Abstract
The vascular organization of the human brain can determine neurological and neurophysiological functions, yet thus far it has not been comprehensively mapped. Aging and diseases such as dementia are known to be associated with changes to the vasculature and normative data could help detect these vascular changes in neuroimaging studies. Furthermore, given the well-known impact of venous vessels on the blood oxygen level dependent (BOLD) signal, information about the common location of veins could help detect biases in existing datasets. In this work, a quantitative atlas of the venous vasculature using quantitative susceptibility maps (QSM) acquired with a 0.6-mm isotropic resolution is presented. The Venous Neuroanatomy (VENAT) atlas was created from 5 repeated 7 Tesla MRI measurements in young and healthy volunteers (n = 20, 10 females, mean age = 25.1 ± 2.5 years) using a two-step registration method on 3D segmentations of the venous vasculature. This cerebral vein atlas includes the average vessel location, diameter (mean: 0.84 ± 0.33 mm) and curvature (0.11 ± 0.05 mm−1) from all participants and provides an in vivo measure of the angio-architectonic organization of the human brain and its variability. This atlas can be used as a basis to understand changes in the vasculature during aging and neurodegeneration, as well as vascular and physiological effects in neuroimaging.
Similar content being viewed by others
References
An Y, Shao C, Wang X, Li Z (2011) Geometric properties estimation from discrete curves using discrete derivatives. Comput Graph 35:916–930. https://doi.org/10.1016/j.cag.2011.02.001
Avants BB, Tustison N, Song G (2009) Advanced normalization tools (ANTS). Insight J 2:1–35. http://hdl.handle.net/10380/3113
Bazin P-L, Plessis V, Fan AP, et al (2016) Vessel segmentation from quantitative susceptibility maps for local oxygenation venography. In: 2016 IEEE 13th International Symposium on Biomedical Imaging (ISBI). IEEE, pp 1135–1138
Bell MA, Ball MJ (1985) Laminar variation in the microvascular architecture of normal human visual cortex (area 17). Brain Res 335:139–143. https://doi.org/10.1016/0006-8993(85)90284-7
Bernier M, Cunnane SC, Whittingstall K (2018) The morphology of the human cerebrovascular system. Hum Brain Mapp. https://doi.org/10.1002/hbm.24337
Bilgic B, Fan AP, Polimeni JR et al (2014) Fast quantitative susceptibility mapping with L1-regularization and automatic parameter selection. Magn Reson Med 72:1444–1459. https://doi.org/10.1002/mrm.25029
Boubela RN, Kalcher K, Huf W et al (2015) fMRI measurements of amygdala activation are confounded by stimulus correlated signal fluctuation in nearby veins draining distant brain regions. Sci Rep 5:10499. https://doi.org/10.1038/srep10499
Bouix S, Siddiqi K, Tannenbaum A (2005) Flux driven automatic centerline extraction. Med Image Anal 9:209–221. https://doi.org/10.1016/j.media.2004.06.026
Boxerman JL, Bandettini PA, Kwong KK et al (1995) The intravascular contribution to fmri signal change: monte carlo modeling and diffusion-weighted studies in vivo. Magn Reson Med 34:4–10. https://doi.org/10.1002/mrm.1910340103
Brown WR, Thore CR (2011) Review: cerebral microvascular pathology in ageing and neurodegeneration. Neuropathol Appl Neurobiol 37:56–74. https://doi.org/10.1111/j.1365-2990.2010.01139.x
Brown WR, Moody DM, Challa VR et al (2002) Venous collagenosis and arteriolar tortuosity in leukoaraiosis. J Neurol Sci 203–204:159–163. https://doi.org/10.1016/S0022-510X(02)00283-6
Browning W (1884) The veins of the brain and its envelopes: their anatomy and bearing on the intracranial circulation. Brooklyn, N.Y. : O’Connor
