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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

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.

References

  1. 1.

    Hagoort, P. The neurobiology of language beyond single-word processing. Science 366, 55–58 (2019).

    CAS  Article  Google Scholar 

  2. 2.

    Anwander, A., Tittgemeyer, M., von Cramon, D. Y., Friederici, A. D. & Knösche, T. R. Connectivity-based parcellation of Broca’s area. Cereb. Cortex 17, 816–825 (2007).

    CAS  Article  Google Scholar 

  3. 3.

    Price, C. J., Seghier, M. L. & Leff, A. P. Predicting language outcome and recovery after stroke: the PLORAS system. Nat. Rev. Neurol. 6, 202–210 (2010).

    Article  Google Scholar 

  4. 4.

    Bornkessel-Schlesewsky, I., Schlesewsky, M., Small, S. L. & Rauschecker, J. P. Neurobiological roots of language in primate audition: common computational properties.Trends Cogn. Sci. 19, 142–150 (2015).

    Article  Google Scholar 

  5. 5.

    Skeide, M. A. & Friederici, A. D. Response to Bornkessel-Schlesewsky et al.—Towards a nonhuman primate model of language? Trends Cogn. Sci. 19, 483 (2015).

    Article  Google Scholar 

  6. 6.

    Thiebaut de Schotten, M., Dell’Acqua, F., Valabregue, R. & Catani, M. Monkey to human comparative anatomy of the frontal lobe association tracts. Cortex 48, 82–96 (2012).

    Article  Google Scholar 

  7. 7.

    Rilling, J. K. et al. The evolution of the arcuate fasciculus revealed with comparative DTI. Nat. Neurosci. 11, 426–428 (2008).

    CAS  Article  Google Scholar 

  8. 8.

    Eichert, N. et al. What is special about the human arcuate fasciculus? Lateralization, projections, and expansion. Cortex 118, 107–115 (2019).

    Article  Google Scholar 

  9. 9.

    Frey, S., Mackey, S. & Petrides, M. Cortico-cortical connections of areas 44 and 45B in the macaque monkey. Brain Lang. 131, 36–55 (2014).

    Article  Google Scholar 

  10. 10.

    Rilling, J., Glasser, M. F., Jbabdi, S., Andersson, J. & Preuss, T. M. Continuity, divergence, and the evolution of brain language pathways. Front. Evol. Neurosci. 3, 11 (2012).

    Article  Google Scholar 

  11. 11.

    Mars, R. B., Eichert, N., Jbabdi, S., Verhagen, L. & Rushworth, M. F. S. Connectivity and the search for specializations in the language-capable brain. Curr. Opin. Behav. Sci. 21, 19–26 (2018).

    Article  Google Scholar 

  12. 12.

    Calabrese, E. et al. A diffusion tensor MRI atlas of the postmortem rhesus macaque Brain. Neuroimage 117, 408–416 (2015).

    Article  Google Scholar 

  13. 13.

    Schmahmann J. D. & Pandya D. N. Fiber Pathways of the Brain (Oxford Univ. Press, 2009).

  14. 14.

    Bailey, P., Von Bonin, G., Garol, H. W. & McCulloch, W. S. Functional organization of temporal lobe of monkey (Macaca mulatta) and chimpanzee (Pan satyrus). J. Neurophysiol. 6, 121–128 (1943).

    Article  Google Scholar 

  15. 15.

    Takaya, S. et al. Asymmetric projections of the arcuate fasciculus to the temporal cortex underlie lateralized language function in the human brain. Front. Neuroanat. 9, 119 (2015).

    Article  Google Scholar 

  16. 16.

    Romanski, L. M. et al. Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat. Neurosci. 2, 1131–1136 (1999).

    CAS  Article  Google Scholar 

  17. 17.

    Rauschecker, J. P. & Scott, S. K. Maps and streams in the auditory cortex: nonhuman primates illuminate human speech processing. Nat. Neurosci. 12, 718–724 (2009).

    CAS  Article  Google Scholar 

  18. 18.

    Zhang, Y. S. & Ghazanfar, A. A. A hierarchy of autonomous systems for vocal production. Trends Neurosci. 43, P115–P126 (2020).

    Article  Google Scholar 

  19. 19.

    Wilson, B. et al. Auditory sequence processing reveals evolutionarily conserved regions of frontal cortex in macaques and humans. Nat. Commun. 6, 8901 (2015).

    CAS  Article  Google Scholar 

  20. 20.

    Flinker, A. & Knight, R. T. Broca’s area in comprehension and production, insights from intracranial studies in humans. Curr. Opin. Behav. Sci. 21, 170–175 (2018).

    Article  Google Scholar 

  21. 21.

    Petkov, C. I., Kayser, C., Augath, M. & Logothetis, N. K. Functional imaging reveals numerous fields in the monkey auditory cortex. PLoS Biol. 4, e215 (2006).

    Article  Google Scholar 

  22. 22.

    Baumann, S. et al. Characterisation of the BOLD response time course at different levels of the auditory pathway in non-human primates. Neuroimage 50, 1099–1108 (2010).

    Article  Google Scholar 

  23. 23.

    van Essen, D. C. et al. The Human Connectome Project: a data acquisition perspective. Neuroimage 62, 2222–2231 (2012).

    CAS  Article  Google Scholar 

  24. 24.

    Dick, F. et al. In vivo functional and myeloarchitectonic mapping of human primary auditory areas. J. Neurosci. 32, 16095–16105 (2012).

    CAS  Article  Google Scholar 

  25. 25.

    Smith, S. M. et al. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23, S208–S219 (2004).

    Article  Google Scholar 

  26. 26.

    Behrens, T. E. J. et al. Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn. Reson. Med. 50, 1077–1088 (2003).

    CAS  Article  Google Scholar 

  27. 27.

    Zhang, Y., Brady, M. & Smith, S. Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans. Med. Imaging 20, 45–57 (2001).

    CAS  Article  Google Scholar 

  28. 28.

    Hackett, T. A., Preuss, T. M. & Kaas, J. H. Architectonic identification of the core region in auditory cortex of macaques, chimpanzees, and humans. J. Comp. Neurol. 441, 197–222 (2001).

    CAS  Article  Google Scholar 

  29. 29.

    Tournier, J.-D., Calamante, F. & Connelly, A. Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution. Neuroimage 35, 1459–1472 (2007).

    Article  Google Scholar 

Download references

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).

Author information

Affiliations

Authors

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.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

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

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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).

Supplementary information

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing