Relating quantitative 7T MRI across cortical depths to cytoarchitectonics, gene expression and connectomics

Peter McColgan; Saskia Helbling; Lenka Vaculčiaková; Kerrin Pine; Konrad Wagstyl; Fakhereh Movahedian Attar; Luke Edwards; Marina Papoutsi; Yongbin Wei; Martijn Pieter Van den Heuvel; Sarah J. Tabrizi; Geraint Rees; Nikolaus Weiskopf

doi:10.1002/hbm.25595

Relating quantitative 7T MRI across cortical depths to cytoarchitectonics, gene expression and connectomics

Peter McColgan^*, Saskia Helbling, Lenka Vaculčiaková, Kerrin Pine, Konrad Wagstyl, Fakhereh Movahedian Attar, Luke Edwards, Marina Papoutsi, Yongbin Wei, Martijn Pieter Van den Heuvel, Sarah J. Tabrizi, Geraint Rees, Nikolaus Weiskopf

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Ultra-high field MRI across the depth of the cortex has the potential to provide anatomically precise biomarkers and mechanistic insights into neurodegenerative disease like Huntington's disease that show layer-selective vulnerability. Here we compare multi-parametric mapping (MPM) measures across cortical depths for a 7T 500 μm whole brain acquisition to (a) layer-specific cell measures from the von Economo histology atlas, (b) layer-specific gene expression, using the Allen Human Brain atlas and (c) white matter connections using high-fidelity diffusion tractography, at a 1.3 mm isotropic voxel resolution, from a 300mT/m Connectom MRI system. We show that R2*, but not R1, across cortical depths is highly correlated with layer-specific cell number and layer-specific gene expression. R1- and R2*-weighted connectivity strength of cortico-striatal and intra-hemispheric cortical white matter connections was highly correlated with grey matter R1 and R2* across cortical depths. Limitations of the layer-specific relationships demonstrated are at least in part related to the high cross-correlations of von Economo atlas cell counts and layer-specific gene expression across cortical layers. These findings demonstrate the potential and limitations of combining 7T MPMs, gene expression and white matter connections to provide an anatomically precise framework for tracking neurodegenerative disease.

Original language	English
Pages (from-to)	4996-5009
Number of pages	14
Journal	Human Brain Mapping
Volume	42
Issue number	15
DOIs	https://doi.org/10.1002/hbm.25595
Publication status	Published - 15 Oct 2021

Bibliographical note

Funding Information:
Bundesministerium für Bildung und Forschung, Grant/Award Number: 01EW1711A & B; FP7 Ideas: European Research Council, Grant/Award Number: 616905; Scientific Education and Research Institute, Grant/Award Number: 15.0137; Swiss State Secretariat for Education, Research and Innovation (SERI); European Union's Horizon 2020 research and innovation programme, Grant/Award Number: 681094 Funding information

Funding Information:
We would like to thank Dr. Evgeniya Kirilina for her advice regarding study design. We would also like to thank the University of Minnesota Center for Magnetic Resonance Research for the provision of the multiband EPI sequence software. We would like to thank C. R?ger and R. Haak (Department of Cardiology, Endodontology and Periodontology, University Medical Center Leipzig) for manufacturing the mouth guards for the optical prospective motion correction. The research leading to these results has received funding from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement n? 616905. N.W. received funding from the BMBF (01EW1711A & B) in the framework of ERA-NET NEURON, and from the NISCI project funded by the European Union's Horizon 2020 research and innovation programme under the grant agreement No 681094, and the Swiss State Secretariat for Education, Research and Innovation (SERI) under contract number 15.0137. Open access funding enabled and organized by Projekt DEAL.

Funding Information:
We would like to thank Dr. Evgeniya Kirilina for her advice regarding study design. We would also like to thank the University of Minnesota Center for Magnetic Resonance Research for the provision of the multiband EPI sequence software. We would like to thank C. Rüger and R. Haak (Department of Cardiology, Endodontology and Periodontology, University Medical Center Leipzig) for manufacturing the mouth guards for the optical prospective motion correction. The research leading to these results has received funding from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007‐2013)/ERC grant agreement n° 616905. N.W. received funding from the BMBF (01EW1711A & B) in the framework of ERA‐NET NEURON, and from the NISCI project funded by the European Union's Horizon 2020 research and innovation programme under the grant agreement No 681094, and the Swiss State Secretariat for Education, Research and Innovation (SERI) under contract number 15.0137. Open access funding enabled and organized by Projekt DEAL.

Publisher Copyright:
© 2021 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.

Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.

