Iwanir, Shachar et al. (2015) International Worm Meeting "Serotonin promotes exploitation in complex environments by accelerating decision-making.."

Brown, Adam, Biron, David, Iwanir, Shachar, Najjar, Dana, Nagy, Stanislav

[International Worm Meeting, 2015]

When resources are not uniformly available, fast responses can provide a competitive advantage. The neurotransmitter serotonin (5-HT) was shown affect C. elegans locomotion on food in steady-state and following a period of food deprivation. We identified a novel role of 5-HT signaling in C. elegans: mediating a rapid response required for efficient exploitation in complex environments. Deficiency in 5-HT synthes­is, as well as genetic ablation of serotonergic neurons, resulted in gradual responses and defective exploitation. Both the ADF and NSM serotonergic neuronal types were implicated in these responses, albeit in different ways. Collectively, physiological imaging, genetic silencing, functional rescues, and optogenetic activation revealed that NSM responses initiated upon encounter and were key to rapid decision-making. In contrast, the onset of ADF responses preceded the physical encounter with the food. The relevance of responding rapidly was demonstrated in patchy environments, where the absence of 5-HT signaling significantly reduced exploitation. Collectively, our results suggest a novel role for 5-HT in decision-making, demonstrate its fitness consequences, and show that NSM and ADF act in concert to modulate locomotion in complex environments. .

Iwanir, Shachar et al. (2013) International Worm Meeting "A calcium-rich breakfast: physiological activity in C. elegans serotonergic neurons during the enhanced slowing response and upon emergence from lethargus."

Palmer, Meagan, Fitzgerald, Ivy, Brown, Adam, Iwanir, Shachar, Najjar, Dana, Biron, David

[International Worm Meeting, 2013]

Serotonin has been implicated in the assessment of resource availability and in the modulation of sleep in vertebrates. Extracellular serotonin levels in the hypothalamus are increased by the presence of food. Additionally, the firing of serotonergic cells in the brainstem raphe nuclei is tonic during wakefulness and significantly reduced during sleep states. In the nematode Caenorhabditis elegans, serotonin signaling has been shown to mediate the enhancing effect of starvation on the slowing response to encountering a food source. However, the understanding of the cellular mechanisms and physiological dynamics underlying this response is incomplete. We combined behavioral studies with physiological imaging of calcium dynamics in the serotonergic NSM and ADF neurons of freely-behaving animals in order to compare the responses to reintroduction of food in two situations: following a period of food deprivation and at the emergence from lethargus, a sleep-like state that involves a cessation of feeding. We identified similarities in the patterns of locomotion and physiological activity of NSM between these two circumstances. The enhanced slowing response was characterized by two phases: (i) preceding a spatial encounter with food, physiological activity in ADF neurons increased (likely via a chemosensory mechanism), concomitant with a gradual decrease in the rate of locomotion, and (ii) upon encountering food, NSM exhibited calcium transients lasting 1-2 minutes, accompanied by a sharp decrease in the rate of locomotion. Emergence from lethargus was associated with a period of extensive feeding and reduced locomotion, accompanied by a transient increased activity in NSM (but not ADF). Our results may point to a common origin of the modulation of serotonin signaling by arousal and feeding states, and suggest roles for both chemosensation and metabolic cues in the regulation of the enhanced slowing response.