Deh K, Nguyen TD, Eskreis-Winkler S et al (2015) Reproducibility of quantitative susceptibility mapping in the brain at two field strengths from two vendors. J Magn Reson Imaging 42:1592–1600. https://doi.org/10.1002/jmri.24943
Deistung A, Schäfer A, Schweser F et al (2013) Toward in vivo histology: a comparison of quantitative susceptibility mapping (QSM) with magnitude-, phase-, and R2⁎-imaging at ultra-high magnetic field strength. Neuroimage 65:299–314. https://doi.org/10.1016/j.neuroimage.2012.09.055
Donahue MJ, Hoogduin H, van Zijl PCM et al (2011) Blood oxygenation level-dependent (BOLD) total and extravascular signal changes and ΔR2* in human visual cortex at 1.5, 3.0 and 7.0 T. NMR Biomed 24:25–34. https://doi.org/10.1002/nbm.1552
Duvernoy HM, Delon S, Vannson JL (1981) Cortical blood vessels of the human brain. Brain Res Bull 7:519–579. https://doi.org/10.1016/0361-9230(81)90007-1
Duyn JH, van Gelderen P, Li T-Q et al (2007) High-field MRI of brain cortical substructure based on signal phase. Proc Natl Acad Sci USA 104:11796–11801. https://doi.org/10.1073/pnas.0610821104
Einhäupl KM, Villringer A, Mehraein S et al (1991) Heparin treatment in sinus venous thrombosis. Lancet 338:597–600. https://doi.org/10.1016/0140-6736(91)90607-Q
Fan AP, Bilgic B, Gagnon L et al (2014) Quantitative oxygenation venography from MRI phase. Magn Reson Med 72:149–159. https://doi.org/10.1002/mrm.24918
Fischer B, Modersitzki J (2003) FLIRT: A flexible image registration toolbox. Springer, Berlin, pp 261–270
Gagnon L, Sakadžić S, Lesage F et al (2015) Quantifying the microvascular origin of BOLD-fMRI from first principles with two-photon microscopy and an oxygen-sensitive nanoprobe. J Neurosci 35:3663–3675. https://doi.org/10.1523/JNEUROSCI.3555-14.2015
Haacke EM, Xu Y, Cheng Y-CN, Reichenbach JR (2004) Susceptibility weighted imaging (SWI). Magn Reson Med 52:612–618. https://doi.org/10.1002/mrm.20198
Haase A, Frahm J, Matthaei D et al (1986) FLASH imaging. Rapid NMR imaging using low flip-angle pulses. J Magn Reson 67:258–266. https://doi.org/10.1016/0022-2364(86)90433-6
Hammond KE, Lupo JM, Xu D et al (2008) Development of a robust method for generating 7.0 T multichannel phase images of the brain with application to normal volunteers and patients with neurological diseases. Neuroimage 39:1682–1692. https://doi.org/10.1016/j.neuroimage.2007.10.037
Keuken MC, Bazin P-L, Crown L et al (2014) Quantifying inter-individual anatomical variability in the subcortex using 7 T structural MRI. Neuroimage 94:40–46. https://doi.org/10.1016/j.neuroimage.2014.03.032
Kramer AF, Erickson KI, Colcombe SJ (2006) Exercise, cognition, and the aging brain. J Appl Physiol 101:1237–1242. https://doi.org/10.1152/japplphysiol.00500.2006
Langkammer C, Schweser F, Krebs N et al (2012) Quantitative susceptibility mapping (QSM) as a means to measure brain iron? A post mortem validation study. Neuroimage 62:1593–1599. https://doi.org/10.1016/J.NEUROIMAGE.2012.05.049
Logothetis NK, Wandell BA (2004) Interpreting the BOLD Signal. Annu Rev Physiol 66:735–769. https://doi.org/10.1146/annurev.physiol.66.082602.092845
Marques JP, Kober T, Krueger G et al (2010) MP2RAGE, a self bias-field corrected sequence for improved segmentation and T1-mapping at high field. Neuroimage 49:1271–1281. https://doi.org/10.1016/J.NEUROIMAGE.2009.10.002
Miyawaki T, Matsui K, Takashima S (1998) Developmental characteristics of vessel density in the human fetal and infant brains. Early Hum Dev 53:65–72. https://doi.org/10.1016/S0378-3782(98)00043-7
O’Reilly TPA, Webb AG, Brink WM (2016) Practical improvements in the design of high permittivity pads for dielectric shimming in neuroimaging at 7 T. J Magn Reson 270:108–114. https://doi.org/10.1016/j.jmr.2016.07.003
