A bipolar taxonomy of adult human brain sulcal morphology related to timing of fetal sulcation and trans-sulcal gene expression gradients

William E Snyder; Petra E. Vértes; Vanessa Kyriakopoulou; Konrad Wagstyl; Logan Z. J. Williams; Dustin Moraczewski; Adam G. Thomas; Vyacheslav R. Karolis; Jakob Seidlitz; Denis Rivière; Emma C. Robinson; Jean-Francois Mangin; Armin Raznahan; Edward T. Bullmore

doi:10.1101/2023.12.19.572454

A bipolar taxonomy of adult human brain sulcal morphology related to timing of fetal sulcation and trans-sulcal gene expression gradients

William E Snyder, Petra E. Vértes, Vanessa Kyriakopoulou, Konrad Wagstyl, Logan Z. J. Williams, Dustin Moraczewski, Adam G. Thomas, Vyacheslav R. Karolis, Jakob Seidlitz, Denis Rivière, Emma C. Robinson, Jean-Francois Mangin, Armin Raznahan, Edward T. Bullmore

University of Cambridge
School of Biomedical Engineering and Imaging Sciences
School of Biomedical Engineering and Imaging Science, KCL, London, UK. [email protected].
Laboratory of Neuropsychology, National Institute of Mental Health, Bethesda, MD 20892, USA; Neurophysiology Imaging Facility, National Institute of Mental Health, National Institute of Neurological Disorders and Stroke, National Eye Institute, Bethesda, MD 20892, USA.
Center for Systems Genomics, Pennsylvania State University, University Park, Pennsylvania, USA.
Université Paris-Saclay, CNRS UMR 8612, Institut Galien Paris-Saclay, Châtenay-Malabry, France
National Institute of Mental Health Intramural Research Program, Bethesda 20892, USA; Neuroimaging & Cognitive Genomics Centre (NICOG), Clinical Neuroimaging Laboratory, NCBES Galway Neuroscience Centre, College of Medicine Nursing and Health Sciences, National University of Ireland Galway, H91 TK33 Galway, Ireland.
1Department of Hepatology, Imperial College London, London, UK. 2Institute of Liver Studies at King's College School of Medicine at King's College Hospital, London, UK. 3Institute of Human Health and Performance, University College London, London, UK. 4Department of Asthma Allergy and Lung Biology, King's College London, London, UK. 5Division of Critical Care Medicine, University of Alberta, Edmonton, Canada.

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Abstract

We developed a computational pipeline (now provided as a resource) for measuring morphological similarity between cortical surface sulci to construct a sulcal phenotype network (SPN) from each magnetic resonance imaging (MRI) scan in an adult cohort (N=34,725; 45-82 years). Networks estimated from pairwise similarities of 40 sulci on 5 morphological metrics comprised two clusters of sulci, represented also by the bipolar distribution of sulci on a linear-to-complex dimension. Linear sulci were more heritable and typically located in unimodal cortex; complex sulci were less heritable and typically located in heteromodal cortex. Aligning these results with an independent fetal brain MRI cohort (N=228; 21-36 gestational weeks), we found that linear sulci formed earlier, and the earliest and latest-forming sulci had the least between-adult variation. Using high-resolution maps of cortical gene expression, we found that linear sulcation is mechanistically underpinned by trans-sulcal gene expression gradients enriched for developmental processes.

Original language	English
Publisher	Neuron
Number of pages	35
DOIs	https://doi.org/10.1101/2023.12.19.572454
Publication status	Accepted/In press - 2024

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Snyder, W. E., Vértes, P. E., Kyriakopoulou, V., Wagstyl, K., Williams, L. Z. J., Moraczewski, D., Thomas, A. G., Karolis, V. R., Seidlitz, J., Rivière, D., Robinson, E. C., Mangin, J.-F., Raznahan, A., & Bullmore, E. T. (Accepted/In press). A bipolar taxonomy of adult human brain sulcal morphology related to timing of fetal sulcation and trans-sulcal gene expression gradients. Neuron. https://doi.org/10.1101/2023.12.19.572454

