The diversity of the cortical morphologies and developmental processes across species.

(a) Phylogenetic relationship of species. Adapted from Takahata et al. (2012); Heuer et al. (2019). Typical real brain surfaces of ferret and primates are presented. Color represents mean curvature. Scale bars: 1 cm (estimated from Herculano-Houzel (2009)). (b) Stained sections of mature brain tissue from ferret, rhesus macaque, and human. Scale bar: 10 mm. Adapted from Rea (2016). (c-e) 3D reconstruction of cortical surfaces of ferret, macaque, and human brains from fetal to adult. (c) Ferret: postnatal day 4, 10, 17 and adult maturation Barnette et al. (2009). Scale bar: 1cm; (d) Macaque: gestation day 85, 110, 135 Liu et al. (2020), and adult maturation Calabrese et al. (2015). Scale bar: 1cm; (e) Human: gestation day 175 (week 25), 210 (week 30), 231 (week 33), 273 (week 39), and adult maturation Barnette et al. (2009). Scale bar: 5cm.

Physical gel model that recapitulates the growth-driven morphogenesis mechanism across phylogeny and developmental stages.

(a) A time-lapse of the physical gel brain mimicking macaque brain development starting from G110. (b) Left views of three physical gels mimicking macaque post gestation day 85, day 110, and day 135 before and after hexane swelling. Scale bar: 1 cm. (c) Comparison of fetal/newborn brain scans and the reconstructed surfaces of swollen physical gels for various species. Scale bars: 1 cm.

Simulations of growing brains of (a) ferret, (b) rhesus macaque, and (c) human.

Starting from smooth fetal/newborn brains, simulations show different gyrification patterns across species. The brains are modeled as soft elastic solids with tangential growth in the gray matter (see Simulations of growing brains for details). Initial 3D geometries are taken from the reconstruction of MRI (see Methods, 3D model reconstruction). Mechanical parameters of growth ratio and cortical thickness are provided in Table 2. Color from dark to light blue represents shape index (as defined in Eq. (2)) from −1 to 1.

Comparison among real (𝒮1), simulated (𝒮2), and gel brains (𝒮3) of ferret, rhesus macaque, and human via morphometric analysis.

(a) 3D cortical surfaces of in vivo, in vitro and in silico models. Left brain surfaces are provided here. The symmetry of the left and right halves of the brain surfaces is discussed in Figs. S3 and S4, Movie S2–S4. Three or four major folds of each brain model are highlighted and served as landmarks. The occipital pole region of macaque brains remains smooth in real and simulated brains. (b) The quasi-conformal disk mapping with landmark matching of cortical surfaces on disk (see Sec Morphometric analysis for details). Blue or red curves represent corresponding landmarks. Color represents shape index (SI, as defined in Eq. (2)). Similarity indices of each simulated and gel brain surfaces are presented in Table 1. (c) Histogram of shape index of ferret, macaque, and human. Black, red, and blue dots represent the probability of shape index of real, gel, and simulated surfaces, respectively.

Similarity index evaluated by comparing the shape index of simulated brains (S), swollen gel brain simulacrums (G) and real brain surfaces (R), calculated with vector p-norm p = 2, as described in Eq. (4).

Parameters for numerical simulations.

Gene-related brain properties and malformation.

Similarity index (main text, Eq.(4)) evaluated by rescaled mean curvature of simulated and gel brain surfaces with comparison to the real brain surfaces, calculated with different vector p-norm: p = 1, p = 2, and p = .

(a) MRI scans showing common malformations of cortical development of human brains. Adapted from (15) with permission. Left: normal brain. Middle: lissencephaly spectrum with agyria–severe pachygyria (arrows). Right: bilateral frontoparietal polymicrogyria with abnormally small gyri and shallow sulci (arrows). Scale bars: 3 cm (estimated from (14)). (b) A noncoding mutation in the GPR56 gene disrupts perisylvian gyri. MRI shows polymicrogyria in the perisylvian area, resulting in a characteristic, thickened appearance. Adapted from (1) with permission.

Illustration of shape index scale divided into nine categories: spherical cup, trough rut, saddle rut, saddle, saddle ridge, ridge, dome and spherical cap. The insets are schematics of local curved surfaces. All outward normals pointing upwards.

The histogram of shape index SI (top two rows) and rescaled mean curvature (bottom two rows) of adult cortical surfaces of ferret, macaque and human. Insets are real brain surfaces. Colors represent shape index SI (Eq. (2) in the main text) or rescaled mean curvature (Eq. (3) in the main text).

Comparison among real (𝒮 1), simulated (𝒮 2), and gel brains (𝒮 3) of ferret, rhesus macaque, and human via morphometric analysis.

(a) 3D cortical surfaces of in vivo, in silico, and in vitro models. Both left and right cortical surfaces are provided to present the left-right symmetry. (b) The quasi-conformal disk mapping with landmark matching of cortical surfaces on disk. Blue or red curves represent corresponding landmarks. Color represents shape index (SI). Similarity indices of each simulated and gel brain surfaces are presented in Table S2.

Comparison across ten primate species.

Each species is listed by its common name and scientific name, and accompanied by a picture. Scale bar: 1cm. Color represents the shape index. Pictures are taken from Wikipedia.