCentral

Chen H, Liu T, Zhao Y, Zhang T, Li Y, Li M, Zhang H, Kuang H, Guo L, Tsien JZ, Liu T (2015) Optimization of large-scale mouse brain connectome via joint evaluation of DTI and neuron tracing data. Neuroimage 115:202–213. https://doi.org/10.1016/j.neuroimage.2015.04.050 CrossRefPubMedPubMedCentral

Dai JK, Wang SX, Shan D, Niu HC, Lei H (2017) A diffusion tensor imaging atlas of white matter in tree shrew. Brain Struct Funct 222(4):1733–1751. https://doi.org/10.1007/s00429-016-1304-z CrossRefPubMed

Deshmane A, Gulani V, Griswold MA, Seiberlich N (2012) Parallel MR imaging. J Magn Reson Image 36(1):55–72. https://doi.org/10.1002/jmri.23639 CrossRef

Dyrby TB, Baare WF, Alexander DC, Jelsing J, Garde E, Sogaard LV (2011) An ex vivo imaging pipeline for producing high-quality and high-resolution diffusion-weighted imaging datasets. Hum Brain Map 32(4):544–563. https://doi.org/10.1002/hbm.21043 CrossRef

Guggisberg AG, Honma SM, Findlay AM, Dalal SS, Kirsch HE, Berger MS, Nagarajan SS (2008) Mapping functional connectivity in patients with brain lesions. Ann Neurol 63(2):193–203. https://doi.org/10.1002/ana.21224 CrossRefPubMedPubMedCentral

Herculano-Houzel S (2009) The human brain in numbers: a linearly scaled-up primate brain. Front Hum Neurosci 3:31. https://doi.org/10.3389/neuro.09.031.2009 CrossRefPubMedPubMedCentral

Hubner NS, Mechling AE, Lee HL, Reisert M, Bienert T, Hennig J, von Elverfeldt D, Harsan LA (2017) The connectomics of brain demyelination: functional and structural patterns in the cuprizone mouse model. Neuroimage 146:1–18. https://doi.org/10.1016/j.neuroimage.2016.11.008 CrossRefPubMed

Insel TR, Landis SC, Collins FS (2013) Research priorities. The NIH BRAIN Initiative. Science 340(6133):687–688. https://doi.org/10.1126/science.1239276 CrossRefPubMedPubMedCentral

Kingwell K (2012) Brain imaging: measures of functional brain connectivity can be used to predict outcome after glioma surgery. Nat Rev Neurol 8(10):532. https://doi.org/10.1038/nrneurol.2012.187 CrossRefPubMed

Liang D, Liu B, Wang J, Ying L (2009) Accelerating SENSE using compressed sensing. Magn Reson Med 62(6):1574–1584. https://doi.org/10.1002/mrm.22161 CrossRefPubMed

Lustig M, Donoho D, Pauly JM (2007) Sparse MRI: the application of compressed sensing for rapid MR imaging. Magn Reson Med 58(6):1182–1195. https://doi.org/10.1002/mrm.21391 CrossRefPubMed

Lustig M, Donoho DL, Santos JM, Pauly JM (2008) Compressed sensing MRI. IEEE Signal Proc Magn 25(2):72–82. https://doi.org/10.1109/Msp.2007.914728 CrossRef

Maier-Hein KH, Neher PF, Houde JC, Cote MA, Garyfallidis E, Zhong J, Chamberland M, Yeh FC, Lin YC, Ji Q, Reddick WE, Glass JO, Chen DQ, Feng Y, Gao C, Wu Y, Ma J, Renjie H, Li Q, Westin CF, Deslauriers-Gauthier S, Gonzalez JOO, Paquette M, St-Jean S, Girard G, Rheault F, Sidhu J, Tax CMW, Guo F, Mesri HY, David S, Froeling M, Heemskerk AM, Leemans A, Bore A, Pinsard B, Bedetti C, Desrosiers M, Brambati S, Doyon J, Sarica A, Vasta R, Cerasa A, Quattrone A, Yeatman J, Khan AR, Hodges W, Alexander S, Romascano D, Barakovic M, Auria A, Esteban O, Lemkaddem A, Thiran JP, Cetingul HE, Odry BL, Mailhe B, Nadar MS, Pizzagalli F, Prasad G, Villalon-Reina JE, Galvis J, Thompson PM, Requejo FS, Laguna PL, Lacerda LM, Barrett R, Dell’Acqua F, Catani M, Petit L, Caruyer E, Daducci A, Dyrby TB, Holland-Letz T, Hilgetag CC, Stieltjes B, Descoteaux M (2017) The challenge of mapping the human connectome based on diffusion tractography. Nat Commun 8(1):1349. https://doi.org/10.1038/s41467-017-01285-x CrossRefPubMedPubMedCentral

