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.

Reviewing Editor

  1. Timothy Verstynen, Carnegie Mellon University, United States

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.

Version 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

  • 3,928
    views
  • 440
    downloads
  • 67
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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

Share this article

https://doi.org/10.7554/eLife.53232

Categories and tags

Research organisms

Further reading

    1. Cell Biology
    2. Neuroscience

    Translational regulation enhances distinction of cell types in the nervous system

    Toshiharu Ichinose, Shu Kondo ... Hiromu Tanimoto
    Research Article

    Multicellular organisms are composed of specialized cell types with distinct proteomes. While recent advances in single-cell transcriptome analyses have revealed differential expression of mRNAs, cellular diversity in translational profiles remains underinvestigated. By performing RNA-seq and Ribo-seq in genetically defined cells in the Drosophila brain, we here revealed substantial post-transcriptional regulations that augment the cell-type distinctions at the level of protein expression. Specifically, we found that translational efficiency of proteins fundamental to neuronal functions, such as ion channels and neurotransmitter receptors, was maintained low in glia, leading to their preferential translation in neurons. Notably, distribution of ribosome footprints on these mRNAs exhibited a remarkable bias toward the 5′ leaders in glia. Using transgenic reporter strains, we provide evidence that the small upstream open-reading frames in the 5’ leader confer selective translational suppression in glia. Overall, these findings underscore the profound impact of translational regulation in shaping the proteomics for cell-type distinction and provide new insights into the molecular mechanisms driving cell-type diversity.

    1. Neuroscience

    Glutamate neurotransmission from leptin receptor cells is required for typical puberty and reproductive function in female mice

    Cristina Sáenz de Miera, Nicole Bellefontaine ... Carol F Elias
    Research Article

    The hypothalamic ventral premammillary nucleus (PMv) is a glutamatergic nucleus essential for the metabolic control of reproduction. However, conditional deletion of leptin receptor long form (LepRb) in vesicular glutamate transporter 2 (Vglut2) expressing neurons results in virtually no reproductive deficits. In this study, we determined the role of glutamatergic neurotransmission from leptin responsive PMv neurons on puberty and fertility. We first assessed if stimulation of PMv neurons induces luteinizing hormone (LH) release in fed adult females. We used the stimulatory form of designer receptor exclusively activated by designer drugs (DREADDs) in LeprCre (LepRb-Cre) mice. We collected blood sequentially before and for 1 hr after intravenous clozapine-N-oxide injection. LH level increased in animals correctly targeted to the PMv, and LH level was correlated to the number of Fos immunoreactive neurons in the PMv. Next, females with deletion of Slc17a6 (Vglut2) in LepRb neurons (LeprΔVGlut2) showed delayed age of puberty, disrupted estrous cycles, increased gonadotropin-releasing hormone (GnRH) concentration in the axon terminals, and disrupted LH secretion, suggesting impaired GnRH release. To assess if glutamate is required for PMv actions in pubertal development, we generated a Cre-induced reexpression of endogenous LepRb (LeprloxTB) with concomitant deletion of Slc17a6 (Vglut2flox) mice. Rescue of Lepr and deletion of Slc17a6 in the PMv was obtained by stereotaxic injection of an adeno-associated virus vector expressing Cre recombinase. Control LeprloxTB mice with PMv LepRb rescue showed vaginal opening, follicle maturation, and became pregnant, while LeprloxTB;Vglut2flox mice showed no pubertal development. Our results indicate that glutamatergic neurotransmission from leptin sensitive neurons regulates the reproductive axis, and that leptin action on pubertal development via PMv neurons requires Vglut2.

    1. Neuroscience

    Emotional vocalizations alter behaviors and neurochemical release into the amygdala

    Zahra Ghasemahmad, Aaron Mrvelj ... Jeffrey J Wenstrup
    Research Article

    The basolateral amygdala (BLA), a brain center of emotional expression, contributes to acoustic communication by first interpreting the meaning of social sounds in the context of the listener’s internal state, then organizing the appropriate behavioral responses. We propose that modulatory neurochemicals such as acetylcholine (ACh) and dopamine (DA) provide internal-state signals to the BLA while an animal listens to social vocalizations. We tested this in a vocal playback experiment utilizing highly affective vocal sequences associated with either mating or restraint, then sampled and analyzed fluids within the BLA for a broad range of neurochemicals and observed behavioral responses of adult male and female mice. In male mice, playback of restraint vocalizations increased ACh release and usually decreased DA release, while playback of mating sequences evoked the opposite neurochemical release patterns. In non-estrus female mice, patterns of ACh and DA release with mating playback were similar to males. Estrus females, however, showed increased ACh, associated with vigilance, as well as increased DA, associated with reward-seeking. Experimental groups that showed increased ACh release also showed the largest increases in an aversive behavior. These neurochemical release patterns and several behavioral responses depended on a single prior experience with the mating and restraint behaviors. Our results support a model in which ACh and DA provide contextual information to sound analyzing BLA neurons that modulate their output to downstream brain regions controlling behavioral responses to social vocalizations.