RRC ID 83981
Author Nakayama A, Watanabe M, Yamashiro R, Kuroyanagi H, Matsuyama HJ, Oshima A, Mori I, Nakano S.
Title A hyperpolarizing neuron recruits undocked innexin hemichannels to transmit neural information in Caenorhabditis elegans.
Journal Proc Natl Acad Sci U S A
Abstract While depolarization of the neuronal membrane is known to evoke the neurotransmitter release from synaptic vesicles, hyperpolarization is regarded as a resting state of chemical neurotransmission. Here, we report that hyperpolarizing neurons can actively signal neural information by employing undocked hemichannels. We show that UNC-7, a member of the innexin family in Caenorhabditis elegans, functions as a hemichannel in thermosensory neurons and transmits temperature information from the thermosensory neurons to their postsynaptic interneurons. By monitoring neural activities in freely behaving animals, we find that hyperpolarizing thermosensory neurons inhibit the activity of the interneurons and that UNC-7 hemichannels regulate this process. UNC-7 is required to control thermotaxis behavior and functions independently of synaptic vesicle exocytosis. Our findings suggest that innexin hemichannels mediate neurotransmission from hyperpolarizing neurons in a manner that is distinct from the synaptic transmission, expanding the way of neural circuitry operations.
Volume 121(21)
Pages e2406565121
Published 2024-5-21
DOI 10.1073/pnas.2406565121
PMID 38753507
PMC PMC11127054
MeSH Animals Caenorhabditis elegans* / metabolism Caenorhabditis elegans Proteins* / genetics Caenorhabditis elegans Proteins* / metabolism Connexins / genetics Connexins / metabolism Interneurons / metabolism Membrane Proteins Neurons* / metabolism Synaptic Transmission* / physiology Synaptic Vesicles / metabolism Taxis Response / physiology
Resource
C.elegans tm1896 tm3524 tm5027 tm4886 tm3485 tm10647 tm14359 tm1983 tm2569 tm2984 tm3886 tm790 tm11713 tm5180 tm10648 tm4639 tm1875 tm5158 tm6467 tm3023