What is special about the human arcuate fasciculus? Lateralization, projections, and expansion

Abstract

Evolutionary adaptations of the human brain are the basis for our unique abilities such as language. An expansion of the arcuate fasciculus (AF), the dorsal language tract, in the human lineage involving left lateralization is considered canonical, but this hypothesis has not been tested in relation to other architectural adaptations in the human brain. Using diffusion-weighted MRI, we examined AF in the human and macaque and quantified species differences in white matter architecture and surface representations. To compare surface results in the two species, we transformed macaque representations to human space using a landmark-based monkey-to-human cortical expansion model. We found that the human dorsal AF, but not the ventral inferior fronto-occipital fasciculus (IFO), is left-lateralized. In the monkey AF is not lateralized. Moreover, compared to the macaque, human AF is relatively increased with respect to IFO. A comparison of human and transformed macaque surface representations suggests that cortical expansion alone cannot account for the species differences in the surface representation of AF. Our results show that the human AF has undergone critical anatomical modifications in comparison with the macaque AF. More generally, this work demonstrates that studies on the human brain specializations underlying the language connectome can benefit from current methodological advances in comparative neuroanatomy.

XTRACT - Standardised protocols for automated tractography in the human and macaque brain

“…We compared our lateralisation results to a priori knowledge from the literature. For both human cohorts (HCP and UK Biobank), we found that reconstructed AF is strongly left-lateralised, while SLF3, IFO and MDLF were right-lateralised, as expected from the literature (Eichert et al, 2019b;Hau et al, 2016;Hecht et al, 2015;Nowell et al, 2016;Panesar et al, 2018;Thiebaut de Schotten et al, 2011a;Zhao et al, 2016). Results were less clear-cut for SLF1 and SLF2, where prior studies (with much fewer numbers of subjects) are inconclusive (Hecht et al, 2015;Howells et al, 2018;Thiebaut de Schotten et al, 2011a).…”

“…In order to demonstrate whether our protocols produce tracts representative of the anatomical expectations, we investigate tract lateralisation using a large number of subjects. Based on the literature, it is expected that AF is left-lateralised (Eichert et al, 2019b;Nowell et al, 2016;Panesar et al, 2018), IFO, MdLF and SLF3 are right-lateralised (Hau et al, 2016;Howells et al, 2018;Menjot de Champfleur et al, 2013;Thiebaut de Schotten et al, 2011a;Zhao et al, 2016), while SLF1 is expected to be non-lateralised (Thiebaut de Schotten et al, 2011a). The literature suggests that the SLF2 is right-lateralised, however, findings are less conclusive as in some cases the reported lateralisation does not reach significance (Hecht et al, 2015;Thiebaut de Schotten et al, 2011a).…”

“…An additional axial plane was placed in the IFG. This protocol was validated by (Eichert et al, 2019b).…”

Cross-species cortical alignment identifies different types of neuroanatomical reorganization in the temporal lobe of higher primates

“…Ex vivo DW-MRI data were obtained from four rhesus macaques (one female, age at death: range 4-14 years) using a 7T magnet. Data acquisition and DW-MRI pre-processing have been previously described in detail (Eichert et al, 2019). Data were acquired using a 2D diffusionweighted spin echo multi slice protocol with single line readout (DW-SEMS; TE = 25 ms; TR = 10 s; matrix size: 128 x 128; resolution 0.6 mm; number of slices: 128; slice thickness: 0.6 mm).…”

“…Such an approach allows us to place different brains into a common space based on one feature and then compare the results to registration based on another feature. This 'common space' concept proved feasible in a previous study testing whether the extension of the human arcuate fasciculus (AF) compared with the macaque AF could be accounted for by differential cortical expansion between the two brains (Eichert et al, 2019). In the present study, we generalize this approach to develop a cross-species registration based on a multimodal surface matching algorithm (MSM, Robinson et al, 2018Robinson et al, , 2014Robinson et al, , 2013 to derive a cortical registration between different species.…”