Diverse modes of synaptic signaling, regulation, and plasticity distinguish two classes of C. elegans glutamatergic neurons
Synaptic vesicle release properties vary between neuronal cell types, but in most cases the molecular basis of this heterogeneity is unknown. Here, we compare in vivo synaptic properties of two neuronal classes in the C. elegans central nervous system, using VGLUT-pHluorin to monitor synaptic vesicl...
| Main Authors: | , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2017-11-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/31234 |
| _version_ | 1811181049696223232 |
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| author | Donovan Ventimiglia Cornelia I Bargmann |
| author_facet | Donovan Ventimiglia Cornelia I Bargmann |
| author_sort | Donovan Ventimiglia |
| collection | DOAJ |
| description | Synaptic vesicle release properties vary between neuronal cell types, but in most cases the molecular basis of this heterogeneity is unknown. Here, we compare in vivo synaptic properties of two neuronal classes in the C. elegans central nervous system, using VGLUT-pHluorin to monitor synaptic vesicle exocytosis and retrieval in intact animals. We show that the glutamatergic sensory neurons AWCON and ASH have distinct synaptic dynamics associated with tonic and phasic synaptic properties, respectively. Exocytosis in ASH and AWCON is differentially affected by SNARE-complex regulators that are present in both neurons: phasic ASH release is strongly dependent on UNC-13, whereas tonic AWCON release relies upon UNC-18 and on the protein kinase C homolog PKC-1. Strong stimuli that elicit high calcium levels increase exocytosis and retrieval rates in AWCON, generating distinct tonic and evoked synaptic modes. These results highlight the differential deployment of shared presynaptic proteins in neuronal cell type-specific functions. |
| first_indexed | 2024-04-11T09:13:07Z |
| format | Article |
| id | doaj.art-c27ca233a5984ba8872e18390fab11d3 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-11T09:13:07Z |
| publishDate | 2017-11-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-c27ca233a5984ba8872e18390fab11d32022-12-22T04:32:26ZengeLife Sciences Publications LtdeLife2050-084X2017-11-01610.7554/eLife.31234Diverse modes of synaptic signaling, regulation, and plasticity distinguish two classes of C. elegans glutamatergic neuronsDonovan Ventimiglia0Cornelia I Bargmann1https://orcid.org/0000-0002-8484-0618Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University, New York, United StatesLulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University, New York, United StatesSynaptic vesicle release properties vary between neuronal cell types, but in most cases the molecular basis of this heterogeneity is unknown. Here, we compare in vivo synaptic properties of two neuronal classes in the C. elegans central nervous system, using VGLUT-pHluorin to monitor synaptic vesicle exocytosis and retrieval in intact animals. We show that the glutamatergic sensory neurons AWCON and ASH have distinct synaptic dynamics associated with tonic and phasic synaptic properties, respectively. Exocytosis in ASH and AWCON is differentially affected by SNARE-complex regulators that are present in both neurons: phasic ASH release is strongly dependent on UNC-13, whereas tonic AWCON release relies upon UNC-18 and on the protein kinase C homolog PKC-1. Strong stimuli that elicit high calcium levels increase exocytosis and retrieval rates in AWCON, generating distinct tonic and evoked synaptic modes. These results highlight the differential deployment of shared presynaptic proteins in neuronal cell type-specific functions.https://elifesciences.org/articles/31234synaptic transmissionsynaptic plasticityendocytosisgenetics |
| spellingShingle | Donovan Ventimiglia Cornelia I Bargmann Diverse modes of synaptic signaling, regulation, and plasticity distinguish two classes of C. elegans glutamatergic neurons eLife synaptic transmission synaptic plasticity endocytosis genetics |
| title | Diverse modes of synaptic signaling, regulation, and plasticity distinguish two classes of C. elegans glutamatergic neurons |
| title_full | Diverse modes of synaptic signaling, regulation, and plasticity distinguish two classes of C. elegans glutamatergic neurons |
| title_fullStr | Diverse modes of synaptic signaling, regulation, and plasticity distinguish two classes of C. elegans glutamatergic neurons |
| title_full_unstemmed | Diverse modes of synaptic signaling, regulation, and plasticity distinguish two classes of C. elegans glutamatergic neurons |
| title_short | Diverse modes of synaptic signaling, regulation, and plasticity distinguish two classes of C. elegans glutamatergic neurons |
| title_sort | diverse modes of synaptic signaling regulation and plasticity distinguish two classes of c elegans glutamatergic neurons |
| topic | synaptic transmission synaptic plasticity endocytosis genetics |
| url | https://elifesciences.org/articles/31234 |
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