Comparing human and chimpanzee temporal lobe neuroanatomy reveals modifications to human language hubs beyond the frontotemporal arcuate fasciculus

Abstract

The biological foundation for the language-ready brain in the human lineage remains a debated subject. In humans, the arcuate fasciculus (AF) white matter and the posterior portions of the middle temporal gyrus are crucial for language. Compared with other primates, the human AF has been shown to dramatically extend into the posterior temporal lobe, which forms the basis of a number of models of the structural connectivity basis of language. Recent advances in both language research and comparative neuroimaging invite a reassessment of the anatomical differences in language streams between humans and our closest relatives. Here, we show that posterior temporal connectivity via the AF in humans compared with chimpanzees is expanded in terms of its connectivity not just to the ventral frontal cortex but also to the parietal cortex. At the same time, posterior temporal regions connect more strongly to the ventral white matter in chimpanzees as opposed to humans. This pattern is present in both brain hemispheres. Additionally, we show that the anterior temporal lobe harbors a combination of connections present in both species through the inferior fronto-occipital fascicle and human-unique expansions through the uncinate and middle and inferior longitudinal fascicles. These findings elucidate structural changes that are unique to humans and may underlie the anatomical foundations for full-fledged language capacity.

Human temporal lobes have been reorganized: A response to Pearson et al, “updated imaging and phylogenetic comparative methods reassess relative temporal lobe size in anthropoids and modern humans”

“…This specialization of the human temporal lobe has been replicated by other research groups (Balezeau et al, 2020;Eichert et al, 2019;Eichert et al, 2020). However, specializations of the human temporal lobe white matter now appear to extend beyond the arcuate fasciculus to other temporal lobe fiber tracts such as the uncinate fasciculus and the middle and inferior longitudinal fascicles, as well as temporal lobe connections with the parietal lobe that may be involved with tool use and imitation (Braunsdorf et al, 2021;Hecht et al, 2013;Ramayya et al, 2010;Sierpowska et al, 2022).…”

Cross-species alignment along the chronological axis reveals evolutionary effect on structural development of human brain

“…Advances in diffusion tensor imaging allow direct quantification of microstructure of fiber tracts, anatomical connectivity strength between brain areas and complex network organization between humans and NHPs. The increased myelination and fiber connections of arcuate fasciculus for language processing have been consistently found in humans compared to NHPs (Balezeau et al, 2020b; Eichert et al, 2019; Rilling et al, 2008; Sierpowska et al, 2022). Complex network analysis based on macroscale structural connectivity network revealed different network hubs, common and unique wiring properties of the human brain (Goulas et al, 2014; Li et al, 2013).…”

“…The increased myelination and fiber connections of arcuate fasciculus for language processing have been consistently found in humans compared to NHPs (Balezeau et al, 2020b;Eichert et al, 2019;Rilling et al, 2008;Sierpowska et al, 2022). Complex network analysis based on macroscale structural connectivity network revealed different network hubs, common and unique wiring properties of the human brain (Goulas et al, 2014;Li et al, 2013).…”