Moldrich RX, Pannek K, Hoch R, Rubenstein JL, Kurniawan ND, Richards LJ (2010) Comparative mouse brain tractography of diffusion magnetic resonance imaging. Neuroimage 51(3):1027–1036. https://doi.org/10.1016/j.neuroimage.2010.03.035 CrossRefPubMedPubMedCentral

Mukai J, Tamura M, Fenelon K, Rosen AM, Spellman TJ, Kang R, MacDermott AB, Karayiorgou M, Gordon JA, Gogos JA (2015) Molecular substrates of altered axonal growth and brain connectivity in a mouse model of schizophrenia. Neuron 86(3):680–695. https://doi.org/10.1016/j.neuron.2015.04.003 CrossRefPubMedPubMedCentral

Oh SW, Harris JA, Ng L, Winslow B, Cain N, Mihalas S, Wang Q, Lau C, Kuan L, Henry AM, Mortrud MT, Ouellette B, Nguyen TN, Sorensen SA, Slaughterbeck CR, Wakeman W, Li Y, Feng D, Ho A, Nicholas E, Hirokawa KE, Bohn P, Joines KM, Peng H, Hawrylycz MJ, Phillips JW, Hohmann JG, Wohnoutka P, Gerfen CR, Koch C, Bernard A, Dang C, Jones AR, Zeng H (2014) A mesoscale connectome of the mouse brain. Nature 508(7495):207–214. https://doi.org/10.1038/nature13186 CrossRefPubMedPubMedCentral

Pandit AS, Robinson E, Aljabar P, Ball G, Gousias IS, Wang Z, Hajnal JV, Rueckert D, Counsell SJ, Montana G, Edwards AD (2014) Whole-brain mapping of structural connectivity in infants reveals altered connection strength associated with growth and preterm birth. Cereb Cortex 24(9):2324–2333. https://doi.org/10.1093/cercor/bht086 CrossRefPubMed

Pievani M, Filippini N, van den Heuvel MP, Cappa SF, Frisoni GB (2014) Brain connectivity in neurodegenerative diseases—from phenotype to proteinopathy. Nat Rev Neurol 10(11):620–633. https://doi.org/10.1038/nrneurol.2014.178 CrossRefPubMed

Poirier GL, Huang W, Tam K, DiFranza JR, King JA (2017) Awake whole-brain functional connectivity alterations in the adolescent spontaneously hypertensive rat feature visual streams and striatal networks. Brain Struct Funct 222(4):1673–1683. https://doi.org/10.1007/s00429-016-1301-2 CrossRefPubMed

Ragan T, Kadiri LR, Venkataraju KU, Bahlmann K, Sutin J, Taranda J, Arganda-Carreras I, Kim Y, Seung HS, Osten P (2012) Serial two-photon tomography for automated ex vivo mouse brain imaging. Nat Methods 9(3):255–258. https://doi.org/10.1038/nmeth.1854 CrossRefPubMedPubMedCentral

Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52(3):1059–1069. https://doi.org/10.1016/j.neuroimage.2009.10.003 CrossRefPubMed

Sierra A, Laitinen T, Grohn O, Pitkanen A (2015) Diffusion tensor imaging of hippocampal network plasticity. Brain Struct Funct 220(2):781–801. https://doi.org/10.1007/s00429-013-0683-7 CrossRefPubMed

Sotiropoulos SN, Jbabdi S, Xu JQ, Andersson JL, Moeller S, Auerbach EJ, Glasser MF, Hernandez M, Sapiro G, Jenkinson M, Feinberg DA, Yacoub E, Lenglet C, Van Essen DC, Ugurbil K, Behrens TEJ, Consortium W-MH (2013) Advances in diffusion MRI acquisition and processing in the human connectome project. Neuroimage 80:125–143. https://doi.org/10.1016/j.neuroimage.2013.05.057 CrossRefPubMedPubMedCentral

