Uncovering the Morphological Evolution of Language-Relevant Brain Areas

Abstract

Human language is supported by a cortical network involving Broca's area which comprises Brodmann Areas 44 and 45 (BA44, BA45). While cytoarchitectonic homolog areas have been identified in nonhuman primates, it remains unknown how these regions evolved to support human language. Here, we use histological data and advanced cortical registration methods to precisely compare the morphology of BA44 and 45 between humans and chimpanzees. We found a general expansion of Broca's areas in humans, with the left BA44 enlarging the most, growing anteriorly into a region known to process syntax. Together with recent functional studies, our findings show that BA44 evolved from a purely action-related region to a more expanded region in humans, with a posterior portion supporting action and an anterior portion supporting syntactic processes. Furthermore, our findings provide a solution for the longstanding debate concerning the structural and functional evolution of Broca's area and its role in action and language.

Figure 1.

(A) Reconstruction pipeline for the cytoarchitectonic surface maps. First, the raw MRI data were cleaned using noise reduction and contrast inversion. Next, the individual surfaces were reconstructed in FreeSurfer. The individual maps of BA44 and BA45 are displayed in black and yellow, respectively. Finally, the individual surfaces and cytoarchitectural maps were registered to the JUNA template surface (B) Probabilistic atlas of regions BA44 and BA45 in the chimpanzee brain, derived from the individual maps, alongside the lateralization index for each individual brain.

Figure 2.

(A) Two-step surface registration, in the first step we align gross anatomical landmarks. This first alignment is then used to start a more granular one, based on sulcal depth. (B) Side-by-side comparison of our chimpanzee probabilistic atlas with the human population overlap of Amunts et al. [15] in the human brain template. Left BA44 is the area that grew the most and shows a large anterior expansion which is not present in Right BA44.

Figure 3.

Percentage of overlap between the chimpanzee BA44 and functional subdivisions of the human BA44 [,–28]. Action-related regions present the highest overlap with action-related areas and virtually no overlap with the syntax area. The chimpanzee BA44 atlas was thresholded at 0.5 to maintain only its core area. The functions being reported are those with the highest P (Activation | Domain) as reported by Clos et al. [26] and Papitto et al. [12], excepting Clos 1, which was originally reported to be a syntax area, but further studies did not find to be involved in basic syntactic operations [26,27].