Left temporal lobe language hubs – a comparative approach

Abstract

The left temporal lobe is a major brain structure involved in language. Non-human primates, such as chimpanzees and bonobos, have language-like abilities and it has been argued that modifications to temporal lobe connectivity might have enabled semantic processing that later evolved into a highly complex language in humans. Previous studies have suggested that the posterior middle temporal gyrus (pMTG) may represent a crucial hub in lexical-semantic processing. For example, it has been repeatedly shown as involved in semantic learning and argued to function as a lexical interface (Rodríguez-Fornells et al., 2009). Anatomically, it serves as a cortical termination for an extensive number of white-matter pathways from both dorsal and ventral streams (Turken & Dronkers, 2011). However, it is unknown if the pattern of connectivity of this region is unique to humans. In the present work, we explore how the pMTG system changed in evolution by comparing white-matter tractograms of humans and chimpanzees. Additionally, the anterior temporal lobe (ATL) was examined as a second semantic node (‘hub-and-spoke’ model; Lambon Ralph et al., 2016). High-resolution diffusion-weighted images (DWI) were obtained from 50 humans (Janssen et al. submitted) and 29 chimpanzees (Pan troglodytes, from an archive of scans obtained prior to the 2015 implementation of U.S. Fish and Wildlife Service and National Institutes of Health regulations governing research with chimpanzees, Bryant et al., 2020). In humans, ATL and pMTG regions of interest (ROIs) were extracted from the AAL anatomical atlas; for the chimpanzees, these ROIs were adapted accordingly. Then, in both species, FSL Probtrackx probabilistic tractography was applied to DWIs to define the extent of white matter converging towards these ROIs. Finally, these maps were compared to the distribution of canonical language-related white-matter tracts in a quantitative manner. The probabilistic tracking originating from ATL revealed an extensive system of pathways formed by the ventral white-matter streams in both humans and chimpanzees. Probabilistic tracking stemming from the pMTG seed in humans showed that the ventral system extends to the dorsal pathways for language via the connection with the inferior parietal lobe. In chimpanzees, the connectivity to the dorsal stream was comparatively less robust. Quantification of these interspecies (dis)similarities indicated that the pMTG difference in connectivity was mainly explained by how this circuitry connects towards the dorsal pathways for language (up to 83% of interspecies variability explained by the connection vía the temporoparietal connection of the arcuate fasciculus, p<.001). By contrast, for the ATL, the interspecies difference was explained by the connectivity towards the ventral pathways for language (up to 90% by left inferior longitudinal fasciculus, p<.001). Our results on the pMTG connectivity highlight the uniqueness of the expansion towards the dorsal language stream. Interestingly, the circuitry related to the ATL is similar between humans and chimpanzees, in both cases showing a robust connection with the IFOF. While the ATL/IFOF system may play a crucial role in conceptualization (Sarubbo et al., 2019), we suggest that the cortical area enabling a connection from the ventral towards the dorsal (phonological) language networks in humans lies in pMTG.

Publication
Poster presentation at SNL 2020
Nikki Janssen
Nikki Janssen
PhD candidate

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