Sporns O, Bullmore ET (2014) From connections to function: the mouse brain connectome atlas. Cell 157(4):773–775. https://doi.org/10.1016/j.cell.2014.04.023 CrossRefPubMed

Stejskal EO, Tanner JE (1965) Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient. J Chem Phys 42(1):288–292. https://doi.org/10.1063/1.1695690 CrossRef

Thomas C, Ye FQ, Irfanoglu MO, Modi P, Saleem KS, Leopold DA, Pierpaoli C (2014) Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc Natl Acad Sci USA 111(46):16574–16579. https://doi.org/10.1073/pnas.1405672111 CrossRefPubMed

Tournier JD, Calamante F, Connelly A (2013) Determination of the appropriate b value and number of gradient directions for high-angular-resolution diffusion-weighted imaging. NMR Biomed 26(12):1775–1786. https://doi.org/10.1002/nbm.3017 CrossRefPubMed

Tuch DS, Reese TG, Wiegell MR, Makris N, Belliveau JW, Wedeen VJ (2002) High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity. Magn Reson Med 48(4):577–582. https://doi.org/10.1002/mrm.10268 CrossRefPubMed

Ugwu ID, Amico F, Carballedo A, Fagan AJ, Frodl T (2015) Childhood adversity, depression, age and gender effects on white matter microstructure: a DTI study. Brain Struct Funct 220(4):1997–2009. https://doi.org/10.1007/s00429-014-0769-x CrossRefPubMed

Volz LJ, Cieslak M, Grafton ST (2018) A probabilistic atlas of fiber crossings for variability reduction of anisotropy measures. Brain Struct Funct 223(2):635–651. https://doi.org/10.1007/s00429-017-1508-x CrossRefPubMed

Vu AT, Auerbach E, Lenglet C, Moeller S, Sotiropoulos SN, Jbabdi S, Andersson J, Yacoub E, Ugurbil K (2015) High resolution whole brain diffusion imaging at 7 T for the human connectome project. Neuroimage 122:318–331. https://doi.org/10.1016/j.neuroimage.2015.08.004 CrossRefPubMedPubMedCentral

Wang N, Badar F, Xia Y (2018) Compressed sensing in quantitative determination of GAG concentration in cartilage by microscopic MRI. Magn Reson Med 79(6):3163–3171. https://doi.org/10.1002/mrm.26973 CrossRefPubMed

Wu Y, Zhu YJ, Tang QY, Zou C, Liu W, Dai RB, Liu X, Wu EX, Ying L, Liang D (2014) Accelerated MR diffusion tensor imaging using distributed compressed sensing. Magn Reson Med 71(2):763–772. https://doi.org/10.1002/mrm.24721 CrossRefPubMed

Yeh FC, Wedeen VJ, Tseng WY (2010) Generalized q-sampling imaging. IEEE Trans Med Image 29(9):1626–1635. https://doi.org/10.1109/TMI.2010.2045126 CrossRef

Yeh FC, Verstynen TD, Wang Y, Fernandez-Miranda JC, Tseng WY (2013) Deterministic diffusion fiber tracking improved by quantitative anisotropy. PLoS One 8(11):e80713. https://doi.org/10.1371/journal.pone.0080713 CrossRefPubMedPubMedCentral

Zhang H, Schneider T, Wheeler-Kingshott CA, Alexander DC (2012) NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage 61(4):1000–1016. https://doi.org/10.1016/j.neuroimage.2012.03.072 CrossRefPubMed

Zingg B, Hintiryan H, Gou L, Song MY, Bay M, Bienkowski MS, Foster NN, Yamashita S, Bowman I, Toga AW, Dong HW (2014) Neural networks of the mouse neocortex. Cell 156(5):1096–1111. https://doi.org/10.1016/j.cell.2014.02.023 CrossRefPubMedPubMedCentral

Titel: Whole mouse brain structural connectomics using magnetic resonance histology
verfasst von: Nian Wang
Robert J. Anderson
Alexandra Badea
Gary Cofer
Russell Dibb
Yi Qi
G. Allan Johnson
Publikationsdatum: 17.09.2018
Verlag: Springer Berlin Heidelberg
Erschienen in: Brain Structure and Function / Ausgabe 9/2018
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-018-1750-x

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Whole mouse brain structural connectomics using magnetic resonance histology

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