Serotonin and the Neuropeptide PDF Initiate and Extend Opposing Behavioral States in C. elegans

• Published in: Cell Vol. 154; no. 5; pp. 1023 - 1035
• Main Authors: Flavell, Steven W., Pokala, Navin, Macosko, Evan Z., Albrecht, Dirk R., Larsch, Johannes, Bargmann, Cornelia I.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 29.08.2013
• Subjects: Animals; Behavior, Animal; Caenorhabditis elegans; Caenorhabditis elegans - physiology; Caenorhabditis elegans Proteins - metabolism; Chloride Channels - metabolism; cyclic AMP; Cyclic AMP - metabolism; foraging; neurons; Neurons - metabolism; neuropeptides; Neuropeptides - metabolism; neurotransmitters; optogenetics; Receptors, G-Protein-Coupled - metabolism; serotonin; Serotonin - metabolism; Signal Transduction
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2013.08.001

Foraging animals have distinct exploration and exploitation behaviors that are organized into discrete behavioral states. Here, we characterize a neuromodulatory circuit that generates long-lasting roaming and dwelling states in Caenorhabditis elegans. We find that two opposing neuromodulators, serotonin and the neuropeptide pigment dispersing factor (PDF), each initiate and extend one behavioral state. Serotonin promotes dwelling states through the MOD-1 serotonin-gated chloride channel. The spontaneous activity of serotonergic neurons correlates with dwelling behavior, and optogenetic modulation of the critical MOD-1-expressing targets induces prolonged dwelling states. PDF promotes roaming states through a Gαs-coupled PDF receptor; optogenetic activation of cAMP production in PDF receptor-expressing cells induces prolonged roaming states. The neurons that produce and respond to each neuromodulator form a distributed circuit orthogonal to the classical wiring diagram, with several essential neurons that express each molecule. The slow temporal dynamics of this neuromodulatory circuit supplement fast motor circuits to organize long-lasting behavioral states. [Display omitted] •Specific neuromodulators are necessary for long-lasting roaming and dwelling states•Serotonergic neurons induce dwelling states through an inhibitory receptor•PDF neuropeptides act through cAMP signaling to induce prolonged roaming states•Optogenetic imitation of serotonin or PDF signaling elicits behavioral changes Two opposing neuromodulators regulate neural circuits with slow temporal dynamics that establish long-lasting alternative behavioral states—roaming and dwelling—related to foraging in C. elegans.