The anterior paired lateral neuron normalizes odour-evoked activity in the Drosophila mushroom body calyx

Elife. 2021 Dec 29:10:e74172. doi: 10.7554/eLife.74172.

Abstract

To identify and memorize discrete but similar environmental inputs, the brain needs to distinguish between subtle differences of activity patterns in defined neuronal populations. The Kenyon cells (KCs) of the Drosophila adult mushroom body (MB) respond sparsely to complex olfactory input, a property that is thought to support stimuli discrimination in the MB. To understand how this property emerges, we investigated the role of the inhibitory anterior paired lateral (APL) neuron in the input circuit of the MB, the calyx. Within the calyx, presynaptic boutons of projection neurons (PNs) form large synaptic microglomeruli (MGs) with dendrites of postsynaptic KCs. Combining electron microscopy (EM) data analysis and in vivo calcium imaging, we show that APL, via inhibitory and reciprocal synapses targeting both PN boutons and KC dendrites, normalizes odour-evoked representations in MGs of the calyx. APL response scales with the PN input strength and is regionalized around PN input distribution. Our data indicate that the formation of a sparse code by the KCs requires APL-driven normalization of their MG postsynaptic responses. This work provides experimental insights on how inhibition shapes sensory information representation in a higher brain centre, thereby supporting stimuli discrimination and allowing for efficient associative memory formation.

Keywords: APL; D. melanogaster; inhibition; microglomerulus; mushroom body; neuroscience; pattern separation; sparse coding.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium / analysis
  • Drosophila melanogaster / physiology*
  • Female
  • Male
  • Microscopy, Confocal
  • Microscopy, Electron
  • Mushroom Bodies / physiology*
  • Mushroom Bodies / ultrastructure
  • Neurons / physiology
  • Neurons / ultrastructure*
  • Presynaptic Terminals
  • Smell / physiology*

Substances

  • Calcium

Associated data

  • Dryad/10.5061/dryad.bk3j9kdd1

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.