Structural Variability Across the Primate Brain: A Cross-Species Comparison

Abstract

A large amount of variability exists across human brains; revealed initially on a small scale by postmortem studies and, more recently, on a larger scale with the advent of neuroimaging. Here we compared structural variability between human and macaque monkey brains using grey and white matter magnetic resonance imaging measures. The monkey brain was overall structurally as variable as the human brain, but variability had a distinct distribution pattern, with some key areas showing high variability. We also report the first evidence of a relationship between anatomical variability and evolutionary expansion in the primate brain. This suggests a relationship between variability and stability, where areas of low variability may have evolved less recently and have more stability, while areas of high variability may have evolved more recently and be less similar across individuals. We showed specific differences between the species in key areas, including the amount of hemispheric asymmetry in variability, which was left-lateralized in the human brain across several phylogenetically recent regions. This suggests that cerebral variability may be another useful measure for comparison between species and may add another dimension to our understanding of evolutionary mechanisms.

Figure 1.

Quantification of the variability. (a) T1 and FA maps templates computed for each species. Red indicated the mask used to calculate average deformation. (b) Average deformation measured for grey and white matter with standard deviations. The left panel indicates absolute values quantified using Euclidean distance. The right panel indicates relative values estimated by the Jacobian determinant.

Figure 2.

Grey matter variability. Three-dimensional projection of the average deformation measured for grey matter in humans (a) and monkeys (b). CS, central sulcus; POS, parieto-occipital sulcus; V1, striate cortex; V2, extra striate area 2; V3, extra striate area 3; V4, extra striate area 4; Cereb, cerebellum; VPC, ventral prefrontal cortex; RPC, rostral prefrontal cortex; LOS, lateral occipital sulcus; IPTa, inferior parietal tertiary association cortex; BA44, pars opercularis; FEF, frontal eye field; TPJ, temporo-parietal junction; aSTG, anterior superior temporal gyrus; STS, superior temporal sulcus. Note that since neither a functional nor microscopic delineation of the microscopically or functionally defined cortical areas has been performed in this research, the localization of the functional areas reported in this illustration is an estimate.

Figure 3.

White matter variability. Three-dimensional projection of the average deformation measured for white matter in humans (a) and monkeys (b). SLFs, branches of the superior longitudinal fasciculus; ATR, anterior thalamic radiation.

Figure 4.

Comparison between grey matter variability (a) and cortical folding (b) in humans. (c) Spearman rho correlations. Results are Bonferroni corrected for multiple comparisons.

Figure 5.

Comparison between grey matter variability in humans and macaque-to-human areal expansion (2). Correlations are shown for each of the major subdivisions of the brain. Spearman rho and P values shown. LH, left hemisphere; RH, right hemisphere. Results are Bonferroni corrected for multiple comparisons.

Figure 6.

Lateralization indices in grey matter variability in humans (left panel) and monkeys (right panel). Note that the scale for both species is different for visualization purposes. ant., anterior; mid., middle; med., medial; post., posterior; sup., superior; inf., inferior; l., lobule; g., gyrus; SMA, supplementary motor area; oper., opercularis; triang., triangularis. *P < 0.05; **P < 0.01; ***P < 0.001. Results are Bonferroni corrected for multiple comparisons.