Olman CA, Yacoub E (2011) High-field FMRI for human applications: an overview of spatial resolution and signal specificity. Open Neuroimag J 5:74–89. https://doi.org/10.2174/1874440001105010074
Parkes LM, Schwarzbach JV, Bouts AA et al (2005) Quantifying the spatial resolution of the gradient echo and spin echo BOLD response at 3 Tesla. Magn Reson Med 54:1465–1472. https://doi.org/10.1002/mrm.20712
Pathak AP, Kim E, Zhang J, Jones MV (2011) Three-dimensional imaging of the mouse neurovasculature with magnetic resonance microscopy. PLoS One. https://doi.org/10.1371/journal.pone.0022643
Peters R (2006) Ageing and the brain. Postgrad Med J 82:84–88. https://doi.org/10.1136/pgmj.2005.036665
Seiyama A, Seki J, Tanabe HC et al (2004) Circulatory basis of fMRI signals: relationship between changes in the hemodynamic parameters and BOLD signal intensity. Neuroimage 21:1204–1214. https://doi.org/10.1016/j.neuroimage.2003.12.002
Serres B, Deistung A, Schäfer A et al (2015) Automatic segmentation of the venous vessel network based on quantitative susceptibility maps and its application to investigate blood oxygenation. Proc Intl Soc Mag Reson Med 23:0169
Shaaban CE, Aizenstein HJ, Jorgensen DR et al (2017) In vivo imaging of venous side cerebral small-vessel disease in older adults: an MRI method at 7T. AJNR Am J Neuroradiol 38:1923–1928. https://doi.org/10.3174/ajnr.A5327
Stüber C, Morawski M, Schäfer A et al (2014) Myelin and iron concentration in the human brain: a quantitative study of MRI contrast. Neuroimage 93:95–106. https://doi.org/10.1016/J.NEUROIMAGE.2014.02.026
Topfer R, Schweser F, Deistung A et al (2015) SHARP edges: recovering cortical phase contrast through harmonic extension. Magn Reson Med 73:851–856. https://doi.org/10.1002/mrm.25148
Towbin A (1973) The syndrome of latent cerebral venous thrombosis: its frequency and relation to age and congestive heart failure. Stroke 4:419–430. https://doi.org/10.1161/01.STR.4.3.419
Turner R (2002) How much codex can a vein drain? Downstream dilution of activation-related cerebral blood oxygenation changes. Neuroimage 16:1062–1067. https://doi.org/10.1006/nimg.2002.1082
Vigneau-Roy N, Bernier M, Descoteaux M, Whittingstall K (2014) Regional variations in vascular density correlate with resting-state and task-evoked blood oxygen level-dependent signal amplitude. Hum Brain Mapp 35:1906–1920. https://doi.org/10.1002/hbm.22301
Villringer A, Seiderer M, Bauer W et al (1989) Diagnosis of superior sagittal sinus thrombosis by three-dimensional magnetic resonance flow imaging. Lancet 333:1086–1087. https://doi.org/10.1016/S0140-6736(89)92490-2
Vogl TJ, Bergman C, Villringer A et al (1994) Dural sinus thrombosis: value of venous MR angiography for diagnosis and follow-up. AJR Am J Roentgenol 162:1191–1198. https://doi.org/10.2214/ajr.162.5.8166009
Voss MW, Nagamatsu LS, Liu-Ambrose T, Kramer AF (2011) Exercise, brain, and cognition across the life span. J Appl Physiol 111:1505–1513. https://doi.org/10.1152/japplphysiol.00210.2011
Wahlund LO, Barkhof F, Fazekas F et al (2001) A new rating scale for age-related white matter changes applicable to MRI and CT. Stroke 32:1318–1322
Wang Y, Liu T (2015) Quantitative susceptibility mapping (QSM): decoding MRI data for a tissue magnetic biomarker. Magn Reson Med 73:82–101. https://doi.org/10.1002/mrm.25358
Ward PGD, Ferris NJ, Raniga P et al (2018) Combining images and anatomical knowledge to improve automated vein segmentation in MRI. Neuroimage 165:294–305. https://doi.org/10.1016/j.neuroimage.2017.10.049