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title = "A bipolar taxonomy of adult human brain sulcal morphology related to timing of fetal sulcation and trans-sulcal gene expression gradients",

abstract = "We developed a computational pipeline (now provided as a resource) for measuring morphological similarity between cortical surface sulci to construct a sulcal phenotype network (SPN) from each magnetic resonance imaging (MRI) scan in an adult cohort (N=34,725; 45-82 years). Networks estimated from pairwise similarities of 40 sulci on 5 morphological metrics comprised two clusters of sulci, represented also by the bipolar distribution of sulci on a linear-to-complex dimension. Linear sulci were more heritable and typically located in unimodal cortex; complex sulci were less heritable and typically located in heteromodal cortex. Aligning these results with an independent fetal brain MRI cohort (N=228; 21-36 gestational weeks), we found that linear sulci formed earlier, and the earliest and latest-forming sulci had the least between-adult variation. Using high-resolution maps of cortical gene expression, we found that linear sulcation is mechanistically underpinned by trans-sulcal gene expression gradients enriched for developmental processes.",

author = "Snyder, {William E} and V{\'e}rtes, {Petra E.} and Vanessa Kyriakopoulou and Konrad Wagstyl and Williams, {Logan Z. J.} and Dustin Moraczewski and Thomas, {Adam G.} and Karolis, {Vyacheslav R.} and Jakob Seidlitz and Denis Rivi{\`e}re and Robinson, {Emma C.} and Jean-Francois Mangin and Armin Raznahan and Bullmore, {Edward T.}",

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doi = "10.1101/2023.12.19.572454",

language = "English",

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Snyder, WE, Vértes, PE, Kyriakopoulou, V, Wagstyl, K, Williams, LZJ, Moraczewski, D, Thomas, AG, Karolis, VR, Seidlitz, J, Rivière, D, Robinson, EC, Mangin, J-F, Raznahan, A & Bullmore, ET 2024 'A bipolar taxonomy of adult human brain sulcal morphology related to timing of fetal sulcation and trans-sulcal gene expression gradients' Neuron. https://doi.org/10.1101/2023.12.19.572454

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T1 - A bipolar taxonomy of adult human brain sulcal morphology related to timing of fetal sulcation and trans-sulcal gene expression gradients

AU - Snyder, William E

AU - Vértes, Petra E.

AU - Kyriakopoulou, Vanessa

AU - Wagstyl, Konrad

AU - Williams, Logan Z. J.

AU - Moraczewski, Dustin

AU - Thomas, Adam G.

AU - Karolis, Vyacheslav R.

AU - Seidlitz, Jakob

AU - Rivière, Denis

AU - Robinson, Emma C.

AU - Mangin, Jean-Francois

AU - Raznahan, Armin

AU - Bullmore, Edward T.

PY - 2024

Y1 - 2024

N2 - We developed a computational pipeline (now provided as a resource) for measuring morphological similarity between cortical surface sulci to construct a sulcal phenotype network (SPN) from each magnetic resonance imaging (MRI) scan in an adult cohort (N=34,725; 45-82 years). Networks estimated from pairwise similarities of 40 sulci on 5 morphological metrics comprised two clusters of sulci, represented also by the bipolar distribution of sulci on a linear-to-complex dimension. Linear sulci were more heritable and typically located in unimodal cortex; complex sulci were less heritable and typically located in heteromodal cortex. Aligning these results with an independent fetal brain MRI cohort (N=228; 21-36 gestational weeks), we found that linear sulci formed earlier, and the earliest and latest-forming sulci had the least between-adult variation. Using high-resolution maps of cortical gene expression, we found that linear sulcation is mechanistically underpinned by trans-sulcal gene expression gradients enriched for developmental processes.

AB - We developed a computational pipeline (now provided as a resource) for measuring morphological similarity between cortical surface sulci to construct a sulcal phenotype network (SPN) from each magnetic resonance imaging (MRI) scan in an adult cohort (N=34,725; 45-82 years). Networks estimated from pairwise similarities of 40 sulci on 5 morphological metrics comprised two clusters of sulci, represented also by the bipolar distribution of sulci on a linear-to-complex dimension. Linear sulci were more heritable and typically located in unimodal cortex; complex sulci were less heritable and typically located in heteromodal cortex. Aligning these results with an independent fetal brain MRI cohort (N=228; 21-36 gestational weeks), we found that linear sulci formed earlier, and the earliest and latest-forming sulci had the least between-adult variation. Using high-resolution maps of cortical gene expression, we found that linear sulcation is mechanistically underpinned by trans-sulcal gene expression gradients enriched for developmental processes.

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DO - 10.1101/2023.12.19.572454

M3 - Preprint

BT - A bipolar taxonomy of adult human brain sulcal morphology related to timing of fetal sulcation and trans-sulcal gene expression gradients

PB - Neuron

ER -

A bipolar taxonomy of adult human brain sulcal morphology related to timing of fetal sulcation and trans-sulcal gene expression gradients

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