Mushroom body output neurons encode valence and guide memory-based action selection in Drosophila

Elife. 2014 Dec 23:3:e04580. doi: 10.7554/eLife.04580.

Abstract

Animals discriminate stimuli, learn their predictive value and use this knowledge to modify their behavior. In Drosophila, the mushroom body (MB) plays a key role in these processes. Sensory stimuli are sparsely represented by ∼2000 Kenyon cells, which converge onto 34 output neurons (MBONs) of 21 types. We studied the role of MBONs in several associative learning tasks and in sleep regulation, revealing the extent to which information flow is segregated into distinct channels and suggesting possible roles for the multi-layered MBON network. We also show that optogenetic activation of MBONs can, depending on cell type, induce repulsion or attraction in flies. The behavioral effects of MBON perturbation are combinatorial, suggesting that the MBON ensemble collectively represents valence. We propose that local, stimulus-specific dopaminergic modulation selectively alters the balance within the MBON network for those stimuli. Our results suggest that valence encoded by the MBON ensemble biases memory-based action selection.

Keywords: D. melanogaster; action selection; behavioral valence; memory; mushroom body; neuroscience; population code; sleep.

Publication types

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

MeSH terms

  • Animals
  • Appetitive Behavior / radiation effects
  • Association Learning / radiation effects
  • Avoidance Learning / radiation effects
  • Behavior, Animal / radiation effects
  • Choice Behavior* / radiation effects
  • Drosophila melanogaster / cytology*
  • Drosophila melanogaster / physiology*
  • Light
  • Memory* / radiation effects
  • Models, Neurological
  • Mushroom Bodies / cytology*
  • Mushroom Bodies / innervation*
  • Mushroom Bodies / radiation effects
  • Neurons / physiology*
  • Neurons / radiation effects
  • Odorants
  • Sleep / radiation effects
  • Time Factors
  • Vision, Ocular