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Uncovering the inferior fronto-occipital fascicle and its topological organization in non-human primates: the missing connection for language evolution

  • Silvio SarubboEmail author
  • Laurent Petit
  • Alessandro De Benedictis
  • Franco Chioffi
  • Maurice Ptito
  • Tim B. Dyrby
Original Article

Abstract

Whether brain networks underlying the multimodal processing of language in humans are present in non-human primates is an unresolved question in primate evolution. Conceptual awareness in humans, which is the backbone of verbal and non-verbal semantic elaboration, involves intracerebral connectivity via the inferior fronto-occipital fascicle (IFOF). While non-human primates can communicate through visual information channels, there has been no formal demonstration that they possess a functional homologue of the human IFOF. Therefore, we undertook a post-mortem diffusion MRI tractography study in conjunction with Klingler micro-dissection to search for IFOF fiber tracts in brain of Old-World (vervet) monkeys. We found clear and concordant evidence from both techniques for the existence of bilateral fiber tracts connecting the frontal and occipital lobes. These tracts closely resembled the human IFOF with respect to trajectory, topological organization, and cortical terminal fields. Moreover, these fibers are clearly distinct from other bundles previously described in this region of monkey brain, i.e., the inferior longitudinal and uncinate fascicles, and the external and extreme capsules. This demonstration of an IFOF in brain of a species that diverged from the human lineage some 22 millions years ago enhances our comprehension about the evolution of language and social behavior.

Keywords

White matter Klingler dissection Inferior fronto-occipital fascicle Brain connectivity Tractography Monkey anatomy 

Notes

Acknowledgements

We are very grateful to the valuable work of proofreading of the present manuscript provided by Inglewood Biomedical Editing (http://www.inglewoodbiomedediting.com).

Compliance with ethical standards

Conflict of interest

Authors have no conflict of interests and did not receive funding for this work.

Ethical approval

The brain specimens were collected from animals enrolled in a terminal project reviewed and approved by the Institutional Review Board of the Behavioural Science Foundation (BSF; St-Kitts, West Indies) and were donated by Prof. Roberta Palmour of McGill University, in a collaboration with the BSF. The human brain dissection presented in the paper was performed in the context of the Structural and Functional Connectivity Lab Project, approved by the Research Ethics Committee of the Azienda Provinciale dei Servizi Sanitari (APSS) of Trento (Italy).

Supplementary material

429_2019_1856_MOESM1_ESM.docx (841 kb)
Supplementary material 1 (DOCX 840 KB)

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© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Division of Neurosurgery, Structural and Functional Connectivity Lab Project“S. Chiara” Hospital, Azienda Provinciale per i Servizi Sanitari (APSS)TrentoItaly
  2. 2.Groupe d’Imagerie NeurofonctionnelleInstitut des Maladies Neurodégénératives, UMR 5293, CNRS, CEA University of BordeauxBordeauxFrance
  3. 3.Neurosurgery Unit, Department of Neuroscience and NeurorehabilitationBambino Gesù Children’s Hospital, IRCCSRomeItaly
  4. 4.École d’optométrieUniversité de MontréalMontrealCanada
  5. 5.Danish Research Centre for Magnetic Resonance, Center for Functional and Diagnostic Imaging and ResearchCopenhagen University Hospital HvidovreHvidovreDenmark
  6. 6.Department of Applied Mathematics and Computer ScienceTechnical University of DenmarkKongens LyngbyDenmark

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