Cross-species cortical alignment identifies different types of anatomical reorganization in the primate temporal lobe

Abstract
Data availability
Article and author information
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Abstract

Evolutionary adaptations of temporo-parietal cortex are considered to be a critical specialization of the human brain. Cortical adaptations, however, can affect different aspects of brain architecture, including local expansion of the cortical sheet or changes in connectivity between cortical areas. We distinguish different types of changes in brain architecture using a computational neuroanatomy approach. We investigate the extent to which between-species alignment, based on cortical myelin, can predict changes in connectivity patterns across macaque, chimpanzee, and human. We show that expansion and relocation of brain areas can predict terminations of several white matter tracts in temporo-parietal cortex, including the middle and superior longitudinal fasciculus, but not the arcuate fasciculus. This demonstrates that the arcuate fasciculus underwent additional evolutionary modifications affecting the temporal lobe connectivity pattern. This approach can flexibly be extended to include other features of cortical organization and other species, allowing direct tests of comparative hypotheses of brain organization.

Data availability

This study used previously published datasets and availability of source data for the different data sets is provided in an overview table in the main manuscript ('Data Availability Overview'). The anonymised human MRI dataset that was generated for the present study is available via OpenNeuro under the accession code ds002634 (version 1.0.1). The results scene files have been made available from the Wellcome Centre for Integrative Neuroimaging's GitLab at git.fmrib.ox.ac.uk/neichert/project_MSM. Group-level myelin-maps and tract surface maps of the three species will be openly accessible as part of the results scene files. Numerical data underlying Figure 5 and Appendix 3 - Figure 2 are provided as Source Data with the article. All further derived data supporting the findings of this study are available from the corresponding author upon request.

The following data sets were generated

1. Eichert
2. N
3. Mars
4. RB
5. Watkins
6. KE
7. project-specific co-authors
(2020) Project_larynx
OpenNeuro, ds002634.

http://dx.doi.org/10.18112/openneuro.ds002634.v1.0.1

The following previously published data sets were used

1. National Chimpanzee Brain Resource
(2019) National Chimpanzee Brain Resource
National Chimpanzee Brain Resource. RRID: SCR_006863.

https://www.chimpanzeebrain.org/
1. Folloni D
2. Verhagen L
3. Mars RB
4. Fouragnan E
5. Constans C
6. Aubry JF
7. Rushworth MFS
8. Sallet J
(2019) University of Oxford WIN Macaque PM
PRIMatE Data Exchange (PRIME-DE) resource. RRID: SCR_016621.

http://fcon_1000.projects.nitrc.org/indi/PRIME/oxford2.html
1. Bridge H
2. Bell AH
3. Ainsworth M
4. Sallet J
5. Premereur E
6. Ahmed B
7. Mitchell AS
8. Schüffelgen U
9. Buckley M
10. Tendler BC
11. Miller KL
12. Mars RB
13. Parker AJ
14. Krug K
(2019) Preserved extrastriate visual network in a monkey with substantial, naturally occurring damage to primary visual cortex
GIN Database: brainwithoutv1.

https://gin.g-node.org/hbridge_oxford/brainwithoutv1

Article and author information

Author details

Nicole Eichert

Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom

For correspondence
nicole.eichert@psy.ox.ac.uk

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-7818-5787
Emma C Robinson

Department of Biomedical Engineering, School of Biomedical Engineering and Imaging Sciences, King's College London, London, United Kingdom

Competing interests
No competing interests declared.
Katherine L Bryant

Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom

Competing interests
No competing interests declared.
Saad Jbabdi

Centre for Functional MRI of the Brain, Department of Clinical Neurology, University of Oxford, Oxford, United Kingdom

Competing interests
No competing interests declared.
Mark Jenkinson

Oxford Centre for Functional MRI of the Brain, University of Oxford, Oxford, United Kingdom

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0001-6043-0166
Longchuan Li

Marcus Autism Center, Children's Healthcare of Atlanta, Emory University, Atlanta, United States

Competing interests
No competing interests declared.
Kristine Krug

Department of Physiology, Anatomy & Genetics, University of Oxford, Oxford, United Kingdom

Competing interests
Kristine Krug, Reviewing editor, eLife.

"This ORCID iD identifies the author of this article:" 0000-0001-7119-9350
Kate E Watkins

Department of Experimental Pschology, University of Oxford, Oxford, United Kingdom

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-2621-482X
Rogier B Mars

Donders Institute for Brain, Cognition and Behaviour, Radboud Universiteit, Nijmegen, Netherlands

Competing interests
No competing interests declared.

Funding

Wellcome (203730/Z/16/Z)

Nicole Eichert

Marie Sklodowska-Curie Fellowship (750026)

Katherine L Bryant

Medical Research Council (MR/L009013/1)

Saad Jbabdi

National Institute for Health Research

Mark Jenkinson

Oxford Biomedical Research Centre

Mark Jenkinson

Biotechnology and Biological Sciences Research Council (BB/H016902/1)

Kristine Krug

Wellcome (101092/Z/13/Z)

Kristine Krug

Other (R01MH118534)

Longchuan Li

Other (P50MH100029)

Longchuan Li

Other (R01MH118285)

Longchuan Li

Wellcome (203139/Z/16/Z)

Rogier B Mars

NIHR Oxford Heath Biomedical Research Centre

Rogier B Mars

Biotechnology and Biological Sciences Research Council (BB/N019814/1)

Rogier B Mars

Netherlands Organization for Scientific Research (452-13-015)

Rogier B Mars

Academy of Medical Sciences

Emma C Robinson

British Heart Foundation

Emma C Robinson

Government Department of Business, Energy and Industrial Strategy

Emma C Robinson

Wellcome (SBF003\1116)

Emma C Robinson

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Chimpanzee data:Data were acquired at the Yerkes National Primate Research Center (YNPRC) at Emory University through separate studies covered by animal research protocols approved by YNPRC and the Emory University Institutional Animal Care and Use Committee (approval no. YER-2001206). These chimpanzee MRI scans 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. All the scans reported in this publication were completed by the end of 2012.Macaque Data:Procedures of the in vivo macaque data acquisition were carried out in accordance with Home Office (UK) Regulations and European Union guidelines (EU directive 86/609/EEC; EU Directive 2010/63/EU).

Human subjects: The study was approved by the Central University (of Oxford) Research Ethics Committee (CUREC, R55787/RE001) in accordance with the regulatory standards of the Code of Ethics of the World Medical Association (Declaration of Helsinki). All participants gave informed consent to their participation and were monetarily compensated for their participation.

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.