Continuity, divergence, and the evolution of brain language pathways

Abstract

Recently, the assumption of evolutionary continuity between humans and non-human primates has been used to bolster the hypothesis that human language is mediated especially by the ventral extreme capsule pathway that mediates auditory object recognition in macaques. Here, we argue for the importance of evolutionary divergence in understanding brain language evolution. We present new comparative data reinforcing our previous conclusion that the dorsal arcuate fasciculus pathway was more significantly modified than the ventral extreme capsule pathway in human evolution. Twenty-six adult human and twenty-six adult chimpanzees were imaged with diffusion-weighted MRI and probabilistic tractography was used to track and compare the dorsal and ventral language pathways. Based on these and other data, we argue that the arcuate fasciculus is likely to be the pathway most essential for higher-order aspects of human language such as syntax and lexical-semantics.

Keywords: arcuate fasciculus; brain; chimpanzee; evolution; extreme capsule; language.

Figure 1

(A–D) Group average left dorsal, right dorsal, left ventral, and right ventral pathways of 26 humans. (E) Left (y = −3 mm) and right (y = 0 mm) dorsal and ventral pathways in coronal slices; dorsal pathway is yellow–red, ventral pathway is light blue–blue. (F–I) Group average left dorsal, right dorsal, left ventral, and right ventral pathways of 26 chimpanzees. (J) Left and right (both y = −2.4 mm) dorsal and ventral pathways in coronal slices. Surface ROIs are displayed as white outlines. Fascicle selection ROIs are displayed as a translucent white layer over the pathways. For surface results, the scale is 0 (clear) to 30 (red) streamlines, for the volume results, the scale is 5 (clear) to 300 (yellow or light blue) streamlines.

Figure 2

Location of arcuate (yellow–orange) and inferior longitudinal fasciculi (ILF, blue) in (A,B) humans and (C,D) chimpanzees as revealed by diffusion tractography. Coronal sections for each species are at the posterior aspect of the splenium (see mid-sagittal insets). Tracts include voxels in which 33% or more subjects have a pathway above threshold (0.1% of waytotal). The black lines indicate the angle of the ILF in humans and chimpanzees. The white dotted line in (A) shows the angle of the ILF of chimps overlaid on the human color FA map. In humans, the arcuate appears to have displaced the ILF in a ventromedial direction.