Wayne Martin WR, Ye FQ, Allen PS (1998) Increasing striatal iron content associated with normal aging. Mov Disord 13:281–286. https://doi.org/10.1002/mds.870130214
Woerz S, Rohr K (2004) A new 3D parametric intensity model for accurate segmentation and quantification of human vessels. In: Proceedings of MICCAI. pp 491–499
Zecca L, Stroppolo A, Gatti A et al (2004) The role of iron and copper molecules in the neuronal vulnerability of locus coeruleus and substantia nigra during aging. Proc Natl Acad Sci 101:9843–9848
Zheng D, LaMantia A, Purves D (1991) Specialized vascularization of the primate visual cortex. J Neurosci 11:2622–2629. https://doi.org/10.1523/JNEUROSCI.11-08-02622.1991
Acknowledgement
The authors thank Domenica Wilfling and Elisabeth Wladimirov for their help with data acquisition and logistics of the multi-modal plasticity initiative (mMPI) dataset. This work was supported by the Max Planck Society, the Canadian National Sciences and Engineering Research Council (RGPIN-2015-04665, C.J.G.), the Heart and Stroke Foundation of Canada (N.I.A. C.J.G.), the National Institute of Health (1K99NS102884, A.P.F.), the Michal and Renata Hornstein Chair in Cardiovascular Imaging (C.J.G.), and the Quebec Bio-Imaging Network (QBIN) for the scholarship for Training course abroad (J.H.).
Funding
This study was funded by the Max Planck Society, the Canadian National Sciences and Engineering Research Council (RGPIN-2015-04665, C.J.G.), the Heart and Stroke Foundation of Canada (N.I.A. C.J.G.), the National Institute of Health (1K99NS102884, A.P.F.) and the Quebec Bio-Imaging Network (QBIN) for the scholarship for Training course abroad (J.H.).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author Yvonne Wanner has an affiliation with Universität Stuttgart, Stuttgart, Germany and with the Concordia University, Department of Physics, Montreal, Canada. The author Arno Villringer has an affiliation with the Max-Planck-Institut fur Kognitions- und Neurowissenschaften, Leipzig, Germany, the Clinic for Cognitive Neurology, University of Leipzig, Leipzig, Germany, the Leipzig University Medical Centre, IFB Adiposity Diseases, Leipzig, Germany, and the Leipzig University Medical Centre, Collaborative Research Centre 1052-A5, Leipzig, Germany, The author Christopher J. Steele has an affiliation with the Concordia University, Department of Psychology, Montreal, Canada and the Max-Planck-Institut fur Kognitions- und Neurowissenschaften, Leipzig, Germany. The author Christine L. Tardif has an affiliation with the McGill University, Department of Biomedical Engineering, Montreal, Canada and the Montreal Neurological Institute, Montreal, Canada. The author Pierre-Louis Bazin has as affiliation with the University of Amsterdam, Faculty of Social and Behavioural Sciences, Amsterdam, Netherlands and the Max-Planck-Institut fur Kognitions- und Neurowissenschaften, Leipzig, Germany. The author Claudine J. Gauthier has an affiliation with Concordia University, Department of Physics, Montreal, Canada and the Montreal Heart Institute, Montreal, Canada.
Research involving human participants
All procedures performed in studies involving human participants were in accordance with the ethical standards of the Ethics Committee of the University of Leipzig and with the 1964 Helsinki declaration and its later amendments.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Huck, J., Wanner, Y., Fan, A.P. et al. High resolution atlas of the venous brain vasculature from 7 T quantitative susceptibility maps. Brain Struct Funct 224, 2467–2485 (2019). https://doi.org/10.1007/s00429-019-01919-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-019-01919-4