Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in Aplysia
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 mo...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2021-06-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/68651 |
| _version_ | 1797997540917903360 |
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| author | Alexis Bédécarrats Laura Puygrenier John Castro O'Byrne Quentin Lade John Simmers Romuald Nargeot |
| author_facet | Alexis Bédécarrats Laura Puygrenier John Castro O'Byrne Quentin Lade John Simmers Romuald Nargeot |
| author_sort | Alexis Bédécarrats |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-11T10:33:22Z |
| format | Article |
| id | doaj.art-23bb4fa689924fc9a4b02a06f2a48173 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T10:33:22Z |
| publishDate | 2021-06-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-23bb4fa689924fc9a4b02a06f2a481732022-12-22T04:29:21ZengeLife Sciences Publications LtdeLife2050-084X2021-06-011010.7554/eLife.68651Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in AplysiaAlexis Bédécarrats0https://orcid.org/0000-0003-3621-5639Laura Puygrenier1John Castro O'Byrne2Quentin Lade3John Simmers4https://orcid.org/0000-0002-7487-4638Romuald Nargeot5https://orcid.org/0000-0002-7939-0333Univ. Bordeaux, INCIA, UMR 5287, F-33076 Bordeaux, Bordeaux, FranceUniv. Bordeaux, INCIA, UMR 5287, F-33076 Bordeaux, Bordeaux, FranceUniv. Bordeaux, INCIA, UMR 5287, F-33076 Bordeaux, Bordeaux, FranceUniv. Bordeaux, INCIA, UMR 5287, F-33076 Bordeaux, Bordeaux, FranceUniv. Bordeaux, INCIA, UMR 5287, F-33076 Bordeaux, Bordeaux, FranceUniv. Bordeaux, INCIA, UMR 5287, F-33076 Bordeaux, Bordeaux, FranceThe 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.https://elifesciences.org/articles/68651pacemakercentral pattern generatorAplysiafeeding behavior |
| spellingShingle | Alexis Bédécarrats Laura Puygrenier John Castro O'Byrne Quentin Lade John Simmers Romuald Nargeot Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in Aplysia eLife pacemaker central pattern generator Aplysia feeding behavior |
| title | Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in Aplysia |
| title_full | Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in Aplysia |
| title_fullStr | Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in Aplysia |
| title_full_unstemmed | Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in Aplysia |
| title_short | Organelle calcium-derived voltage oscillations in pacemaker neurons drive the motor program for food-seeking behavior in Aplysia |
| title_sort | organelle calcium derived voltage oscillations in pacemaker neurons drive the motor program for food seeking behavior in aplysia |
| topic | pacemaker central pattern generator Aplysia feeding behavior |
| url | https://elifesciences.org/articles/68651 |
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