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

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Ventura-Antunes, Lissa, Mota, Bruno, Herculano-Houzel, Suzana·2013·Frontiers in Neuroanatomy
DOI 10.3389/fnana.2013.00003PMC PMC3620553
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Abstract

Expansion of the cortical gray matter in evolution has been accompanied by an even faster expansion of the subcortical white matter volume and by folding of the gray matter surface, events traditionally considered to occur homogeneously across mammalian species. Here we investigate how white matter expansion and cortical folding scale across species of rodents and primates as the gray matter gains neurons. We find very different scaling rules of white matter expansion across the two orders, favoring volume conservation and smaller propagation times in primates. For a similar number of cortical neurons, primates have a smaller connectivity fraction and less white matter volume than rodents; moreover, as the cortex gains neurons, there is a much faster increase in white matter volume and in its ratio to gray matter volume in rodents than in primates. Order-specific scaling of the white matter can be attributed to different scaling of average fiber caliber and neuronal connectivity in rodents and primates. Finally, cortical folding increases as different functions of the number of cortical neurons in rodents and primates, scaling faster in the latter than in the former. While the neuronal rules that govern gray and white matter scaling are different across rodents and primates, we find that they can be explained by the same unifying model, with order-specific exponents. The different scaling of the white matter has implications for the scaling of propagation time and computational capacity in evolution, and calls for a reappraisal of developmental models of cortical expansion in evolution.

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Crossref · 10.3389/fnana.2013.00003

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Figures

Figure 1 Scaling of gray and white matter volumes (VG and VW, respectively) and total cortical volume (VG + W) in rodents (green) and primates (red). (A) Total cortical volume increases more steeply with increasing numbers of cortical neurons in rodents than in primates. (B) White matter volume increases as non-overlapping functions of gray matter volume in rodents and primates. (C) Gray matter volume increases faster with increasing numbers of cortical neurons in rodents than in primates. (D) White matter volume also increases faster with increasing numbers of cortical neurons in rodents than in primates. Each point represents one species. Power functions are plotted for each mammalian order with the respective 95% confidence intervals (dotted lines). Exponents are indicated.
Figure 1 Scaling of gray and white matter volumes (VG and VW, respectively) and total cortical volume (VG + W) in rodents (green) and primates (red). (A) Total cortical volume increases more steeply with increasing numbers of cortical neurons in rodents than in primates. (B) White matter volume increases as non-overlapping functions of gray matter volume in rodents and primates. (C) Gray matter volume increases faster with increasing numbers of cortical neurons in rodents than in primates. (D) White matter volume also increases faster with increasing numbers of cortical neurons in rodents than in primates. Each point represents one species. Power functions are plotted for each mammalian order with the respective 95% confidence intervals (dotted lines). Exponents are indicated.CC BY · PubMed Central
Figure 2 Scaling of average cortical thickness (A) and of average neuronal density (B) as a function of numbers of cortical neurons in rodents (green) and primates (red). Power functions, where the exponents are significant at the level of p < 0.05, are plotted for each mammalian order with the respective 95% confidence intervals (dotted lines). Exponents are indicated.
Figure 2 Scaling of average cortical thickness (A) and of average neuronal density (B) as a function of numbers of cortical neurons in rodents (green) and primates (red). Power functions, where the exponents are significant at the level of p < 0.05, are plotted for each mammalian order with the respective 95% confidence intervals (dotted lines). Exponents are indicated.CC BY · PubMed Central
Figure 3 Scaling of average number of neurons underneath 1 mm2 of cortical gray matter as a function of gray matter volume in rodents (green) and primates (red). The power function for rodents is plotted with the respective 95% confidence interval (dotted lines).
Figure 3 Scaling of average number of neurons underneath 1 mm2 of cortical gray matter as a function of gray matter volume in rodents (green) and primates (red). The power function for rodents is plotted with the respective 95% confidence interval (dotted lines).CC BY · PubMed Central
Figure 4 Scaling laws for the white matter. (A) White matter volume scales differently with increasing surface area of the white matter (AW) in rodents (green) than in primates (red). (B) White/gray matter volume ratio increases faster in rodents than in primates with increasing numbers of cortical neurons. (C) White matter volume scales faster with increasing numbers of other cells (OW, presumably mostly oligodendrocytes) in the white matter in rodents than in primates. (D) The number of other cells in the white matter increases much faster with increasing numbers of cortical neurons in rodents than in primates. Each point represents one species. Power functions are plotted for each mammalian order with the respective 95% confidence intervals (dotted lines). Exponents are indicated.
Figure 4 Scaling laws for the white matter. (A) White matter volume scales differently with increasing surface area of the white matter (AW) in rodents (green) than in primates (red). (B) White/gray matter volume ratio increases faster in rodents than in primates with increasing numbers of cortical neurons. (C) White matter volume scales faster with increasing numbers of other cells (OW, presumably mostly oligodendrocytes) in the white matter in rodents than in primates. (D) The number of other cells in the white matter increases much faster with increasing numbers of cortical neurons in rodents than in primates. Each point represents one species. Power functions are plotted for each mammalian order with the respective 95% confidence intervals (dotted lines). Exponents are indicated.CC BY · PubMed Central
Figure 5 Scaling of the connectivity fraction, n(A) and of average axonal caliber (B) as a function of numbers of cortical neurons in rodents (green) and primates (red). (A) n, a value proportional to the fraction of cortical neurons connected through the white matter, calculated as (AW/NG) × (OW/VW), is higher in rodents than in primates. (B) a, a value proportional to the average axonal caliber, calculated as the ratio VW/OW, is higher in primates than in rodents, but increases with number of cortical neurons in rodents to reach primate levels.
Figure 5 Scaling of the connectivity fraction, n(A) and of average axonal caliber (B) as a function of numbers of cortical neurons in rodents (green) and primates (red). (A) n, a value proportional to the fraction of cortical neurons connected through the white matter, calculated as (AW/NG) × (OW/VW), is higher in rodents than in primates. (B) a, a value proportional to the average axonal caliber, calculated as the ratio VW/OW, is higher in primates than in rodents, but increases with number of cortical neurons in rodents to reach primate levels.CC BY · PubMed Central
Figure 6 Scaling of the folding index of the gray matter (FG) as a function of gray matter volume (A), number of cortical neurons (B) and cortical thickness (C) in rodents (green) and primates (red). Each point represents one species. Power functions are plotted for each mammalian order with the respective 95% confidence intervals (dotted lines). Exponents are indicated.
Figure 6 Scaling of the folding index of the gray matter (FG) as a function of gray matter volume (A), number of cortical neurons (B) and cortical thickness (C) in rodents (green) and primates (red). Each point represents one species. Power functions are plotted for each mammalian order with the respective 95% confidence intervals (dotted lines). Exponents are indicated.CC BY · PubMed Central

