Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in Aplysia

Abstract

The expression of motivated behaviors depends on both external and internally-arising neural stimuli, yet the intrinsic releasing mechanisms for such variably occurring behaviors remain elusive. In isolated nervous system preparations of Aplysia, we have found that irregularly expressed cycles of motor output underlying food-seeking behavior arise from regular membrane potential oscillations of varying magnitude in an identified pair of interneurons (B63) in the bilateral buccal ganglia. This rhythmic signal, which is specific to the B63 cells, is generated by organelle-derived intracellular calcium fluxes that activate voltage-independent plasma membrane channels. The resulting voltage oscillation spreads throughout a subset of gap junction-coupled buccal network neurons and by triggering plateau potential-mediated bursts in B63, can initiate motor output driving food-seeking action. Thus, an atypical neuronal pacemaker mechanism, based on rhythmic intracellular calcium store release and intercellular propagation, can act as an autonomous intrinsic releaser for the occurrence of a motivated behavior.

Data availability

Source data file have been provided for Figures 2,3,10:Bédécarrats, Alexis et al. (2021), Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in Aplysia, Dryad, Dataset, https://doi.org/10.5061/dryad.pvmcvdnkr

The following data sets were generated

Article and author information

Author details

  1. Alexis Bédécarrats

    Neuroscience, University of Bordeaux, INCIA, UMR 5287, Bordeaux, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3621-5639
  2. Laura Puygrenier

    Univ. Bordeaux, INCIA, UMR 5287, F-33076 Bordeaux, France. CNRS, INCIA, UMR 5287, F-33076 Bordeaux, France., University of Bordeaux, INCIA, UMR 5287, Bordeaux, France
    Competing interests
    The authors declare that no competing interests exist.
  3. John Castro O'Byrne

    Univ. Bordeaux, INCIA, UMR 5287, F-33076 Bordeaux, France. CNRS, INCIA, UMR 5287, F-33076 Bordeaux, France., University of Bordeaux, INCIA, UMR 5287, Bordeaux Cedex, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Quentin Lade

    Univ. Bordeaux, INCIA, UMR 5287, F-33076 Bordeaux, France. CNRS, INCIA, UMR 5287, F-33076 Bordeaux, France., University of Bordeaux, INCIA, UMR 5287, Bordeaux Cedex, France
    Competing interests
    The authors declare that no competing interests exist.
  5. John Simmers

    INCIA UMR 5287, University of Bordeaux, INCIA, UMR 5287, Bordeaux, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7487-4638
  6. Romuald Nargeot

    Univ. Bordeaux, INCIA, UMR 5287, F-33076 Bordeaux, France. CNRS, INCIA, UMR 5287, F-33076 Bordeaux, France., University of Bordeaux, INCIA, UMR 5287, Bordeaux Cedex, France
    For correspondence
    romuald.nargeot@u-bordeaux.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7939-0333

Funding

Agence Nationale de la Recherche (ANR-13-BV5-0014-01)

  • Romuald Nargeot

Agence Nationale de la Recherche (ANR-10-Idex-03-02)

  • Alexis Bédécarrats

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

Copyright

© 2021, Bédécarrats 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.

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  1. Alexis Bédécarrats
  2. Laura Puygrenier
  3. John Castro O'Byrne
  4. Quentin Lade
  5. John Simmers
  6. Romuald Nargeot
(2021)
Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in Aplysia
eLife 10:e68651.
https://doi.org/10.7554/eLife.68651

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https://doi.org/10.7554/eLife.68651

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