Keywords

gene expression
histology
neurodegeneration
ultra-high field MRI

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McColgan, P., Helbling, S., Vaculčiaková, L., Pine, K., Wagstyl, K., Attar, F. M., Edwards, L., Papoutsi, M., Wei, Y., Van den Heuvel, M. P., Tabrizi, S. J., Rees, G., & Weiskopf, N. (2021). Relating quantitative 7T MRI across cortical depths to cytoarchitectonics, gene expression and connectomics. Human Brain Mapping, 42(15), 4996-5009. https://doi.org/10.1002/hbm.25595

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title = "Relating quantitative 7T MRI across cortical depths to cytoarchitectonics, gene expression and connectomics",

abstract = "Ultra-high field MRI across the depth of the cortex has the potential to provide anatomically precise biomarkers and mechanistic insights into neurodegenerative disease like Huntington's disease that show layer-selective vulnerability. Here we compare multi-parametric mapping (MPM) measures across cortical depths for a 7T 500 μm whole brain acquisition to (a) layer-specific cell measures from the von Economo histology atlas, (b) layer-specific gene expression, using the Allen Human Brain atlas and (c) white matter connections using high-fidelity diffusion tractography, at a 1.3 mm isotropic voxel resolution, from a 300mT/m Connectom MRI system. We show that R2*, but not R1, across cortical depths is highly correlated with layer-specific cell number and layer-specific gene expression. R1- and R2*-weighted connectivity strength of cortico-striatal and intra-hemispheric cortical white matter connections was highly correlated with grey matter R1 and R2* across cortical depths. Limitations of the layer-specific relationships demonstrated are at least in part related to the high cross-correlations of von Economo atlas cell counts and layer-specific gene expression across cortical layers. These findings demonstrate the potential and limitations of combining 7T MPMs, gene expression and white matter connections to provide an anatomically precise framework for tracking neurodegenerative disease.",

keywords = "gene expression, histology, neurodegeneration, ultra-high field MRI",

author = "Peter McColgan and Saskia Helbling and Lenka Vacul{\v c}iakov{\'a} and Kerrin Pine and Konrad Wagstyl and Attar, {Fakhereh Movahedian} and Luke Edwards and Marina Papoutsi and Yongbin Wei and {Van den Heuvel}, {Martijn Pieter} and Tabrizi, {Sarah J.} and Geraint Rees and Nikolaus Weiskopf",

note = "Funding Information: Bundesministerium f{\"u}r Bildung und Forschung, Grant/Award Number: 01EW1711A & B; FP7 Ideas: European Research Council, Grant/Award Number: 616905; Scientific Education and Research Institute, Grant/Award Number: 15.0137; Swiss State Secretariat for Education, Research and Innovation (SERI); European Union's Horizon 2020 research and innovation programme, Grant/Award Number: 681094 Funding information Funding Information: We would like to thank Dr. Evgeniya Kirilina for her advice regarding study design. We would also like to thank the University of Minnesota Center for Magnetic Resonance Research for the provision of the multiband EPI sequence software. We would like to thank C. R?ger and R. Haak (Department of Cardiology, Endodontology and Periodontology, University Medical Center Leipzig) for manufacturing the mouth guards for the optical prospective motion correction. The research leading to these results has received funding from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement n? 616905. N.W. received funding from the BMBF (01EW1711A & B) in the framework of ERA-NET NEURON, and from the NISCI project funded by the European Union's Horizon 2020 research and innovation programme under the grant agreement No 681094, and the Swiss State Secretariat for Education, Research and Innovation (SERI) under contract number 15.0137. Open access funding enabled and organized by Projekt DEAL. Funding Information: We would like to thank Dr. Evgeniya Kirilina for her advice regarding study design. We would also like to thank the University of Minnesota Center for Magnetic Resonance Research for the provision of the multiband EPI sequence software. We would like to thank C. R{\"u}ger and R. Haak (Department of Cardiology, Endodontology and Periodontology, University Medical Center Leipzig) for manufacturing the mouth guards for the optical prospective motion correction. The research leading to these results has received funding from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007‐2013)/ERC grant agreement n° 616905. N.W. received funding from the BMBF (01EW1711A & B) in the framework of ERA‐NET NEURON, and from the NISCI project funded by the European Union's Horizon 2020 research and innovation programme under the grant agreement No 681094, and the Swiss State Secretariat for Education, Research and Innovation (SERI) under contract number 15.0137. Open access funding enabled and organized by Projekt DEAL. Publisher Copyright: {\textcopyright} 2021 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.",

year = "2021",

month = oct,

day = "15",

doi = "10.1002/hbm.25595",

language = "English",

volume = "42",

pages = "4996--5009",

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T1 - Relating quantitative 7T MRI across cortical depths to cytoarchitectonics, gene expression and connectomics

AU - McColgan, Peter

AU - Helbling, Saskia

AU - Vaculčiaková, Lenka

AU - Pine, Kerrin

AU - Wagstyl, Konrad

AU - Attar, Fakhereh Movahedian

AU - Edwards, Luke

AU - Papoutsi, Marina

AU - Wei, Yongbin

AU - Van den Heuvel, Martijn Pieter

AU - Tabrizi, Sarah J.

