Heterosynaptic Plasticity Underlies Aversive Olfactory Learning in Drosophila

Neuron. 2015 Dec 2;88(5):985-998. doi: 10.1016/j.neuron.2015.11.003.

Abstract

Although associative learning has been localized to specific brain areas in many animals, identifying the underlying synaptic processes in vivo has been difficult. Here, we provide the first demonstration of long-term synaptic plasticity at the output site of the Drosophila mushroom body. Pairing an odor with activation of specific dopamine neurons induces both learning and odor-specific synaptic depression. The plasticity induction strictly depends on the temporal order of the two stimuli, replicating the logical requirement for associative learning. Furthermore, we reveal that dopamine action is confined to and distinct across different anatomical compartments of the mushroom body lobes. Finally, we find that overlap between sparse representations of different odors defines both stimulus specificity of the plasticity and generalizability of associative memories across odors. Thus, the plasticity we find here not only manifests important features of associative learning but also provides general insights into how a sparse sensory code is read out.

Publication types

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

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Avoidance Learning / physiology*
  • Calcium
  • Drosophila
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Excitatory Postsynaptic Potentials / physiology
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Nerve Net / physiology*
  • Neuronal Plasticity / physiology*
  • Odorants
  • Olfactory Bulb / cytology*
  • Olfactory Bulb / physiology*
  • Optogenetics
  • Patch-Clamp Techniques
  • Photic Stimulation
  • Sensory Receptor Cells / drug effects
  • Sensory Receptor Cells / physiology*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism

Substances

  • Drosophila Proteins
  • GAL4 protein, Drosophila
  • Transcription Factors
  • Green Fluorescent Proteins
  • Calcium