Synaptic and peptidergic connectome of a neurosecretory centre in the annelid brain

  1. Elizabeth A Williams  Is a corresponding author
  2. Csaba Verasztó
  3. Sanja Jasek
  4. Markus Conzelmann
  5. Réza Shahidi
  6. Philipp Bauknecht
  7. Olivier Mirabeau
  8. Gáspár Jékely  Is a corresponding author
  1. Max Planck Institute for Developmental Biology, Germany
  2. Institut Curie, France

Abstract

Neurosecretory centers in animal brains use peptidergic signaling to influence physiology and behavior. Understanding neurosecretory center function requires mapping cell types, synapses, and peptidergic networks. Here we use transmission electron microscopy and gene expression mapping to analyze the synaptic and peptidergic connectome of an entire neurosecretory center. We reconstructed 78 neurosecretory neurons and mapped their synaptic connectivity in the brain of larval Platynereis dumerilii, a marine annelid. These neurons form an anterior neurosecretory center expressing many neuropeptides, including hypothalamic peptide orthologs and their receptors. Analysis of peptide-receptor pairs in spatially mapped single-cell transcriptome data revealed sparsely connected networks linking specific neuronal subsets. We experimentally analyzed one peptide-receptor pair and found that a neuropeptide can couple neurosecretory and synaptic brain signaling. Our study uncovered extensive networks of peptidergic signaling within a neurosecretory center and its connection to the synaptic brain.

Data availability

The following previously published data sets were used

Article and author information

Author details

  1. Elizabeth A Williams

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    For correspondence
    elizabeth.williams@tuebingen.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3067-3137
  2. Csaba Verasztó

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6295-7148
  3. Sanja Jasek

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Markus Conzelmann

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Réza Shahidi

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Philipp Bauknecht

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Olivier Mirabeau

    Cancer Genetics Unit, Inserm U830, Institut Curie, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Gáspár Jékely

    Max Planck Institute for Developmental Biology, Tübingen, Germany
    For correspondence
    G.Jekely@exeter.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8496-9836

Funding

Max-Planck-Gesellschaft (N/A)

  • Elizabeth A Williams
  • Csaba Verasztó
  • Sanja Jasek
  • Markus Conzelmann
  • Philipp Bauknecht

Deutsche Forschungsgemeinschaft (JE 777/1-1)

  • Elizabeth A Williams

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

Copyright

© 2017, Williams 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

  • 3,144
    views
  • 448
    downloads
  • 95
    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. Elizabeth A Williams
  2. Csaba Verasztó
  3. Sanja Jasek
  4. Markus Conzelmann
  5. Réza Shahidi
  6. Philipp Bauknecht
  7. Olivier Mirabeau
  8. Gáspár Jékely
(2017)
Synaptic and peptidergic connectome of a neurosecretory centre in the annelid brain
eLife 6:e26349.
https://doi.org/10.7554/eLife.26349

Share this article

https://doi.org/10.7554/eLife.26349

Further reading

    1. Neuroscience
    Ilya A Rybak, Natalia A Shevtsova ... Alain Frigon
    Research Advance

    Locomotion is controlled by spinal circuits that interact with supraspinal drives and sensory feedback from the limbs. These sensorimotor interactions are disrupted following spinal cord injury. The thoracic lateral hemisection represents an experimental model of an incomplete spinal cord injury, where connections between the brain and spinal cord are abolished on one side of the cord. To investigate the effects of such an injury on the operation of the spinal locomotor network, we used our computational model of cat locomotion recently published in eLife (Rybak et al., 2024) to investigate and predict changes in cycle and phase durations following a thoracic lateral hemisection during treadmill locomotion in tied-belt (equal left-right speeds) and split-belt (unequal left-right speeds) conditions. In our simulations, the ‘hemisection’ was always applied to the right side. Based on our model, we hypothesized that following hemisection the contralesional (‘intact’, left) side of the spinal network is mostly controlled by supraspinal drives, whereas the ipsilesional (‘hemisected’, right) side is mostly controlled by somatosensory feedback. We then compared the simulated results with those obtained during experiments in adult cats before and after a mid-thoracic lateral hemisection on the right side in the same locomotor conditions. Our experimental results confirmed many effects of hemisection on cat locomotion predicted by our simulations. We show that having the ipsilesional hindlimb step on the slow belt, but not the fast belt, during split-belt locomotion substantially reduces the effects of lateral hemisection. The model provides explanations for changes in temporal characteristics of hindlimb locomotion following hemisection based on altered interactions between spinal circuits, supraspinal drives, and somatosensory feedback.

    1. Neuroscience
    Jill R Turner, Jocelyn Martin
    Insight

    Reversing opioid overdoses in rats using a drug that does not enter the brain prevents the sudden and severe withdrawal symptoms associated with therapeutics that target the central nervous system.