Temporally specific engagement of distinct neuronal circuits regulating olfactory habituation in Drosophila

Elife. 2018 Dec 21;7:e39569. doi: 10.7554/eLife.39569.

Abstract

Habituation is the process that enables salience filtering, precipitating perceptual changes that alter the value of environmental stimuli. To discern the neuronal circuits underlying habituation to brief inconsequential stimuli, we developed a novel olfactory habituation paradigm, identifying two distinct phases of the response that engage distinct neuronal circuits. Responsiveness to the continuous odor stimulus is maintained initially, a phase we term habituation latency and requires Rutabaga Adenylyl-Cyclase-depended neurotransmission from GABAergic Antennal Lobe Interneurons and activation of excitatory Projection Neurons (PNs) and the Mushroom Bodies. In contrast, habituation depends on the inhibitory PNs of the middle Antenno-Cerebral Track, requires inner Antenno-Cerebral Track PN activation and defines a temporally distinct phase. Collectively, our data support the involvement of Lateral Horn excitatory and inhibitory stimulation in habituation. These results provide essential cellular substrates for future analyses of the molecular mechanisms that govern the duration and transition between these distinct temporal habituation phases.

Editorial note: This article has been through an editorial process in which the authors decide how to respond to the issues raised during peer review. The Reviewing Editor's assessment is that all the issues have been addressed (see decision letter).

Keywords: D. melanogaster; Drosophila; lateral horn; mushroom bodies; neuroscience; olfactory habituation; projection neurons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetates / pharmacology
  • Adenylyl Cyclases / genetics
  • Adenylyl Cyclases / metabolism
  • Animals
  • Arthropod Antennae / cytology
  • Arthropod Antennae / drug effects
  • Arthropod Antennae / physiology*
  • Benzaldehydes / pharmacology
  • Diacetyl / pharmacology
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / cytology
  • Drosophila melanogaster / drug effects*
  • Drosophila melanogaster / physiology
  • Gene Expression
  • Hydroxyurea / toxicity
  • Interneurons / cytology
  • Interneurons / drug effects
  • Interneurons / physiology*
  • Mushroom Bodies / cytology
  • Mushroom Bodies / drug effects
  • Mushroom Bodies / physiology*
  • Octanols / pharmacology
  • Odorants / analysis
  • Olfactory Pathways / cytology
  • Olfactory Pathways / drug effects
  • Olfactory Pathways / physiology*
  • Olfactory Receptor Neurons / cytology
  • Olfactory Receptor Neurons / drug effects
  • Olfactory Receptor Neurons / physiology*
  • Smell / physiology*
  • Synaptic Transmission / physiology

Substances

  • Acetates
  • Benzaldehydes
  • Drosophila Proteins
  • Octanols
  • ethyl acetate
  • Adenylyl Cyclases
  • Rut protein, Drosophila
  • Diacetyl
  • benzaldehyde
  • Hydroxyurea

Grant support

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