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BigBrain 3D atlas of cortical layers: cortical and laminar thickness gradients diverge in sensory and motor cortices

View ORCID ProfileKonrad Wagstyl, Stéphanie Larocque, Guillem Cucurull, Claude Lepage, Joseph Paul Cohen, Sebastian Bludau, Nicola Palomero-Gallagher, Lindsay B. Lewis, Thomas Funck, Hannah Spitzer, Timo Dicksheid, Paul C Fletcher, Adriana Romero, Karl Zilles, Katrin Amunts, Yoshua Bengio, Alan C. Evans
doi: https://doi.org/10.1101/580597
Konrad Wagstyl
1McGill Centre for Integrative Neuroscience, Montreal Neurological Institute, Montreal, Canada, H3A 2B4
2Department of Psychiatry, University of Cambridge, Cambridge, UK, CB2 0SZ
3Wellcome Trust Centre for Neuroimaging, University College London, London, UK, WC1N 3AR
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  • ORCID record for Konrad Wagstyl
  • For correspondence: k.wagstyl@ucl.ac.uk
Stéphanie Larocque
4MILA, Université de Montréal, Montreal, Canada, H2S 3H1
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Guillem Cucurull
4MILA, Université de Montréal, Montreal, Canada, H2S 3H1
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Claude Lepage
1McGill Centre for Integrative Neuroscience, Montreal Neurological Institute, Montreal, Canada, H3A 2B4
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Joseph Paul Cohen
4MILA, Université de Montréal, Montreal, Canada, H2S 3H1
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Sebastian Bludau
5Institute of Neuroscience and Medicine (INM-1), Forschungszentrum Jülich GmbH, Germany, 52425
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Nicola Palomero-Gallagher
5Institute of Neuroscience and Medicine (INM-1), Forschungszentrum Jülich GmbH, Germany, 52425
6Department of Psychiatry, Psychotherapy and Psychosomatics, Medical Faculty, RWTH Aachen University, Aachen, 52074 Aachen
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Lindsay B. Lewis
1McGill Centre for Integrative Neuroscience, Montreal Neurological Institute, Montreal, Canada, H3A 2B4
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Thomas Funck
1McGill Centre for Integrative Neuroscience, Montreal Neurological Institute, Montreal, Canada, H3A 2B4
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Hannah Spitzer
5Institute of Neuroscience and Medicine (INM-1), Forschungszentrum Jülich GmbH, Germany, 52425
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Timo Dicksheid
5Institute of Neuroscience and Medicine (INM-1), Forschungszentrum Jülich GmbH, Germany, 52425
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Paul C Fletcher
2Department of Psychiatry, University of Cambridge, Cambridge, UK, CB2 0SZ
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Adriana Romero
4MILA, Université de Montréal, Montreal, Canada, H2S 3H1
7Department of Computer Science, McGill University, Montreal, Canada, H3A 0E9
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Karl Zilles
5Institute of Neuroscience and Medicine (INM-1), Forschungszentrum Jülich GmbH, Germany, 52425
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Katrin Amunts
5Institute of Neuroscience and Medicine (INM-1), Forschungszentrum Jülich GmbH, Germany, 52425
8Cecile und Oskar Vogt Institute for Brain Research, Heinrich Heine University Duesseldorf, University Hospital Duesseldorf, Duesseldorf, Germany, 40225
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Yoshua Bengio
4MILA, Université de Montréal, Montreal, Canada, H2S 3H1
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Alan C. Evans
1McGill Centre for Integrative Neuroscience, Montreal Neurological Institute, Montreal, Canada, H3A 2B4
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Abstract

Histological atlases of the cerebral cortex, such as those made famous by Brodmann and von Economo, are invaluable for understanding human brain microstructure and its relationship with functional organization in the brain. However, these existing atlases are limited to small numbers of manually annotated samples from a single cerebral hemisphere, measured from 2D histological sections. We present the first whole-brain quantitative 3D laminar atlas of the human cerebral cortex. This atlas was derived from a 3D histological model of the human brain at 20 micron isotropic resolution (BigBrain), using a convolutional neural network to segment, automatically, the cortical layers in both hemispheres. Our approach overcomes many of the historical challenges with measurement of histological thickness in 2D and the resultant laminar atlas provides an unprecedented level of precision and detail.

We utilized this BigBrain cortical atlas to test whether previously reported thickness gradients, as measured by MRI in sensory and motor processing cortices, were present in a histological atlas of cortical thickness, and which cortical layers were contributing to these gradients. Cortical thickness increased across sensory processing hierarchies, primarily driven by layers III, V and VI. In contrast, fronto-motor cortices showed the opposite pattern, with decreases in total and pyramidal layer thickness. These findings illustrate how this laminar atlas will provide a link between single-neuron morphology, mesoscale cortical layering, macroscopic cortical thickness and, ultimately, functional neuroanatomy.

Footnotes

  • This manuscript has been updated to include comparisons with Von Economo dataset, including changes to all figures. Overall conclusions of the study are unchanged.

  • https://bigbrain.loris.ca/

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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Posted December 10, 2019.
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BigBrain 3D atlas of cortical layers: cortical and laminar thickness gradients diverge in sensory and motor cortices
Konrad Wagstyl, Stéphanie Larocque, Guillem Cucurull, Claude Lepage, Joseph Paul Cohen, Sebastian Bludau, Nicola Palomero-Gallagher, Lindsay B. Lewis, Thomas Funck, Hannah Spitzer, Timo Dicksheid, Paul C Fletcher, Adriana Romero, Karl Zilles, Katrin Amunts, Yoshua Bengio, Alan C. Evans
bioRxiv 580597; doi: https://doi.org/10.1101/580597
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BigBrain 3D atlas of cortical layers: cortical and laminar thickness gradients diverge in sensory and motor cortices
Konrad Wagstyl, Stéphanie Larocque, Guillem Cucurull, Claude Lepage, Joseph Paul Cohen, Sebastian Bludau, Nicola Palomero-Gallagher, Lindsay B. Lewis, Thomas Funck, Hannah Spitzer, Timo Dicksheid, Paul C Fletcher, Adriana Romero, Karl Zilles, Katrin Amunts, Yoshua Bengio, Alan C. Evans
bioRxiv 580597; doi: https://doi.org/10.1101/580597

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