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.

Reviewing Editor

  1. Paul Katz, University of Massachusetts Amherst

Version history

  1. Received: March 22, 2021
  2. Accepted: June 29, 2021
  3. Accepted Manuscript published: June 30, 2021 (version 1)
  4. Version of Record published: July 7, 2021 (version 2)
  5. Version of Record updated: July 14, 2021 (version 3)

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.

Metrics

  • 1,731
    views
  • 174
    downloads
  • 6
    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. 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

Share this article

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

Further reading

    1. Neuroscience
    Kenta Abe, Yuki Kambe ... Tatsuo Sato
    Research Article

    Midbrain dopamine neurons impact neural processing in the prefrontal cortex (PFC) through mesocortical projections. However, the signals conveyed by dopamine projections to the PFC remain unclear, particularly at the single-axon level. Here, we investigated dopaminergic axonal activity in the medial PFC (mPFC) during reward and aversive processing. By optimizing microprism-mediated two-photon calcium imaging of dopamine axon terminals, we found diverse activity in dopamine axons responsive to both reward and aversive stimuli. Some axons exhibited a preference for reward, while others favored aversive stimuli, and there was a strong bias for the latter at the population level. Long-term longitudinal imaging revealed that the preference was maintained in reward- and aversive-preferring axons throughout classical conditioning in which rewarding and aversive stimuli were paired with preceding auditory cues. However, as mice learned to discriminate reward or aversive cues, a cue activity preference gradually developed only in aversive-preferring axons. We inferred the trial-by-trial cue discrimination based on machine learning using anticipatory licking or facial expressions, and found that successful discrimination was accompanied by sharper selectivity for the aversive cue in aversive-preferring axons. Our findings indicate that a group of mesocortical dopamine axons encodes aversive-related signals, which are modulated by both classical conditioning across days and trial-by-trial discrimination within a day.

    1. Neuroscience
    Baiwei Liu, Zampeta-Sofia Alexopoulou, Freek van Ede
    Research Article

    Working memory enables us to bridge past sensory information to upcoming future behaviour. Accordingly, by its very nature, working memory is concerned with two components: the past and the future. Yet, in conventional laboratory tasks, these two components are often conflated, such as when sensory information in working memory is encoded and tested at the same location. We developed a task in which we dissociated the past (encoded location) and future (to-be-tested location) attributes of visual contents in working memory. This enabled us to independently track the utilisation of past and future memory attributes through gaze, as observed during mnemonic selection. Our results reveal the joint consideration of past and future locations. This was prevalent even at the single-trial level of individual saccades that were jointly biased to the past and future. This uncovers the rich nature of working memory representations, whereby both past and future memory attributes are retained and can be accessed together when memory contents become relevant for behaviour.