Optical Dissection of Synaptic Plasticity for Early Adaptation in Caenorhabditis elegans

To understand neuronal information processing, it is essential to investigate the input-output relationship and its modulation via detailed dissections of synaptic transmission between pre- and postsynaptic neurons. In Caenorhabditis elegans, pre-exposure to an odorant for five minutes reduces chemotaxis (early adaptation). AWC sensory neurons and AIY interneurons are crucial for this adaptation; AWC neurons sense volatile odors, and AIY interneurons receive glutamatergic inputs from AWC neurons. However, modulations via early adaptation of the input-output relationship between AWC and AIY are not well characterized. Here we use a variety of fluorescent imaging techniques to show that reduced synaptic-vesicle release without Ca²⁺ modulation in AWC neurons suppresses the Ca²⁺ response in AIY neurons via early adaptation. First, early adaptation modulates the Ca²⁺ response in AIY but not AWC neurons. Adaptation in the Ca²⁺ signal measured in AIY neurons is caused by adaptation in glutamate release from AWC neurons. Further, we found that a G protein γ-subunit, GPC-1, is related to modulation of glutamate input to AIY. Our results dissect the modulation of the pre- and postsynaptic relationship in vivo based on optical methods, and demonstrate the importance of neurotransmitter-release modulation in presynaptic neurons without Ca²⁺ modulation.