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Sodium-mediated plateau potentials in an identified decisional neuron contribute to feeding-related motor pattern genesis in Aplysia

Motivated behaviors such as feeding depend on the functional properties of decision neurons to provide the flexibility required for behavioral adaptation. Here, we analyzed the ionic basis of the endogenous membrane properties of an identified decision neuron (B63) that drive radula biting cycles un...

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Autores principales: Bédécarrats, Alexis, Simmers, John, Nargeot, Romuald
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10288323/
https://www.ncbi.nlm.nih.gov/pubmed/37361713
http://dx.doi.org/10.3389/fncir.2023.1200902
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author Bédécarrats, Alexis
Simmers, John
Nargeot, Romuald
author_facet Bédécarrats, Alexis
Simmers, John
Nargeot, Romuald
author_sort Bédécarrats, Alexis
collection PubMed
description Motivated behaviors such as feeding depend on the functional properties of decision neurons to provide the flexibility required for behavioral adaptation. Here, we analyzed the ionic basis of the endogenous membrane properties of an identified decision neuron (B63) that drive radula biting cycles underlying food-seeking behavior in Aplysia. Each spontaneous bite cycle arises from the irregular triggering of a plateau-like potential and resultant bursting by rhythmic subthreshold oscillations in B63’s membrane potential. In isolated buccal ganglion preparations, and after synaptic isolation, the expression of B63’s plateau potentials persisted after removal of extracellular calcium, but was completely suppressed in a tetrodotoxin (TTX)- containing bath solution, thereby indicating the contribution of a transmembrane Na(+) influx. Potassium outward efflux through tetraethylammonium (TEA)- and calcium-sensitive channels was found to contribute to each plateau’s active termination. This intrinsic plateauing capability, in contrast to B63’s membrane potential oscillation, was blocked by the calcium-activated non-specific cationic current (I(CAN)) blocker flufenamic acid (FFA). Conversely, the SERCA blocker cyclopianozic acid (CPA), which abolished the neuron’s oscillation, did not prevent the expression of experimentally evoked plateau potentials. These results therefore indicate that the dynamic properties of the decision neuron B63 rely on two distinct mechanisms involving different sub-populations of ionic conductances.
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spelling pubmed-102883232023-06-24 Sodium-mediated plateau potentials in an identified decisional neuron contribute to feeding-related motor pattern genesis in Aplysia Bédécarrats, Alexis Simmers, John Nargeot, Romuald Front Neural Circuits Neural Circuits Motivated behaviors such as feeding depend on the functional properties of decision neurons to provide the flexibility required for behavioral adaptation. Here, we analyzed the ionic basis of the endogenous membrane properties of an identified decision neuron (B63) that drive radula biting cycles underlying food-seeking behavior in Aplysia. Each spontaneous bite cycle arises from the irregular triggering of a plateau-like potential and resultant bursting by rhythmic subthreshold oscillations in B63’s membrane potential. In isolated buccal ganglion preparations, and after synaptic isolation, the expression of B63’s plateau potentials persisted after removal of extracellular calcium, but was completely suppressed in a tetrodotoxin (TTX)- containing bath solution, thereby indicating the contribution of a transmembrane Na(+) influx. Potassium outward efflux through tetraethylammonium (TEA)- and calcium-sensitive channels was found to contribute to each plateau’s active termination. This intrinsic plateauing capability, in contrast to B63’s membrane potential oscillation, was blocked by the calcium-activated non-specific cationic current (I(CAN)) blocker flufenamic acid (FFA). Conversely, the SERCA blocker cyclopianozic acid (CPA), which abolished the neuron’s oscillation, did not prevent the expression of experimentally evoked plateau potentials. These results therefore indicate that the dynamic properties of the decision neuron B63 rely on two distinct mechanisms involving different sub-populations of ionic conductances. Frontiers Media S.A. 2023-06-09 /pmc/articles/PMC10288323/ /pubmed/37361713 http://dx.doi.org/10.3389/fncir.2023.1200902 Text en Copyright © 2023 Bédécarrats, Simmers and Nargeot. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neural Circuits
Bédécarrats, Alexis
Simmers, John
Nargeot, Romuald
Sodium-mediated plateau potentials in an identified decisional neuron contribute to feeding-related motor pattern genesis in Aplysia
title Sodium-mediated plateau potentials in an identified decisional neuron contribute to feeding-related motor pattern genesis in Aplysia
title_full Sodium-mediated plateau potentials in an identified decisional neuron contribute to feeding-related motor pattern genesis in Aplysia
title_fullStr Sodium-mediated plateau potentials in an identified decisional neuron contribute to feeding-related motor pattern genesis in Aplysia
title_full_unstemmed Sodium-mediated plateau potentials in an identified decisional neuron contribute to feeding-related motor pattern genesis in Aplysia
title_short Sodium-mediated plateau potentials in an identified decisional neuron contribute to feeding-related motor pattern genesis in Aplysia
title_sort sodium-mediated plateau potentials in an identified decisional neuron contribute to feeding-related motor pattern genesis in aplysia
topic Neural Circuits
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10288323/
https://www.ncbi.nlm.nih.gov/pubmed/37361713
http://dx.doi.org/10.3389/fncir.2023.1200902
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