A hyperpolarizing neuron recruits undocked innexin hemichannels to transmit neural information in Caenorhabditis elegans

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 undock...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2024-05, Vol.121 (21), p.e2406565121
Main Authors: Nakayama, Airi, Watanabe, Masakatsu, Yamashiro, Riku, Kuroyanagi, Hiroo, Matsuyama, Hironori J, Oshima, Atsunori, Mori, Ikue, Nakano, Shunji
Format: Article
Language:English
Subjects:
Animals
Biological Sciences
Caenorhabditis elegans
Caenorhabditis elegans - metabolism
Caenorhabditis elegans Proteins - genetics
Caenorhabditis elegans Proteins - metabolism
Circuits
Connexins - genetics
Connexins - metabolism
Depolarization
Exocytosis
Hyperpolarization
Interneurons
Interneurons - metabolism
Membrane potential
Membrane Proteins
Neural networks
Neurons
Neurons - metabolism
Neurotransmission
Neurotransmitter release
Synaptic transmission
Synaptic Transmission - physiology
Synaptic vesicles
Synaptic Vesicles - metabolism
Taxis Response - physiology
Thermotaxis
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Summary: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 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.
ISSN:0027-8424
1091-6490
1091-6490
DOI:10.1073/pnas.2406565121