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Research works printed but not linked: 2

  1. Le Gros Clark W. (1945). Deformation patterns on the cerebral cortex, in Essays on Growth and Form, eds Le Gros Clark W. E. Medawar P. B. (Oxford: Oxford University Press), 1– 23
  2. Welker W. (1990). Why does cerebral cortex fissure and fold? A review of determinants of gyri and sulci, in Cerebral Cortex, Comparative structure and evolution of cerebral cortex, part II, Vol. 8B, eds Jones E. G. Peters A. (New York, NY: Plenum Press), 3– 136

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Metadata

Authors
Ventura-Antunes, L., Mota, B., & Herculano-Houzel, S.
Affiliations
Universidade Federal do Rio de Janeiro (BR)
ORCID
Mota, Bruno
Venue
Frontiers in Neuroanatomy
Publisher
Frontiers Media SA
Published
2013
Volume
7
Pages
3-3
ISSN
1662-5129 (ISSN-L)
DOI
10.3389/fnana.2013.00003
PMC
PMC3620553
OpenAlex
W2044032178
Cited by
129
References
31
Citations by year
2026: 8 · 2025: 12 · 2024: 13 · 2023: 7 · 2022: 13 · 2021: 8 · 2020: 12 · 2019: 7 · 2018: 6 · 2017: 12 · 2016: 15 · 2015: 8 · 2014: 6 · 2013: 2
FWCI
8.02
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Neuroanatomy (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • James S. McDonnell Foundation
  • Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
  • Conselho Nacional de Desenvolvimento Científico e Tecnológico
  • Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro
Topics
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Primate Behavior and Ecology
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords
white matter volume, cortical folding, cortical connectivity, primate brain evolution, propagation time, cortical expansion, scaling exponents, brain evolution

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