title: Food responsiveness regulates episodic behavioral states inCaenorhabditis elegans.
abstract: Animals optimize survival and reproduction in part through control of behavioral states, which depend on an organism's internal and external environments. In the nematodeCaenorhabditis elegansa variety of behavioral states have been described, including roaming, dwelling, quiescence, and episodic swimming. These states have been considered in isolation under varied experimental conditions, making it difficult to establish a unified picture of how they are regulated. Using long-term imaging, we examinedC. elegansepisodic behavioral states under varied mechanical and nutritional environments. We found that animals alternate between high-activity (active) and low-activity (sedentary) episodes in any mechanical environment, while the incidence of episodes and their behavioral composition depend on food levels. During active episodes, worms primarily roam, as characterized by continuous whole body movement. During sedentary episodes, animals exhibit dwelling (slower movements confined to the anterior half of the body) and quiescence (a complete lack of movement). Roaming, dwelling, and quiescent states are manifest not only through locomotory characteristics but also in pharyngeal pumping (feeding) and in egg-laying behaviors. Next, we analyzed the genetic basis of behavioral states. We found that modulation of behavioral states depends on neuropeptides and insulin-like signaling in the nervous system. Sensory neurons and the Foraging homolog EGL-4 regulate behavior through control of active/sedentary episodes. Optogenetic stimulation of dopaminergic and serotonergic neurons induced dwelling, implicating dopamine as a dwell-promoting neurotransmitter. Our findings provide a more unified description of behavioral states and suggest that perception of nutrition is a conserved mechanism for regulating animal behavior.NEW & NOTEWORTHYOne strategy by which animals adapt to their internal states and external environments is by adopting behavioral states. The roundwormCaenorhabditis elegansis an attractive model for investigating how behavioral states are genetically and neuronally controlled. Here we describe the hierarchical organization of behavioral states characterized by locomotory activity, feeding, and egg-laying. We show that decisions to engage in these behaviors are controlled by the nervous system through insulin-like signaling and the perception of food.
authors.affiliation: Department of Bioengineering, School of Engineering and Applied Sciences, University of Pennsylvania, Philadelphia, Pennsylvania; and.
authors.forename: Richard J
authors.initials: RJ
authors.lastname: McCloskey
authors.affiliation: Department of Bioengineering, School of Engineering and Applied Sciences, University of Pennsylvania, Philadelphia, Pennsylvania; and.
authors.forename: Anthony D
authors.initials: AD
authors.lastname: Fouad
authors.affiliation: Department of Bioengineering, School of Engineering and Applied Sciences, University of Pennsylvania, Philadelphia, Pennsylvania; and.
authors.forename: Matthew A
authors.initials: MA
authors.lastname: Churgin
authors.affiliation: Department of Bioengineering, School of Engineering and Applied Sciences, University of Pennsylvania, Philadelphia, Pennsylvania; and fangyen@seas.upenn.edu.|Department of Neuroscience, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.
authors.forename: Christopher
authors.initials: C
authors.lastname: Fang-Yen
mesh_terms: D000818:Animals; D017173:Caenorhabditis elegans / Q000235:genetics / Q000502:physiology*; D029742:Caenorhabditis elegans Proteins / Q000235:genetics; D017869:Cyclic GMP-Dependent Protein Kinases / Q000235:genetics; D059290:Dopaminergic Neurons / Q000378:metabolism / Q000502:physiology; D005247:Feeding Behavior; D009068:Movement; D012098:Reproduction; D011984:Sensory Receptor Cells / Q000378:metabolism / Q000502:physiology; D059326:Serotonergic Neurons / Q000378:metabolism / Q000502:physiology
chemical_list: D029742:Caenorhabditis elegans Proteins; D017869:Cyclic GMP-Dependent Protein Kinases; C470349:EGL-4 protein, C elegans
keywords: behavioral state; egg-laying; feeding; insulin-like signaling; locomotion