Literature DB >> 31285343

White matter volume and white/gray matter ratio in mammalian species as a consequence of the universal scaling of cortical folding.

Bruno Mota1, Sandra E Dos Santos2, Lissa Ventura-Antunes2, Débora Jardim-Messeder3, Kleber Neves3, Rodrigo S Kazu3,4, Stephen Noctor5, Kelly Lambert6, Mads F Bertelsen7, Paul R Manger8, Chet C Sherwood9,10, Jon H Kaas11, Suzana Herculano-Houzel11,12,13.   

Abstract

Because the white matter of the cerebral cortex contains axons that connect distant neurons in the cortical gray matter, the relationship between the volumes of the 2 cortical compartments is key for information transmission in the brain. It has been suggested that the volume of the white matter scales universally as a function of the volume of the gray matter across mammalian species, as would be expected if a global principle of wiring minimization applied. Using a systematic analysis across several mammalian clades, here we show that the volume of the white matter does not scale universally with the volume of the gray matter across mammals and is not optimized for wiring minimization. Instead, the ratio between volumes of gray and white matter is universally predicted by the same equation that predicts the degree of folding of the cerebral cortex, given the clade-specific scaling of cortical thickness, such that the volume of the gray matter (or the ratio of gray to total cortical volumes) divided by the square root of cortical thickness is a universal function of total cortical volume, regardless of the number of cortical neurons. Thus, the very mechanism that we propose to generate cortical folding also results in compactness of the white matter to a predictable degree across a wide variety of mammalian species.

Entities:  

Keywords:  brain size; cortical folding; evolution; scaling; white matter

Year:  2019        PMID: 31285343      PMCID: PMC6660724          DOI: 10.1073/pnas.1716956116

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  27 in total

1.  Wiring optimization in cortical circuits.

Authors:  Dmitri B Chklovskii; Thomas Schikorski; Charles F Stevens
Journal:  Neuron       Date:  2002-04-25       Impact factor: 17.173

2.  Connectivity-driven white matter scaling and folding in primate cerebral cortex.

Authors:  Suzana Herculano-Houzel; Bruno Mota; Peiyan Wong; Jon H Kaas
Journal:  Proc Natl Acad Sci U S A       Date:  2010-10-18       Impact factor: 11.205

3.  Cellular scaling rules for the brains of an extended number of primate species.

Authors:  Mariana Gabi; Christine E Collins; Peiyan Wong; Laila B Torres; Jon H Kaas; Suzana Herculano-Houzel
Journal:  Brain Behav Evol       Date:  2010-09-30       Impact factor: 1.808

4.  Isotropic fractionator: a simple, rapid method for the quantification of total cell and neuron numbers in the brain.

Authors:  Suzana Herculano-Houzel; Roberto Lent
Journal:  J Neurosci       Date:  2005-03-09       Impact factor: 6.167

5.  Cellular scaling rules for primate brains.

Authors:  Suzana Herculano-Houzel; Christine E Collins; Peiyan Wong; Jon H Kaas
Journal:  Proc Natl Acad Sci U S A       Date:  2007-02-20       Impact factor: 11.205

6.  A universal scaling law between gray matter and white matter of cerebral cortex.

Authors:  K Zhang; T J Sejnowski
Journal:  Proc Natl Acad Sci U S A       Date:  2000-05-09       Impact factor: 11.205

7.  Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain.

Authors:  Frederico A C Azevedo; Ludmila R B Carvalho; Lea T Grinberg; José Marcelo Farfel; Renata E L Ferretti; Renata E P Leite; Wilson Jacob Filho; Roberto Lent; Suzana Herculano-Houzel
Journal:  J Comp Neurol       Date:  2009-04-10       Impact factor: 3.215

8.  How the cortex gets its folds: an inside-out, connectivity-driven model for the scaling of Mammalian cortical folding.

