Gamma neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila

Curr Biol. 2012 Apr 10;22(7):608-14. doi: 10.1016/j.cub.2012.02.014. Epub 2012 Mar 15.

Abstract

Mushroom body (MB)-dependent olfactory learning in Drosophila provides a powerful model to investigate memory mechanisms. MBs integrate olfactory conditioned stimulus (CS) inputs with neuromodulatory reinforcement (unconditioned stimuli, US), which for aversive learning is thought to rely on dopaminergic (DA) signaling to DopR, a D1-like dopamine receptor expressed in MBs. A wealth of evidence suggests the conclusion that parallel and independent signaling occurs downstream of DopR within two MB neuron cell types, with each supporting half of memory performance. For instance, expression of the Rutabaga (Rut) adenylyl cyclase in γ neurons is sufficient to restore normal learning to rut mutants, whereas expression of Neurofibromatosis 1 (NF1) in α/β neurons is sufficient to rescue NF1 mutants. DopR mutations are the only case where memory performance is fully eliminated, consistent with the hypothesis that DopR receives the US inputs for both γ and α/β lobe traces. We demonstrate, however, that DopR expression in γ neurons is sufficient to fully support short- and long-term memory. We argue that DA-mediated CS-US association is formed in γ neurons followed by communication between γ and α/β neurons to drive consolidation.

Publication types

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

MeSH terms

  • Adenylyl Cyclases / metabolism
  • Animals
  • Avoidance Learning
  • Conditioning, Classical
  • Dopaminergic Neurons / physiology
  • Drosophila Proteins / metabolism*
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / physiology*
  • Memory, Long-Term
  • Memory, Short-Term
  • Models, Animal
  • Motor Neurons, Gamma / physiology
  • Mushroom Bodies / physiology*
  • Nerve Tissue Proteins / metabolism
  • Receptors, Dopamine / metabolism*
  • Signal Transduction
  • Smell
  • ras GTPase-Activating Proteins / metabolism

Substances

  • Dop1R1 protein, Drosophila
  • Drosophila Proteins
  • NF1 protein, Drosophila
  • Nerve Tissue Proteins
  • Receptors, Dopamine
  • ras GTPase-Activating Proteins
  • Adenylyl Cyclases