Short- and long-term memory in Drosophila require cAMP signaling in distinct neuron types

Curr Biol. 2009 Aug 25;19(16):1341-50. doi: 10.1016/j.cub.2009.07.016. Epub 2009 Jul 30.


Background: A common feature of memory and its underlying synaptic plasticity is that each can be dissected into short-lived forms involving modification or trafficking of existing proteins and long-term forms that require new gene expression. An underlying assumption of this cellular view of memory consolidation is that these different mechanisms occur within a single neuron. At the neuroanatomical level, however, different temporal stages of memory can engage distinct neural circuits, a notion that has not been conceptually integrated with the cellular view.

Results: Here, we investigated this issue in the context of aversive Pavlovian olfactory memory in Drosophila. Previous studies have demonstrated a central role for cAMP signaling in the mushroom body (MB). The Ca(2+)-responsive adenylyl cyclase RUTABAGA is believed to be a coincidence detector in gamma neurons, one of the three principle classes of MB Kenyon cells. We were able to separately restore short-term or long-term memory to a rutabaga mutant with expression of rutabaga in different subsets of MB neurons.

Conclusions: Our findings suggest a model in which the learning experience initiates two parallel associations: a short-lived trace in MB gamma neurons, and a long-lived trace in alpha/beta neurons.

Publication types

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

MeSH terms

  • Adenylyl Cyclases / deficiency
  • Adenylyl Cyclases / genetics
  • Adenylyl Cyclases / physiology*
  • Animals
  • Animals, Genetically Modified
  • Avoidance Learning / physiology
  • Conditioning, Classical / physiology
  • Cyclic AMP / physiology*
  • Drosophila Proteins / deficiency
  • Drosophila Proteins / genetics
  • Drosophila Proteins / physiology*
  • Drosophila melanogaster / cytology
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / physiology*
  • Female
  • Gene Knockout Techniques
  • Genetic Complementation Test
  • Male
  • Memory / physiology*
  • Memory, Short-Term / physiology
  • Mushroom Bodies / cytology
  • Mushroom Bodies / physiology*
  • Neurons / classification
  • Neurons / physiology*
  • Point Mutation
  • Recombinant Fusion Proteins / physiology
  • Retention, Psychology / physiology
  • Second Messenger Systems / physiology*
  • Smell / physiology


  • Drosophila Proteins
  • Recombinant Fusion Proteins
  • Cyclic AMP
  • Adenylyl Cyclases
  • Rut protein, Drosophila