A single neuron in C. elegans orchestrates multiple motor outputs through parallel modes of transmission

• Published in: Current biology 2023-10, Vol.33 (20), p.4430-4445.e6
• Main Authors: Huang, Yung-Chi, Luo, Jinyue, Huang, Wenjia, Baker, Casey M., Gomes, Matthew A., Meng, Bohan, Byrne, Alexandra B., Flavell, Steven W.
• Format: Article
• Language: English
• Subjects: Animals; Caenorhabditis elegans - physiology; Caenorhabditis elegans Proteins; Motor Neurons - physiology; Oviposition - physiology; Serotonergic Neurons; Serotonin - physiology
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2023.08.088

Animals generate a wide range of highly coordinated motor outputs, which allows them to execute purposeful behaviors. Individual neurons in the circuits that generate behaviors have a remarkable capacity for flexibility as they exhibit multiple axonal projections, transmitter systems, and modes of neural activity. How these multi-functional properties of neurons enable the generation of adaptive behaviors remains unknown. Here, we show that the HSN neuron in C. elegans evokes multiple motor programs over different timescales to enable a suite of behavioral changes during egg laying. Using HSN activity perturbations and in vivo calcium imaging, we show that HSN acutely increases egg laying and locomotion while also biasing the animals toward low-speed dwelling behavior over minutes. The acute effects of HSN on egg laying and high-speed locomotion are mediated by separate sets of HSN transmitters and different HSN axonal compartments. The long-lasting effects on dwelling are mediated in part by HSN release of serotonin, which is taken up and re-released by NSM, another serotonergic neuron class that directly evokes dwelling. Our results show how the multi-functional properties of a single neuron allow it to induce a coordinated suite of behaviors and also reveal that neurons can borrow serotonin from one another to control behavior. •The HSN neuron elicits acute egg laying and speeding, as well as long-term slowing•HSN controls egg laying and speeding using distinct transmitters and compartments•HSN promotes long-term slowing through serotonin release•HSN serotonin is taken up and re-released by NSM neurons, which drive slowing Animals generate purposeful behaviors through coordinated motor outputs. Here, Huang et al. show that the HSN neuron in C. elegans evokes multiple motor programs over different timescales to enable a range of behavioral changes during egg laying. The study also reveals that neurons can borrow serotonin from one another to control behavior.