Activity of defined mushroom body output neurons underlies learned olfactory behavior in Drosophila

Neuron. 2015 Apr 22;86(2):417-27. doi: 10.1016/j.neuron.2015.03.025. Epub 2015 Apr 9.

Abstract

During olfactory learning in fruit flies, dopaminergic neurons assign value to odor representations in the mushroom body Kenyon cells. Here we identify a class of downstream glutamatergic mushroom body output neurons (MBONs) called M4/6, or MBON-β2β'2a, MBON-β'2mp, and MBON-γ5β'2a, whose dendritic fields overlap with dopaminergic neuron projections in the tips of the β, β', and γ lobes. This anatomy and their odor tuning suggests that M4/6 neurons pool odor-driven Kenyon cell synaptic outputs. Like that of mushroom body neurons, M4/6 output is required for expression of appetitive and aversive memory performance. Moreover, appetitive and aversive olfactory conditioning bidirectionally alters the relative odor-drive of M4β' neurons (MBON-β'2mp). Direct block of M4/6 neurons in naive flies mimics appetitive conditioning, being sufficient to convert odor-driven avoidance into approach, while optogenetically activating these neurons induces avoidance behavior. We therefore propose that drive to the M4/6 neurons reflects odor-directed behavioral choice.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Appetitive Behavior / physiology*
  • Avoidance Learning / physiology
  • Brain / physiology
  • Dopaminergic Neurons / physiology*
  • Drosophila / physiology*
  • Drosophila Proteins / genetics
  • Gene Expression
  • Mushroom Bodies / innervation*
  • Neurons / physiology
  • Smell / physiology*
  • Transcription Factors / genetics

Substances

  • Drosophila Proteins
  • GAL4 protein, Drosophila
  • Transcription Factors