Molecular and Sensory Basis of a Food Related Two-State Behavior in C. elegans

Abstract

Most animals display multiple behavioral states and control the time allocation to each of their activity phases depending on their environment. Here we develop a new quantitative method to analyze Caenorhabditis elegans behavioral states. We show that the dwelling and roaming two-state behavior of C. elegans is tightly controlled by the concentration of food in the environment of the animal. Sensory perception through the amphid neurons is necessary to extend roaming phases while internal metabolic perception of food nutritional value is needed to induce dwelling. Our analysis also shows that the proportion of time spent in each state is modulated by past nutritional experiences of the animal. This two-state behavior is regulated through serotonin as well as insulin and TGF-beta signaling pathways. We propose a model where food nutritional value is assessed through internal metabolic signaling. Biogenic amines signaling could allow the worm to adapt to fast changes in the environment when peptide transcriptional pathways may mediate slower adaptive changes.

TMC-1 attenuates C. elegans development and sexual behaviour in a chemically defined food environment

“…Previous studies found that locomotor activity is linked to an animal's nutritional state; food-stressed animals seek food and increase exploratory behaviour, whereas food-satiated animals decrease exploratory behaviour 7,20,21 . We found that wild-type L1 larvae moved faster than tmc-1(rg1003) mutants on CeMM plates after 30 min of exposure, whereas on food-deprived NGM plates the locomotion rates for both groups of worms were much higher, but equivalent (Fig.…”

The ETS-5 transcription factor regulates activity states in Caenorhabditis elegans by controlling satiety

“…When malnourished, animals seek out a new food source by actively exploring their environment (roaming), whereas animals that are well fed tend to explore less (dwelling) and when fully sated enter a quiescent or sleep-like state (1-3, 8, 9). Transitions between these behavioral states can be regulated by sensory perception of external stimuli and through gut signals or other internal cues that are generated according to food quality (3,4,6).…”

“…In invertebrates and vertebrates, appetite, locomotor activity, and sleep rhythms are all driven by nutritional state (1)(2)(3)(4)(5)(6)(7). When malnourished, animals seek out a new food source by actively exploring their environment (roaming), whereas animals that are well fed tend to explore less (dwelling) and when fully sated enter a quiescent or sleep-like state (1-3, 8, 9).…”

“…Nematodes exhibit different behaviors when cultured on low-quality food compared to high-quality food, with high-quality food defined as a superior supporter of worm growth (1,4). Sensory perception of food in the environment can promote roaming, whereas internal perception of food abundance in the intestine promotes dwelling (3). As such, animals that are unable to sense their environment, and thus cannot sense the presence of food, exhibit reduced time spent roaming (9).…”

“…Postprandial somnolence is thought to reflect an increase in the tone of the parasympathetic nervous system relative to the sympathetic nervous system, as well as altered activity of arousal circuits as a result of increased blood glucose levels, although the pathways mediating these effects are poorly understood (15). In C. elegans, neuronal signaling pathways using serotonin (5-HT), pigment-dispersing factor (PDF) neuropeptides, TGF-β, and the cGMP-dependent protein kinase EGL-4 regulate roaming, dwelling, and quiescent behaviors (1)(2)(3)9). These modulators of foodregulated behavior function in dedicated, mostly nonoverlapping neuronal circuits that detect environmental cues, along with evaluating internal metabolic status (2); however, the transcriptional control of food-regulated behaviors has not yet been defined.…”