ON selectivity in the Drosophila visual system is a multisynaptic process involving both glutamatergic and GABAergic inhibition

Elife. 2019 Sep 19:8:e49373. doi: 10.7554/eLife.49373.

Abstract

Sensory systems sequentially extract increasingly complex features. ON and OFF pathways, for example, encode increases or decreases of a stimulus from a common input. This ON/OFF pathway split is thought to occur at individual synaptic connections through a sign-inverting synapse in one of the pathways. Here, we show that ON selectivity is a multisynaptic process in the Drosophila visual system. A pharmacogenetics approach demonstrates that both glutamatergic inhibition through GluClα and GABAergic inhibition through Rdl mediate ON responses. Although neurons postsynaptic to the glutamatergic ON pathway input L1 lose all responses in GluClα mutants, they are resistant to a cell-type-specific loss of GluClα. This shows that ON selectivity is distributed across multiple synapses, and raises the possibility that cell-type-specific manipulations might reveal similar strategies in other sensory systems. Thus, sensory coding is more distributed than predicted by simple circuit motifs, allowing for robust neural processing.

Keywords: D. melanogaster; GABAergic inhibition; ON selectivity; distributed coding; feature extraction; glutamatergic inhibition; neuroscience; vision.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Drosophila / physiology*
  • Excitatory Amino Acid Agents / metabolism
  • GABA Agents / metabolism
  • Interneurons / physiology*
  • Models, Neurological
  • Visual Pathways / physiology*
  • Visual Perception*

Substances

  • Excitatory Amino Acid Agents
  • GABA Agents

Associated data

  • GEO/GSE103772
  • GEO/GSE116969