Unveiling the Dual Role of the Dopaminergic System on Locomotion and the Innate Value for an Aversive Olfactory Stimulus in Drosophila

Neuroscience. 2018 Feb 10:371:433-444. doi: 10.1016/j.neuroscience.2017.12.032. Epub 2017 Dec 29.

Abstract

The communication between sensory systems and the specific brain centers that process this information is crucial to develop adequate behavioral responses. Modulatory systems, including dopaminergic circuits, regulate this communication to finely tune the behavioral response associated to any given stimulus. For instance, the Mushroom Body (MB), an insect brain integration center that receives and processes several sensory stimuli and organizes the execution of motor programs, communicates with MB output neurons (MBONs) to develop behavioral responses associated to olfactory stimuli. This communication is modulated by dopaminergic neural systems. Here we show that silencing dopaminergic neurons increases the aversive response observed in adult flies exposed to Benzaldehyde (Bz) or octanol. We studied the contribution of two dopaminergic clusters that innervate different zones of MB, Protocerebral anterior medial (PAM) and Protocerebral posterior lateral 1 (PPL1), on the innate value to the aversive stimulus and the associated locomotor behavior. In order to do this, we manipulated the synaptic transmission of these neural clusters through the expression of Tetanus toxin, Kir2.1 and Transient receptor potential cation channel A1 (TrpA1) channels. Our results show that neurons in PPL1 and PAM differentially modulate the innate value to Bz in adult flies. On the other hand, blocking neurotransmission or genetic silencing of PAM neurons results in decreased locomotor behavior in flies, an effect not observed when silencing PPL1. Our results suggest that as in mammals, specific dopaminergic pathways differentially modulate locomotor behavior and the innate value for an odorant, a limbic-like response in Drosophila.

Keywords: Drosophila; dopaminergic neurons; motor programs; odor valence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Avoidance Learning / drug effects
  • Avoidance Learning / physiology*
  • Dopamine / metabolism*
  • Drosophila / anatomy & histology
  • Drosophila / metabolism*
  • Drosophila Proteins / metabolism
  • Ion Channels
  • Motor Activity / drug effects
  • Motor Activity / physiology*
  • Mushroom Bodies / cytology
  • Mushroom Bodies / drug effects
  • Mushroom Bodies / metabolism
  • Neurons / cytology
  • Neurons / drug effects
  • Neurons / metabolism
  • Olfactory Perception / drug effects
  • Olfactory Perception / physiology*
  • Potassium Channels, Inwardly Rectifying / antagonists & inhibitors
  • Potassium Channels, Inwardly Rectifying / metabolism
  • Smell / drug effects
  • Smell / physiology
  • Synaptic Transmission / drug effects
  • Synaptic Transmission / physiology
  • TRPA1 Cation Channel / metabolism

Substances

  • Drosophila Proteins
  • Ion Channels
  • Kir2.1 channel
  • Potassium Channels, Inwardly Rectifying
  • TRPA1 Cation Channel
  • TrpA1 protein, Drosophila
  • Dopamine