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Neuromodulation Enables Temperature Robustness and Coupling Between Fast and Slow Oscillator Circuits

Acute temperature changes can disrupt neuronal activity and coordination with severe consequences for animal behavior and survival. Nonetheless, two rhythmic neuronal circuits in the crustacean stomatogastric ganglion (STG) and their coordination are maintained across a broad temperature range. Howe...

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Autores principales: Städele, Carola, Stein, Wolfgang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8996074/
https://www.ncbi.nlm.nih.gov/pubmed/35418838
http://dx.doi.org/10.3389/fncel.2022.849160
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author Städele, Carola
Stein, Wolfgang
author_facet Städele, Carola
Stein, Wolfgang
author_sort Städele, Carola
collection PubMed
description Acute temperature changes can disrupt neuronal activity and coordination with severe consequences for animal behavior and survival. Nonetheless, two rhythmic neuronal circuits in the crustacean stomatogastric ganglion (STG) and their coordination are maintained across a broad temperature range. However, it remains unclear how this temperature robustness is achieved. Here, we dissociate temperature effects on the rhythm generating circuits from those on upstream ganglia. We demonstrate that heat-activated factors extrinsic to the rhythm generators are essential to the slow gastric mill rhythm’s temperature robustness and contribute to the temperature response of the fast pyloric rhythm. The gastric mill rhythm crashed when its rhythm generator in the STG was heated. It was restored when upstream ganglia were heated and temperature-matched to the STG. This also increased the activity of the peptidergic modulatory projection neuron (MCN1), which innervates the gastric mill circuit. Correspondingly, MCN1’s neuropeptide transmitter stabilized the rhythm and maintained it over a broad temperature range. Extrinsic neuromodulation is thus essential for the oscillatory circuits in the STG and enables neural circuits to maintain function in temperature-compromised conditions. In contrast, integer coupling between pyloric and gastric mill rhythms was independent of whether extrinsic inputs and STG pattern generators were temperature-matched or not, demonstrating that the temperature robustness of the coupling is enabled by properties intrinsic to the rhythm generators. However, at near-crash temperature, integer coupling was maintained only in some animals while it was absent in others. This was true despite regular rhythmic activity in all animals, supporting that degenerate circuit properties result in idiosyncratic responses to environmental challenges.
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spelling pubmed-89960742022-04-12 Neuromodulation Enables Temperature Robustness and Coupling Between Fast and Slow Oscillator Circuits Städele, Carola Stein, Wolfgang Front Cell Neurosci Neuroscience Acute temperature changes can disrupt neuronal activity and coordination with severe consequences for animal behavior and survival. Nonetheless, two rhythmic neuronal circuits in the crustacean stomatogastric ganglion (STG) and their coordination are maintained across a broad temperature range. However, it remains unclear how this temperature robustness is achieved. Here, we dissociate temperature effects on the rhythm generating circuits from those on upstream ganglia. We demonstrate that heat-activated factors extrinsic to the rhythm generators are essential to the slow gastric mill rhythm’s temperature robustness and contribute to the temperature response of the fast pyloric rhythm. The gastric mill rhythm crashed when its rhythm generator in the STG was heated. It was restored when upstream ganglia were heated and temperature-matched to the STG. This also increased the activity of the peptidergic modulatory projection neuron (MCN1), which innervates the gastric mill circuit. Correspondingly, MCN1’s neuropeptide transmitter stabilized the rhythm and maintained it over a broad temperature range. Extrinsic neuromodulation is thus essential for the oscillatory circuits in the STG and enables neural circuits to maintain function in temperature-compromised conditions. In contrast, integer coupling between pyloric and gastric mill rhythms was independent of whether extrinsic inputs and STG pattern generators were temperature-matched or not, demonstrating that the temperature robustness of the coupling is enabled by properties intrinsic to the rhythm generators. However, at near-crash temperature, integer coupling was maintained only in some animals while it was absent in others. This was true despite regular rhythmic activity in all animals, supporting that degenerate circuit properties result in idiosyncratic responses to environmental challenges. Frontiers Media S.A. 2022-03-28 /pmc/articles/PMC8996074/ /pubmed/35418838 http://dx.doi.org/10.3389/fncel.2022.849160 Text en Copyright © 2022 Städele and Stein. 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 Neuroscience
Städele, Carola
Stein, Wolfgang
Neuromodulation Enables Temperature Robustness and Coupling Between Fast and Slow Oscillator Circuits
title Neuromodulation Enables Temperature Robustness and Coupling Between Fast and Slow Oscillator Circuits
title_full Neuromodulation Enables Temperature Robustness and Coupling Between Fast and Slow Oscillator Circuits
title_fullStr Neuromodulation Enables Temperature Robustness and Coupling Between Fast and Slow Oscillator Circuits
title_full_unstemmed Neuromodulation Enables Temperature Robustness and Coupling Between Fast and Slow Oscillator Circuits
title_short Neuromodulation Enables Temperature Robustness and Coupling Between Fast and Slow Oscillator Circuits
title_sort neuromodulation enables temperature robustness and coupling between fast and slow oscillator circuits
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8996074/
https://www.ncbi.nlm.nih.gov/pubmed/35418838
http://dx.doi.org/10.3389/fncel.2022.849160
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