Author:

Abstract:

Finding a food source and staying in its vicinity is a crucial survival strategy. How neuronal circuits integrate multiple sensory cues from the environment, and from the body, to maintain locomotion towards a food source and to help the animal to remain at it, is a relevant problem, requiring coordination of long-term navigational strategies and “local” fine-control of body movements. We analyzed a network of neurons controlling body posture and locomotion strategy in food related behaviors. We used an unbiased optogenetic approach to characterize the AVK interneurons. We expressed Channelrhodopsin (ChR2) and Halorhodopsin (NpHR) in AVK. Upon photoinhibition in the absence of food, animals showed increased body curvature and highly irregular locomotion, while AVK photostimulation had no effect. OFF food, AVK releases FLP-1 neuropeptides to inhibit subsets of motor neurons and other cells to alter locomotion of the animal. Body curvature is reduced by FLP-1; conversely, when its release is inhibited, curvature increases. We found that AVK is inhibited by the presence of food, and in this situation, i.e. ON food, photoactivation of AVK leads to FLP-1 peptide release and to decreased bending angles. Thus, food modulates the activity state of AVK. Synthetic FLP-1 peptides inhibited cholinergic motor neurons at the NMJ. We identified a FLP-1 receptor required for AVK-FLP-1 effects: NPR-6 is expressed in VC motor neurons, and in further neurons required for chemosensation and feeding, and NPR-6 was activated by FLP-1 peptides in a cell culture assay. The inhibition of AVK by food is in part mediated by dopaminergic (DA) PDE neurons that sense food. Consequently, photostimulation of the DA cells reduced body curvature. PDE neurons innervate and modulate (via the DOP-3 receptor) another neuron affecting body curvature, the proprioceptive DVA cell, which releases excitatory NLP-12 neuropeptides onto motor neurons. Photoexcitation and -inhibition of DVA increased and reduced bending, respectively, thus AVK and DVA work in opposite ways. Both AVK and DVA neurons are coupled to SMB head motor neurons, by chemical synapses (AVK, DVA) and by gap junctions (AVK). Eliminating SMB or gap junctions connecting AVK-SMB, both phenocopied effects of AVK ablation on bending angles. Hence, a network of DA neurons, responding to food, modulates signaling through peptidergic AVK and DVA neurons, that both affect motor neurons in the head and body to alter locomotion behavior.