A Neural Circuit Arbitrates between Persistence and Withdrawal in Hungry Drosophila

Neuron. 2019 Nov 6;104(3):544-558.e6. doi: 10.1016/j.neuron.2019.07.028. Epub 2019 Aug 27.

Abstract

In pursuit of food, hungry animals mobilize significant energy resources and overcome exhaustion and fear. How need and motivation control the decision to continue or change behavior is not understood. Using a single fly treadmill, we show that hungry flies persistently track a food odor and increase their effort over repeated trials in the absence of reward suggesting that need dominates negative experience. We further show that odor tracking is regulated by two mushroom body output neurons (MBONs) connecting the MB to the lateral horn. These MBONs, together with dopaminergic neurons and Dop1R2 signaling, control behavioral persistence. Conversely, an octopaminergic neuron, VPM4, which directly innervates one of the MBONs, acts as a brake on odor tracking by connecting feeding and olfaction. Together, our data suggest a function for the MB in internal state-dependent expression of behavior that can be suppressed by external inputs conveying a competing behavioral drive.

Keywords: DopR2; Drosophila melanogaster; dopamine; foraging; goal-directed behavior; learning; mushroom body; octopamine; olfactory system; persistence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Appetitive Behavior / physiology*
  • Behavior, Animal
  • Dopamine / metabolism*
  • Dopaminergic Neurons / metabolism
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster
  • Food
  • Hunger
  • Motivation*
  • Mushroom Bodies / cytology
  • Mushroom Bodies / metabolism*
  • Mushroom Bodies / physiology
  • Neural Pathways / physiology
  • Neurons / metabolism*
  • Octopamine / metabolism*
  • Odorants
  • Receptors, Dopamine D1 / metabolism
  • Reward
  • Smell

Substances

  • Dop1R2 protein, Drosophila
  • Drosophila Proteins
  • Receptors, Dopamine D1
  • Octopamine
  • Dopamine