An Excitatory/Inhibitory Switch From Asymmetric Sensory Neurons Defines Postsynaptic Tuning for a Rapid Response to NaCl in Caenorhabditis elegans
The neural networks that regulate animal behaviors are encoded in terms of neuronal excitation and inhibition at the synapse. However, how the temporal activity of neural circuits is dynamically and precisely characterized by each signaling interaction via excitatory or inhibitory synapses, and how...
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doaj-53bebaa584af4c2aa0d6192a885f326f2020-11-25T01:03:31ZengFrontiers Media S.A.Frontiers in Molecular Neuroscience1662-50992019-01-011110.3389/fnmol.2018.00484422766An Excitatory/Inhibitory Switch From Asymmetric Sensory Neurons Defines Postsynaptic Tuning for a Rapid Response to NaCl in Caenorhabditis elegansMasahiro KuramochiMotomichi DoiThe neural networks that regulate animal behaviors are encoded in terms of neuronal excitation and inhibition at the synapse. However, how the temporal activity of neural circuits is dynamically and precisely characterized by each signaling interaction via excitatory or inhibitory synapses, and how both synaptic patterns are organized to achieve fine regulation of circuit activities is unclear. Here, we show that in Caenorhabditis elegans, the excitatory/inhibitory switch from asymmetric sensory neurons (ASEL/R) following changes in NaCl concentration is required for a rapid and fine response in postsynaptic interneurons (AIBs). We found that glutamate released by the ASEL neuron inhibits AIBs via a glutamate-gated chloride channel localized at the distal region of AIB neurites. Conversely, glutamate released by the ASER neuron activates AIBs via an AMPA-type ionotropic receptor and a G-protein-coupled metabotropic glutamate receptor. Interestingly, these excitatory receptors are mainly distributed at the proximal regions of the neurite. Our results suggest that these convergent synaptic patterns can tune and regulate the proper behavioral response to environmental changes in NaCl.https://www.frontiersin.org/article/10.3389/fnmol.2018.00484/fullsynapse integrationC. eleganssalt-chemotaxis behaviorCa2+ imagingglutamate |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Masahiro Kuramochi Motomichi Doi |
spellingShingle |
Masahiro Kuramochi Motomichi Doi An Excitatory/Inhibitory Switch From Asymmetric Sensory Neurons Defines Postsynaptic Tuning for a Rapid Response to NaCl in Caenorhabditis elegans Frontiers in Molecular Neuroscience synapse integration C. elegans salt-chemotaxis behavior Ca2+ imaging glutamate |
author_facet |
Masahiro Kuramochi Motomichi Doi |
author_sort |
Masahiro Kuramochi |
title |
An Excitatory/Inhibitory Switch From Asymmetric Sensory Neurons Defines Postsynaptic Tuning for a Rapid Response to NaCl in Caenorhabditis elegans |
title_short |
An Excitatory/Inhibitory Switch From Asymmetric Sensory Neurons Defines Postsynaptic Tuning for a Rapid Response to NaCl in Caenorhabditis elegans |
title_full |
An Excitatory/Inhibitory Switch From Asymmetric Sensory Neurons Defines Postsynaptic Tuning for a Rapid Response to NaCl in Caenorhabditis elegans |
title_fullStr |
An Excitatory/Inhibitory Switch From Asymmetric Sensory Neurons Defines Postsynaptic Tuning for a Rapid Response to NaCl in Caenorhabditis elegans |
title_full_unstemmed |
An Excitatory/Inhibitory Switch From Asymmetric Sensory Neurons Defines Postsynaptic Tuning for a Rapid Response to NaCl in Caenorhabditis elegans |
title_sort |
excitatory/inhibitory switch from asymmetric sensory neurons defines postsynaptic tuning for a rapid response to nacl in caenorhabditis elegans |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Molecular Neuroscience |
issn |
1662-5099 |
publishDate |
2019-01-01 |
description |
The neural networks that regulate animal behaviors are encoded in terms of neuronal excitation and inhibition at the synapse. However, how the temporal activity of neural circuits is dynamically and precisely characterized by each signaling interaction via excitatory or inhibitory synapses, and how both synaptic patterns are organized to achieve fine regulation of circuit activities is unclear. Here, we show that in Caenorhabditis elegans, the excitatory/inhibitory switch from asymmetric sensory neurons (ASEL/R) following changes in NaCl concentration is required for a rapid and fine response in postsynaptic interneurons (AIBs). We found that glutamate released by the ASEL neuron inhibits AIBs via a glutamate-gated chloride channel localized at the distal region of AIB neurites. Conversely, glutamate released by the ASER neuron activates AIBs via an AMPA-type ionotropic receptor and a G-protein-coupled metabotropic glutamate receptor. Interestingly, these excitatory receptors are mainly distributed at the proximal regions of the neurite. Our results suggest that these convergent synaptic patterns can tune and regulate the proper behavioral response to environmental changes in NaCl. |
topic |
synapse integration C. elegans salt-chemotaxis behavior Ca2+ imaging glutamate |
url |
https://www.frontiersin.org/article/10.3389/fnmol.2018.00484/full |
work_keys_str_mv |
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