Synaptic activity in serotonergic neurons is required for air-puff stimulated flight in Drosophila melanogaster

PLoS One. 2012;7(9):e46405. doi: 10.1371/journal.pone.0046405. Epub 2012 Sep 27.

Abstract

Background: Flight is an integral component of many complex behavioral patterns in insects. The giant fiber circuit has been well studied in several insects including Drosophila. However, components of the insect flight circuit that respond to an air-puff stimulus and comprise the flight central pattern generator are poorly defined. Aminergic neurons have been implicated in locust, moth and Drosophila flight. Here we have investigated the requirement of neuronal activity in serotonergic neurons, during development and in adults, on air-puff induced flight in Drosophila.

Methodology/principal findings: To target serotonergic neurons specifically, a Drosophila strain that contains regulatory regions from the TRH (Tryptophan Hydroxylase) gene linked to the yeast transcription factor GAL4 was used. By blocking synaptic transmission from serotonergic neurons with a tetanus toxin transgene or by hyperpolarisation with Kir2.1, close to 50% adults became flightless. Temporal expression of a temperature sensitive Dynamin mutant transgene (Shi(ts)) suggests that synaptic function in serotonergic neurons is required both during development and in adults. Depletion of IP(3)R in serotonergic neurons via RNAi did not affect flight. Interestingly, at all stages a partial requirement for synaptic activity in serotonergic neurons was observed. The status of serotonergic neurons was investigated in the central nervous system of larvae and adults expressing tetanus toxin. A small but significant reduction was observed in serotonergic cell number in adult second thoracic segments from flightless tetanus toxin expressing animals.

Conclusions: These studies show that loss of synaptic activity in serotonergic neurons causes a flight deficit. The temporal focus of the flight deficit is during pupal development and in adults. The cause of the flight deficit is likely to be loss of neurons and reduced synaptic function. Based on the partial phenotypes, serotonergic neurons appear to be modulatory, rather than an intrinsic part of the flight circuit.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Count
  • Central Nervous System / cytology
  • Central Nervous System / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / physiology*
  • Dynamins / genetics
  • Dynamins / metabolism
  • Flight, Animal / physiology*
  • Gene Expression Regulation, Developmental
  • Larva / physiology
  • Potassium Channels, Inwardly Rectifying / genetics
  • Potassium Channels, Inwardly Rectifying / metabolism
  • Pupa / physiology
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism
  • Serotonergic Neurons / cytology
  • Serotonergic Neurons / metabolism*
  • Synaptic Transmission / physiology*
  • Tetanus Toxin / genetics
  • Tetanus Toxin / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transgenes
  • Tryptophan Hydroxylase / genetics
  • Tryptophan Hydroxylase / metabolism

Substances

  • DNA-Binding Proteins
  • Drosophila Proteins
  • GAL4 protein, S cerevisiae
  • Kir2.1 channel
  • Potassium Channels, Inwardly Rectifying
  • Saccharomyces cerevisiae Proteins
  • Tetanus Toxin
  • Transcription Factors
  • Tryptophan Hydroxylase
  • Dynamins

Grant support

This work was supported by research fellowships from the Council of Scientific and Industrial research (http://rdpp.csir.res.in/csir_acsir/Home.aspx) to Sufia Sadaf. The project was supported financially by grants from the Department of Biotechnology (http://dbtindia.nic.in/index.asp), the Department of Science and Technology (http://www.dst.gov.in/), and the National Centre for Biological Sciences, Tata Institute of Fundamental Research (http://www.ncbs.res.in) to GH. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.