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.
| Original language | English (US) |
|---|---|
| Pages (from-to) | 15253-15261 |
| Number of pages | 9 |
| Journal | Proceedings of the National Academy of Sciences of the United States of America |
| Volume | 116 |
| Issue number | 30 |
| DOIs | |
| State | Published - Jul 23 2019 |
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Keywords
- Brain size
- Cortical folding
- Evolution
- Scaling
- White matter
ASJC Scopus subject areas
- General
Cite this
White matter volume and white/gray matter ratio in mammalian species as a consequence of the universal scaling of cortical folding. / Mota, Bruno; Dos Santos, Sandra E.; Ventura-Antunes, Lissa; Jardim-Messeder, Débora; Neves, Kleber; Kazu, Rodrigo S.; Noctor, Stephen C; Lambert, Kelly; Bertelsen, Mads F.; Manger, Paul R.; Sherwood, Chet C.; Kaas, Jon H.; Herculano-Houzel, Suzana.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 116, No. 30, 23.07.2019, p. 15253-15261.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - White matter volume and white/gray matter ratio in mammalian species as a consequence of the universal scaling of cortical folding
AU - Mota, Bruno
AU - Dos Santos, Sandra E.
AU - Ventura-Antunes, Lissa
AU - Jardim-Messeder, Débora
AU - Neves, Kleber
AU - Kazu, Rodrigo S.
AU - Noctor, Stephen C
AU - Lambert, Kelly
AU - Bertelsen, Mads F.
AU - Manger, Paul R.
AU - Sherwood, Chet C.
AU - Kaas, Jon H.
AU - Herculano-Houzel, Suzana
PY - 2019/7/23
Y1 - 2019/7/23
N2 - 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.
AB - 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.
KW - Brain size
KW - Cortical folding
KW - Evolution
KW - Scaling
KW - White matter
UR - http://www.scopus.com/inward/record.url?scp=85069704227&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85069704227&partnerID=8YFLogxK
U2 - 10.1073/pnas.1716956116
DO - 10.1073/pnas.1716956116
M3 - Article
C2 - 31285343
AN - SCOPUS:85069704227
VL - 116
SP - 15253
EP - 15261
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
SN - 0027-8424
IS - 30
ER -