Primate auditory prototype in the evolution of the arcuate fasciculus

Abstract

The human arcuate fasciculus pathway is crucial for language, interconnecting posterior temporal and inferior frontal areas. Whether a monkey homolog exists is controversial and the nature of human-specific specialization unclear. Using monkey, ape and human auditory functional fields and diffusion-weighted MRI, we identified homologous pathways originating from the auditory cortex. This discovery establishes a primate auditory prototype for the arcuate fasciculus, reveals an earlier phylogenetic origin and illuminates its remarkable transformation.

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Fig. 1: Existing view and evidence for monkey dorsal and ventral auditory pathways.
Fig. 2: Chimpanzee and human tractography of auditory dorsal and ventral pathways.
Fig. 3: Summary of auditory dorsal and ventral pathway strength and lateralization in macaques, chimpanzees and humans.

Data availability

The ultra-high resolution postmortem macaque dataset is from a previously shared resource. The chimpanzee and human datasets are from available resources (S500 group of the Human Connectome Project, http://www.chimpanzeebrain.org; the chimpanzee resource is available upon request and the NCBR staff are contacted via the main landing page). The awake macaque dMRI data is available from the Open Science Framework at https://osf.io/arqp8/ and will be made available at the PRIMatE MRI Data Exchange (https://fcon_1000.projects.nitrc.org/indi/indiPRIME.html). The ROIs are found in available atlases or as part of previous publications.

Code availability

Custom code and analyses were not required. Analysis pipelines used FSL (FDT v.6.0.1); other processing pipelines are as noted.

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Acknowledgements

We thank N. Eichert, R. Mars, A. Mitchell and M. Rushworth for their excellent discussion. This study was supported by the Wellcome Trust (grant no. WT091681MA to T.D.G., grant no. WT092606AIA to C.I.P. and grant no. WT110198 to B.W.); the Max Planck Society (to A.D.F. and A.A.); the European Research Council (MECHIDENT to C.I.P.); and the National Institutes of Health (Matthew Howard III with T.D.G. and C.I.P., grant no. R01-DC04290).

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Contributions

C.I.P., F.B., A.D.F. and T.D.G. conceived the study. F.B., B.W., G.G., F.D., A.A. and C.I.P. conducted the study and the analyses. F.B., B.W., G.G., F.D., W.H., A.A., A.D.F., T.D.G. and C.I.P. provided the materials. C.I.P., F.B. and B.W. wrote the paper with revisions from coauthors G.G., F.D., W.H., A.A., A.D.F. and T.D.G.

Corresponding authors

Correspondence to Fabien Balezeau or Benjamin Wilson or Christopher I. Petkov.

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The authors declare no competing interests.

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Peer review information Nature Neuroscience thanks Afonso Silva and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Macaque deterministic tractography.

Axial (left) and sagittal (right) slices showing diffusion weighted fractional anisotropy (FA) map overlaid with deterministic tractography. The sagittal slice shows the auditory pathways coursing to inferior frontal cortex via a ventral pathway medially involving the Uncinate Fasciculus/Extreme Capsule (UF/EC) pathway and laterally via the Middle Longitudinal Fasciculus (MdLF). No clear dorsal pathway from auditory cortex is observed using deterministic tractography. Diffusion directions, green: anterior-posterior; blue: dorsal-ventral; red: medial-lateral.

Extended Data Fig. 2 Lateral sulcus exclusion mask in the macaques.

To avoid artefactual dorsal pathway voxels not emanating from auditory cortex, an exclusion mask covering the full extent of the Sylvian fissure (lateral sulcus) separating the superior temporal plane and dorsal regions in frontal and parietal cortex was defined. Omission of this mask causes strong false positive dorsal pathways involvement because some auditory cortex voxels in the superior temporal plane are mislocalized to the dorsal lateral sulcus owing to partial volume effects. The lateral sulcus exclusion mask ensured that the analyses are more conservative with regards to spurious dorsal supra-temporal plane to inferior frontal cortex pathway connectivity.

Extended Data Fig. 3 Example comparison of probabilistic dMRI to a macaque fibre pathways atlas coronal section.

Comparison of one of the coronal slices (left) showing tractography from the MM seed region, with a similarly located coronal section (right) from the Schmahmann and Pandya macaque brain pathways atlas13 (copyright permission obtained from Oxford Publishing Limited), suggests that the dorsal pathways that we observed involve the macaque AF and parts of the Superior Longitudinal Fasciculus (SLF). SLF II/III: Superior Longitudinal Fasciculus II/III; AF: Arcuate Fasciculus; EC: Extreme Capsule pathway (Uncinate Fasciculus is visible on more anterior coronal sections); MdLF: Middle Longitudinal Fasciculus.

Extended Data Fig. 4 Mean relative connectivity heat maps for each macaque auditory cortical field.

Showing mean relative dorsal and ventral connectivity from each ACF (from Fig. 1e) rendered on the cortical surface for closer comparison with the human results (Fig. 2e).

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Balezeau, F., Wilson, B., Gallardo, G. et al. Primate auditory prototype in the evolution of the arcuate fasciculus. Nat Neurosci 23, 611–614 (2020). https://doi.org/10.1038/s41593-020-0623-9

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