Food Sensation Modulates Locomotion by Dopamine and Neuropeptide Signaling in a Distributed Neuronal Network

Neuron. 2018 Dec 19;100(6):1414-1428.e10. doi: 10.1016/j.neuron.2018.10.024. Epub 2018 Nov 1.

Abstract

Finding food and remaining at a food source are crucial survival strategies. We show how neural circuits and signaling molecules regulate these food-related behaviors in Caenorhabditis elegans. In the absence of food, AVK interneurons release FLP-1 neuropeptides that inhibit motorneurons to regulate body posture and velocity, thereby promoting dispersal. Conversely, AVK photoinhibition promoted dwelling behavior. We identified FLP-1 receptors required for these effects in distinct motoneurons. The DVA interneuron antagonizes signaling from AVK by releasing cholecystokinin-like neuropeptides that potentiate cholinergic neurons, in response to dopaminergic neurons that sense food. Dopamine also acts directly on AVK via an inhibitory dopamine receptor. Both AVK and DVA couple to head motoneurons by electrical and chemical synapses to orchestrate either dispersal or dwelling behavior, thus integrating environmental and proprioceptive signals. Dopaminergic regulation of food-related behavior, via similar neuropeptides, may be conserved in mammals.

Keywords: Ca2+ imaging; FMRFamide neuropeptides; behavioral quantification; behavioral switching; channelrhodopsin-2; halorhodopsin; optogenetics; premotor navigational regulation; sensory integration; video tracking.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Calcium / metabolism
  • Channelrhodopsins / genetics
  • Channelrhodopsins / metabolism
  • Dopamine / metabolism
  • Dopamine / pharmacology*
  • Food*
  • Locomotion / drug effects*
  • Neural Pathways / drug effects
  • Neural Pathways / physiology*
  • Neuropeptides / metabolism
  • Neuropeptides / pharmacology*
  • Optogenetics
  • Receptors, Dopamine / genetics
  • Receptors, Dopamine / physiology
  • Sensation / physiology*
  • Sensory Receptor Cells / drug effects*
  • Sensory Receptor Cells / physiology

Substances

  • Caenorhabditis elegans Proteins
  • Channelrhodopsins
  • Neuropeptides
  • Receptors, Dopamine
  • Calcium
  • Dopamine