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

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 ann...

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Main Authors: Konrad Wagstyl, Stéphanie Larocque, Guillem Cucurull, Claude Lepage, Joseph Paul Cohen, Sebastian Bludau, Nicola Palomero-Gallagher, Lindsay B Lewis, Thomas Funck, Hannah Spitzer, Timo Dickscheid, Paul C Fletcher, Adriana Romero, Karl Zilles, Katrin Amunts, Yoshua Bengio, Alan C Evans
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-04-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3000678
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author Konrad Wagstyl
Stéphanie Larocque
Guillem Cucurull
Claude Lepage
Joseph Paul Cohen
Sebastian Bludau
Nicola Palomero-Gallagher
Lindsay B Lewis
Thomas Funck
Hannah Spitzer
Timo Dickscheid
Paul C Fletcher
Adriana Romero
Karl Zilles
Katrin Amunts
Yoshua Bengio
Alan C Evans
author_facet Konrad Wagstyl
Stéphanie Larocque
Guillem Cucurull
Claude Lepage
Joseph Paul Cohen
Sebastian Bludau
Nicola Palomero-Gallagher
Lindsay B Lewis
Thomas Funck
Hannah Spitzer
Timo Dickscheid
Paul C Fletcher
Adriana Romero
Karl Zilles
Katrin Amunts
Yoshua Bengio
Alan C Evans
author_sort Konrad Wagstyl
collection DOAJ
description 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. It was derived from a 3D histological atlas of the human brain at 20-micrometer 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, motor-frontal cortices showed the opposite pattern, with decreases in total and pyramidal layer thickness from motor to frontal association cortices. 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.
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spelling doaj.art-5dd45009725c4010961ce9e5ad0d21252022-12-21T18:34:12ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852020-04-01184e300067810.1371/journal.pbio.3000678BigBrain 3D atlas of cortical layers: Cortical and laminar thickness gradients diverge in sensory and motor cortices.Konrad WagstylStéphanie LarocqueGuillem CucurullClaude LepageJoseph Paul CohenSebastian BludauNicola Palomero-GallagherLindsay B LewisThomas FunckHannah SpitzerTimo DickscheidPaul C FletcherAdriana RomeroKarl ZillesKatrin AmuntsYoshua BengioAlan C EvansHistological 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. It was derived from a 3D histological atlas of the human brain at 20-micrometer 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, motor-frontal cortices showed the opposite pattern, with decreases in total and pyramidal layer thickness from motor to frontal association cortices. 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.https://doi.org/10.1371/journal.pbio.3000678
spellingShingle Konrad Wagstyl
Stéphanie Larocque
Guillem Cucurull
Claude Lepage
Joseph Paul Cohen
Sebastian Bludau
Nicola Palomero-Gallagher
Lindsay B Lewis
Thomas Funck
Hannah Spitzer
Timo Dickscheid
Paul C Fletcher
Adriana Romero
Karl Zilles
Katrin Amunts
Yoshua Bengio
Alan C Evans
BigBrain 3D atlas of cortical layers: Cortical and laminar thickness gradients diverge in sensory and motor cortices.
PLoS Biology
title BigBrain 3D atlas of cortical layers: Cortical and laminar thickness gradients diverge in sensory and motor cortices.
title_full BigBrain 3D atlas of cortical layers: Cortical and laminar thickness gradients diverge in sensory and motor cortices.
title_fullStr BigBrain 3D atlas of cortical layers: Cortical and laminar thickness gradients diverge in sensory and motor cortices.
title_full_unstemmed BigBrain 3D atlas of cortical layers: Cortical and laminar thickness gradients diverge in sensory and motor cortices.
title_short BigBrain 3D atlas of cortical layers: Cortical and laminar thickness gradients diverge in sensory and motor cortices.
title_sort bigbrain 3d atlas of cortical layers cortical and laminar thickness gradients diverge in sensory and motor cortices
url https://doi.org/10.1371/journal.pbio.3000678
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