Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster

J Comp Neurol. 2016 Jun 15;524(9):1920-56. doi: 10.1002/cne.23966. Epub 2016 Mar 9.

Abstract

In Drosophila melanogaster olfactory sensory neurons (OSNs) establish synapses with projection neurons (PNs) and local interneurons within antennal lobe (AL) glomeruli. Substantial knowledge regarding this circuitry has been obtained by functional studies, whereas ultrastructural evidence of synaptic contacts is scarce. To fill this gap, we studied serial sections of three glomeruli using electron microscopy. Ectopic expression of a membrane-bound peroxidase allowed us to map synaptic sites along PN dendrites. Our data prove for the first time that each of the three major types of AL neurons is both pre- and postsynaptic to the other two types, as previously indicated by functional studies. PN dendrites carry a large proportion of output synapses, with approximately one output per every three input synapses. Detailed reconstructions of PN dendrites showed that these synapses are distributed unevenly, with input and output sites partially segregated along a proximal-distal gradient and the thinnest branches carrying solely input synapses. Moreover, our data indicate synapse clustering, as we found evidence of dendritic tiling of PN dendrites. PN output synapses exhibited T-shaped presynaptic densities, mostly arranged as tetrads. In contrast, output synapses from putative OSNs showed elongated presynaptic densities in which the T-bar platform was supported by several pedestals and contacted as many as 20 postsynaptic profiles. We also discovered synaptic contacts between the putative OSNs. The average synaptic density in the glomerular neuropil was about two synapses/µm(3) . These results are discussed with regard to current models of olfactory glomerular microcircuits across species.

Keywords: Drosophila melanogaster; glomerulus; olfactory system; projection neuron; synaptic microcircuits; ultrastructure.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Arthropod Antennae / cytology*
  • Arthropod Antennae / ultrastructure
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / anatomy & histology*
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Imaging, Three-Dimensional
  • Microscopy, Confocal
  • Microscopy, Electron, Transmission
  • Models, Anatomic
  • Neuropil / physiology*
  • Neuropil / ultrastructure
  • Synapses / physiology*
  • Synapses / ultrastructure

Substances

  • Drosophila Proteins
  • Green Fluorescent Proteins