1. Neuroscience

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

  1. Nicole Eichert  Is a corresponding author
  2. Emma C Robinson
  3. Katherine L Bryant
  4. Saad Jbabdi
  5. Mark Jenkinson
  6. Longchuan Li
  7. Kristine Krug
  8. Kate E Watkins
  9. Rogier B Mars
  1. University of Oxford, United Kingdom
  2. King's College London, United Kingdom
  3. Emory University, United States
  4. Radboud Universiteit, Netherlands
https://doi.org/10.7554/eLife.53232
Share this article
Cite this article
  1. Nicole Eichert
  2. Emma C Robinson
  3. Katherine L Bryant
  4. Saad Jbabdi
  5. Mark Jenkinson
  6. Longchuan Li
  7. Kristine Krug
  8. Kate E Watkins
  9. Rogier B Mars
(2020)
Cross-species cortical alignment identifies different types of anatomical reorganization in the primate temporal lobe
eLife 9:e53232.
https://doi.org/10.7554/eLife.53232
  2. Download BibTeX
  3. Download .RIS

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
The following previously published data sets were used

Article and author information

Author details

  1. 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.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7818-5787

  2. 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.

  3. Katherine L Bryant

    Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.

  4. 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.

  5. Mark Jenkinson

    Oxford Centre for Functional MRI of the Brain, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6043-0166

  6. Longchuan Li

    Marcus Autism Center, Children's Healthcare of Atlanta, Emory University, Atlanta, United States
    Competing interests
    No competing interests declared.

  7. Kristine Krug

    Department of Physiology, Anatomy & Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    Kristine Krug, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7119-9350

  8. Kate E Watkins

    Department of Experimental Pschology, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2621-482X

  9. 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.

Reviewing Editor

  1. Timothy Verstynen, Carnegie Mellon University, United States

Publication history

  1. Received: October 31, 2019
  2. Accepted: March 19, 2020
  3. Accepted Manuscript published: March 23, 2020 (version 1)
  4. Version of Record published: April 23, 2020 (version 2)

Copyright

© 2020, Eichert et al.

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.

Metrics

  • 3,327
    Page views
  • 403
    Downloads
  • 37
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Nicole Eichert
  2. Emma C Robinson
  3. Katherine L Bryant
  4. Saad Jbabdi
  5. Mark Jenkinson
  6. Longchuan Li
  7. Kristine Krug
  8. Kate E Watkins
  9. Rogier B Mars
(2020)
Cross-species cortical alignment identifies different types of anatomical reorganization in the primate temporal lobe
eLife 9:e53232.
https://doi.org/10.7554/eLife.53232

Categories and tags

Research organisms

Further reading

    1. Developmental Biology
    2. Neuroscience

    Origin of wiring specificity in an olfactory map revealed by neuron type-specific, time-lapse imaging of dendrite targeting

    Kenneth Kin Lam Wong, Tongchao Li ... Liqun Luo
    Research Article

    How does wiring specificity of neural maps emerge during development? Formation of the adult Drosophila olfactory glomerular map begins with patterning of projection neuron (PN) dendrites at the early pupal stage. To better understand the origin of wiring specificity of this map, we created genetic tools to systematically characterize dendrite patterning across development at PN type-specific resolution. We find that PNs use lineage and birth order combinatorially to build the initial dendritic map. Specifically, birth order directs dendrite targeting in rotating and binary manners for PNs of the anterodorsal and lateral lineages, respectively. Two-photon- and adaptive optical lattice light-sheet microscope-based time-lapse imaging reveals that PN dendrites initiate active targeting with direction-dependent branch stabilization on the timescale of seconds. Moreover, PNs that are used in both the larval and adult olfactory circuits prune their larval-specific dendrites and re-extend new dendrites simultaneously to facilitate timely olfactory map organization. Our work highlights the power and necessity of type-specific neuronal access and time-lapse imaging in identifying wiring mechanisms that underlie complex patterns of functional neural maps.

    1. Neuroscience

    Generative network modeling reveals quantitative definitions of bilateral symmetry exhibited by a whole insect brain connectome

    Benjamin D Pedigo, Mike Powell ... Joshua T Vogelstein
    Research Article

    Comparing connectomes can help explain how neural connectivity is related to genetics, disease, development, learning, and behavior. However, making statistical inferences about the significance and nature of differences between two networks is an open problem, and such analysis has not been extensively applied to nanoscale connectomes. Here, we investigate this problem via a case study on the bilateral symmetry of a larval Drosophila brain connectome. We translate notions of'bilateral symmetry' to generative models of the network structure of the left and right hemispheres, allowing us to test and refine our understanding of symmetry. We find significant differences in connection probabilities both across the entire left and right networks and between specific cell types. By rescaling connection probabilities or removing certain edges based on weight, we also present adjusted definitions of bilateral symmetry exhibited by this connectome. This work shows how statistical inferences from networks can inform the study of connectomes, facilitating future comparisons of neural structures.

    1. Neuroscience

    Oligodendrocyte-mediated myelin plasticity and its role in neural synchronization

    Sinisa Pajevic, Dietmar Plenz ... R Douglas Fields
    Research Article

    Temporal synchrony of signals arriving from different neurons or brain regions is essential for proper neural processing. Nevertheless, it is not well understood how such synchrony is achieved and maintained in a complex network of time-delayed neural interactions. Myelin plasticity, accomplished by oligodendrocytes (OLs), has been suggested as an efficient mechanism for controlling timing in brain communications through adaptive changes of axonal conduction velocity and consequently conduction time delays, or latencies; however, local rules and feedback mechanisms that OLs use to achieve synchronization are not known. We propose a mathematical model of oligodendrocyte-mediated myelin plasticity (OMP) in which OLs play an active role in providing such feedback. This is achieved without using arrival times at the synapse or modulatory signaling from astrocytes; instead, it relies on the presence of global and transient OL responses to local action potentials in the axons they myelinate. While inspired by OL morphology, we provide the theoretical underpinnings that motivated the model and explore its performance for a wide range of its parameters. Our results indicate that when the characteristic time of OL’s transient intracellular responses to neural spikes is between 10 and 40 ms and the firing rates in individual axons are relatively low (⪅ 10 Hz), the OMP model efficiently synchronizes correlated and time-locked signals while latencies in axons carrying independent signals are unaffected. This suggests a novel form of selective synchronization in the CNS in which oligodendrocytes play an active role by modulating the conduction delays of correlated spike trains as they traverse to their targets.