AU - Rees, Geraint

AU - Weiskopf, Nikolaus

N1 - Funding Information: Bundesministerium für Bildung und Forschung, Grant/Award Number: 01EW1711A & B; FP7 Ideas: European Research Council, Grant/Award Number: 616905; Scientific Education and Research Institute, Grant/Award Number: 15.0137; Swiss State Secretariat for Education, Research and Innovation (SERI); European Union's Horizon 2020 research and innovation programme, Grant/Award Number: 681094 Funding information Funding Information: We would like to thank Dr. Evgeniya Kirilina for her advice regarding study design. We would also like to thank the University of Minnesota Center for Magnetic Resonance Research for the provision of the multiband EPI sequence software. We would like to thank C. R?ger and R. Haak (Department of Cardiology, Endodontology and Periodontology, University Medical Center Leipzig) for manufacturing the mouth guards for the optical prospective motion correction. The research leading to these results has received funding from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement n? 616905. N.W. received funding from the BMBF (01EW1711A & B) in the framework of ERA-NET NEURON, and from the NISCI project funded by the European Union's Horizon 2020 research and innovation programme under the grant agreement No 681094, and the Swiss State Secretariat for Education, Research and Innovation (SERI) under contract number 15.0137. Open access funding enabled and organized by Projekt DEAL. Funding Information: We would like to thank Dr. Evgeniya Kirilina for her advice regarding study design. We would also like to thank the University of Minnesota Center for Magnetic Resonance Research for the provision of the multiband EPI sequence software. We would like to thank C. Rüger and R. Haak (Department of Cardiology, Endodontology and Periodontology, University Medical Center Leipzig) for manufacturing the mouth guards for the optical prospective motion correction. The research leading to these results has received funding from the European Research Council under the European Union's Seventh Framework Programme (FP7/2007‐2013)/ERC grant agreement n° 616905. N.W. received funding from the BMBF (01EW1711A & B) in the framework of ERA‐NET NEURON, and from the NISCI project funded by the European Union's Horizon 2020 research and innovation programme under the grant agreement No 681094, and the Swiss State Secretariat for Education, Research and Innovation (SERI) under contract number 15.0137. Open access funding enabled and organized by Projekt DEAL. Publisher Copyright: © 2021 The Authors. Human Brain Mapping published by Wiley Periodicals LLC. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

PY - 2021/10/15

Y1 - 2021/10/15

N2 - Ultra-high field MRI across the depth of the cortex has the potential to provide anatomically precise biomarkers and mechanistic insights into neurodegenerative disease like Huntington's disease that show layer-selective vulnerability. Here we compare multi-parametric mapping (MPM) measures across cortical depths for a 7T 500 μm whole brain acquisition to (a) layer-specific cell measures from the von Economo histology atlas, (b) layer-specific gene expression, using the Allen Human Brain atlas and (c) white matter connections using high-fidelity diffusion tractography, at a 1.3 mm isotropic voxel resolution, from a 300mT/m Connectom MRI system. We show that R2*, but not R1, across cortical depths is highly correlated with layer-specific cell number and layer-specific gene expression. R1- and R2*-weighted connectivity strength of cortico-striatal and intra-hemispheric cortical white matter connections was highly correlated with grey matter R1 and R2* across cortical depths. Limitations of the layer-specific relationships demonstrated are at least in part related to the high cross-correlations of von Economo atlas cell counts and layer-specific gene expression across cortical layers. These findings demonstrate the potential and limitations of combining 7T MPMs, gene expression and white matter connections to provide an anatomically precise framework for tracking neurodegenerative disease.

AB - Ultra-high field MRI across the depth of the cortex has the potential to provide anatomically precise biomarkers and mechanistic insights into neurodegenerative disease like Huntington's disease that show layer-selective vulnerability. Here we compare multi-parametric mapping (MPM) measures across cortical depths for a 7T 500 μm whole brain acquisition to (a) layer-specific cell measures from the von Economo histology atlas, (b) layer-specific gene expression, using the Allen Human Brain atlas and (c) white matter connections using high-fidelity diffusion tractography, at a 1.3 mm isotropic voxel resolution, from a 300mT/m Connectom MRI system. We show that R2*, but not R1, across cortical depths is highly correlated with layer-specific cell number and layer-specific gene expression. R1- and R2*-weighted connectivity strength of cortico-striatal and intra-hemispheric cortical white matter connections was highly correlated with grey matter R1 and R2* across cortical depths. Limitations of the layer-specific relationships demonstrated are at least in part related to the high cross-correlations of von Economo atlas cell counts and layer-specific gene expression across cortical layers. These findings demonstrate the potential and limitations of combining 7T MPMs, gene expression and white matter connections to provide an anatomically precise framework for tracking neurodegenerative disease.

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KW - histology

KW - neurodegeneration

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Relating quantitative 7T MRI across cortical depths to cytoarchitectonics, gene expression and connectomics

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Keywords

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