Diverse modes of synaptic signaling, regulation, and plasticity distinguish two classes of C. elegans glutamatergic neurons.

Donovan Ventimiglia,Cornelia I Bargmann

doi:10.7554/elife.31234

Abstract

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.

Highlights

Neurotransmitter release is a highly regulated process that varies at different synapses, and at the same synapse over time (Atwood and Karunanithi, 2002)
Using vesicular glutamate transporter (VGLUT)-pHluorin fusions, we show that the release and retrieval of glutamatergic synaptic vesicles in two sensory neurons, AWCON and ASH, are kinetically distinct and matched to their signaling properties
Based on calcium imaging studies, the AWCON olfactory neurons are tonically active at rest, inhibited by odor stimuli, and transiently activated upon odor removal before a return to baseline (Chalasani et al, 2007; Gordus et al, 2015; Kato et al, 2014) (Figure 1A)

Summary

Introduction

Neurotransmitter release is a highly regulated process that varies at different synapses, and at the same synapse over time (Atwood and Karunanithi, 2002). Studies in the zebrafish retina represent one example in which synapses of two distinct neuronal classes, ON- and OFF-bipolar cells, have been compared in vivo in intact animals, leading to insights into their similarities and differences (Odermatt et al, 2012). We extend this approach to the central nervous system of the nematode worm Caenorhabditis elegans, and relate diversity in synaptic properties to requirements for specific synaptic proteins in individual neurons. The synaptic properties of neurons in the central nervous system have only begun to be explored (Lindsay et al, 2011)

Methods

Results

Conclusion