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. 2023 Sep 1;21(9):e3002266.
doi: 10.1371/journal.pbio.3002266. eCollection 2023 Sep.

Morphological evolution of language-relevant brain areas

Guillermo Gallardo  1 , Cornelius Eichner  1 , Chet C Sherwood  2 , William D Hopkins  3 , Alfred Anwander  1 , Angela D Friederici  1
Affiliations

Morphological evolution of language-relevant brain areas

Guillermo Gallardo et al. PLoS Biol. .

Abstract

Human language is supported by a cortical network involving Broca's area, which comprises Brodmann Areas 44 and 45 (BA44 and 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 BA45 in 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 and receptorarchitectural studies, our findings support the conclusion that BA44 evolved from an action-related region to a bipartite system, with a posterior portion supporting action and an anterior portion supporting syntactic processes. Our findings add novel insights to the longstanding debate on the relationship between language and action, and the evolution of Broca's area.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 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. The underlying data can be found in the GitHub/Zotero repository, under the results/chimpanzee-atlas folder.
Fig 2
Fig 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 and colleagues [21] 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. The underlying data and scripts used can be found in the GitHub/Zotero repository, under the scripts/ and results/human-comparison folders.
Fig 3
Fig 3. Percentage of overlap between the chimpanzee BA44 and functional subdivisions of the human BA44 [,–38].
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 and colleagues [36] and Papitto and colleagues [17], except Clos 1, which was originally reported to be a syntax area, but further studies did not find to be involved in basic syntactic operations [36,37]. The underlying data and scripts used can be found in the GitHub/Zotero repository, under the scripts/ and results/human-comparison folders.
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Publication types

Grants and funding

This study was funded by the Max Planck Society under the inter-institutional funds of the president for the project “Evolution of Brain Connectivity (EBC)” to AF. This work was supported, in part, by NIH grants AG-067419, NS-092988, and NS- 42867 to WDH and CCS. All aspects of this research conformed to existing US and NIH federal policies on the ethical use of chimpanzees in research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.