Authors:  Bruno Mota; Suzana Herculano-Houzel
Journal:  Front Neuroanat       Date:  2012-02-02       Impact factor: 3.856

9.  Segregation of the brain into gray and white matter: a design minimizing conduction delays.

Authors:  Quan Wen; Dmitri B Chklovskii
Journal:  PLoS Comput Biol       Date:  2005-12-30       Impact factor: 4.475

10.  Different scaling of white matter volume, cortical connectivity, and gyrification across rodent and primate brains.

Authors:  Lissa Ventura-Antunes; Bruno Mota; Suzana Herculano-Houzel
Journal:  Front Neuroanat       Date:  2013-04-09       Impact factor: 3.856

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  9 in total

1.  Cerebral cortical folding, parcellation, and connectivity in humans, nonhuman primates, and mice.

Authors:  David C Van Essen; Chad J Donahue; Timothy S Coalson; Henry Kennedy; Takuya Hayashi; Matthew F Glasser
Journal:  Proc Natl Acad Sci U S A       Date:  2019-12-23       Impact factor: 11.205

Review 2.  Neuroprotection and neuroregeneration: roles for the white matter.

Authors:  Vito Antonio Baldassarro; Agnese Stanzani; Luciana Giardino; Laura Calzà; Luca Lorenzini
Journal:  Neural Regen Res       Date:  2022-11       Impact factor: 6.058

3.  Scaling Principles of White Matter Connectivity in the Human and Nonhuman Primate Brain.

Authors:  Dirk Jan Ardesch; Lianne H Scholtens; Siemon C de Lange; Lea Roumazeilles; Alexandre A Khrapitchev; Todd M Preuss; James K Rilling; Rogier B Mars; Martijn P van den Heuvel
Journal:  Cereb Cortex       Date:  2022-06-16       Impact factor: 4.861

4.  Constant neuropilar ratio in the insect brain.

Authors:  Alexey A Polilov; Anastasia A Makarova
Journal:  Sci Rep       Date:  2020-12-08       Impact factor: 4.379

5.  Segmentation of Cerebral Small Vessel Diseases-White Matter Hyperintensities Based on a Deep Learning System.

Authors:  Wei Shan; Yunyun Duan; Yu Zheng; Zhenzhou Wu; Shang Wei Chan; Qun Wang; Peiyi Gao; Yaou Liu; Kunlun He; Yongjun Wang
Journal:  Front Med (Lausanne)       Date:  2021-11-25

6.  Short- and Long-Range Connections Differentially Modulate the Dynamics and State of Small-World Networks.

Authors:  Simon Arvin; Andreas Nørgaard Glud; Keisuke Yonehara
Journal:  Front Comput Neurosci       Date:  2022-01-25       Impact factor: 2.380

7.  Establishing a Baseline for Human Cortical Folding Morphological Variables: A Multisite Study.

Authors:  Fernanda H P de Moraes; Victor B B Mello; Fernanda Tovar-Moll; Bruno Mota
Journal:  Front Neurosci       Date:  2022-07-18       Impact factor: 5.152

8.  Regional White Matter Scaling in the Human Brain.

Authors:  Allysa Warling; Cassidy L McDermott; Siyuan Liu; Jakob Seidlitz; Amanda L Rodrigue; Ajay Nadig; Ruben C Gur; Raquel E Gur; David Roalf; Tyler M Moore; David Glahn; Theodore D Satterthwaite; Edward T Bullmore; Armin Raznahan
Journal:  J Neurosci       Date:  2021-07-09       Impact factor: 6.167

9.  Structural Attributes and Principles of the Neocortical Connectome in the Marmoset Monkey.

Authors:  Panagiota Theodoni; Piotr Majka; David H Reser; Daniel K Wójcik; Marcello G P Rosa; Xiao-Jing Wang
Journal:  Cereb Cortex       Date:  2021-11-23       Impact factor: 4.861

  9 in total

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