The functional neuroanatomy of the left temporal lobe white matter – an interdisciplinary approach based on intraoperative and comparative studies.

Abstract

The left temporal lobe is claimed to be involved in language comprehension in both the classical (Wernicke, 1874) and contemporary dual-pathway models for language processing (Hickok & Poeppel, 2007, Roelofs, 2014), but the role of neuroanatomical subcomponents of this lobe in distinct facets of lexical-semantic processing has still not been fully uncovered. In the present work, we explore how the pMTG system changed in the evolution by comparing white matter dissections of humans and chimpanzees.
High resolution diffusion-weighted imaging (DWI) data for 50 healthy subjects (mean age=43.7±21.6 yrs) were acquired by Janssen et al. (in prep). Diffusion-weighted data from 29 chimpanzees (Pan troglodytes; 28 ± 17 yrs), were obtained from a data 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. Access to these scans was acquired through the US-based National Chimpanzee Brain Resource.
For human participants, two binary masks were defined within the Montreal Neurological Institute (MNI) space using SPM Marsbar extraction tool and AAL anatomical atlas: pMTG and the anterior temporal lobe (ATL; both for the left hemisphere). The ATL was used as a second, potential semantic node, following the ‘hub-and-spoke’ model (Ralph, Jefferies, Patterson, & Rogers, 2016). The pMTG mask was defined by restricting the middle temporal gyrus to its portion located posteriorly to the central sulcus (y=-18, Turken & Dronkers, 2011). The ATL mask was obtained by joining 5 parts: middle and superior temporal poles and the anterior portions of the inferior, middle and superior temporal gyri (terminating at y=-17, thus not overlapping with pMTG). Subsequently, the masks were transferred to each individual’s diffusion space and their corresponding white matter connections were calculated using a probabilistic approach (FSL probtrackx). All individual results were then warped to the MNI space and two unified outputs were calculated for the whole sample: the normalized mean, thresholded at 99% of the robust range, and the overlap of normalized and thresholded individual tractograms. In chimpanzees, masks were manually drawn to correspond to human cortical areas using homologous sulcal and gyral landmarks in chimpanzees, using recent sulcal/gyral maps for this species (Falk et al., 2018). All remaining steps were kept the same.
Visual inspection of the results revealed an extensive ventral system of white matter pathways (including IFOF) originating from the left ATL seed in both humans and chimpanzees. Importantly, the maps did not substantially differ between the two species. In humans, the probabilistic tracking from pMTG showed that the ventral white-matter system extends to both the right hemisphere via the tapetum and to the dorsal pathways for language via the connection between the posterior superior temporal sulcus and the inferior parietal lobe. In chimpanzees, this circuitry was similar with regard to the interhemispheric connections, but connectivity to the dorsal stream was less robust than in humans. Formal quantification of these (dis)similarities is currently ongoing.
Our results on the pMTG-related white-matter connections in humans confirmed the previous findings by Turken and Dronkers (2011). Furthermore, we extended the examination of these connections to another species, potentially confirming the uniqueness of the expansion towards the dorsal language stream in humans. Interestingly, the circuitry related to the ATL seed is similar between humans and chimpanzees, in both cases showing a connection with the IFOF. Together with the recent evidence on IFOF involvement in processing and integration of visual information for basic communication acts in vervet monkeys (Sarubbo et al., 2019), our results suggest that while the ATL/IFOF system may play a crucial role in conceptualization, it is the pMTG white matter circuitry that connects the ventral stream to the network related to phonological processing.
These findings also have important clinical implications. Our results add new evidence in support of the claim that the pMTG is a crucial node serving as a lexical interface. This implies that this region should be handled with particular caution in surgeries for removal of brain tumors or epileptic foci, and it could be key in understanding language recovery following brain injury.