Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in Aplysia
- University of Bordeaux, INCIA, UMR 5287, France
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
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Data from: Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in AplysiaDryad Digital Repository, doi:10.5061/dryad.pvmcvdnkr.
Article and author information
Author details
Alexis Bédécarrats
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
- Paul Katz, University of Massachusetts Amherst
Version history
- Received: March 22, 2021
- Accepted: June 29, 2021
- Accepted Manuscript published: June 30, 2021 (version 1)
- Version of Record published: July 7, 2021 (version 2)
- 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.
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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
Further reading
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Learning requires the ability to link actions to outcomes. How motivation facilitates learning is not well understood. We designed a behavioral task in which mice self-initiate trials to learn cue-reward contingencies and found that the anterior cingulate region of the prefrontal cortex (ACC) contains motivation-related signals to maximize rewards. In particular, we found that ACC neural activity was consistently tied to trial initiations where mice seek to leave unrewarded cues to reach reward-associated cues. Notably, this neural signal persisted over consecutive unrewarded cues until reward-associated cues were reached, and was required for learning. To determine how ACC inherits this motivational signal we performed projection-specific photometry recordings from several inputs to ACC during learning. In doing so, we identified a ramp in bulk neural activity in orbitofrontal cortex (OFC)-to-ACC projections as mice received unrewarded cues, which continued ramping across consecutive unrewarded cues, and finally peaked upon reaching a reward-associated cue, thus maintaining an extended motivational state. Cellular resolution imaging of OFC confirmed these neural correlates of motivation, and further delineated separate ensembles of neurons that sequentially tiled the ramp. Together, these results identify a mechanism by which OFC maps out task structure to convey an extended motivational state to ACC to facilitate goal-directed learning.
