Membrane electrical excitability is necessary for the free-running larval Drosophila circadian clock

J Neurobiol. 2005 Jan;62(1):1-13. doi: 10.1002/neu.20053.

Abstract

Drosophila larvae and adult pacemaker neurons both express free-running oscillations of period (PER) and timeless (TIM) proteins that constitute the core of the cell-autonomous circadian molecular clock. Despite similarities between the adult and larval molecular oscillators, adults and larvae differ substantially in the complexity and organization of their pacemaker neural circuits, as well as in behavioral manifestations of circadian rhythmicity. We have shown previously that electrical silencing of adult Drosophila circadian pacemaker neurons through targeted expression of either an open rectifier or inward rectifier K(+) channel stops the free-running oscillations of the circadian molecular clock. This indicates that neuronal electrical activity in the pacemaker neurons is essential to the normal function of the adult intracellular clock. In the current study, we show that in constant darkness the free-running larval pacemaker clock-like that of the adult pacemaker neurons they give rise to-requires membrane electrical activity to oscillate. In contrast to the free-running clock, the molecular clock of electrically silenced larval pacemaker neurons continues to oscillate in diurnal (light-dark) conditions. This specific disruption of the free-running clock caused by targeted K(+) channel expression likely reflects a specific cell-autonomous clock-membrane feedback loop that is common to both larval and adult neurons, and is not due to blocking pacemaker synaptic outputs or disruption of pacemaker neuronal morphology.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Biological Clocks / genetics*
  • Cell Membrane / genetics
  • Cell Membrane / metabolism*
  • Circadian Rhythm / genetics*
  • Darkness
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / cytology
  • Drosophila melanogaster / metabolism
  • Drosophila melanogaster / physiology*
  • Feedback / physiology
  • Gene Expression Regulation, Developmental / genetics
  • Larva / cytology
  • Larva / metabolism
  • Larva / physiology
  • Membrane Potentials / genetics
  • Nervous System / cytology
  • Nervous System / metabolism*
  • Neural Pathways / physiology
  • Neurons / metabolism*
  • Nuclear Proteins / metabolism
  • Period Circadian Proteins
  • Photic Stimulation
  • Potassium Channels / genetics
  • Potassium Channels, Inwardly Rectifying / genetics
  • Synaptic Transmission / genetics

Substances

  • Drosophila Proteins
  • Kir2.1 channel
  • Nuclear Proteins
  • Ork1 protein, Drosophila
  • PER protein, Drosophila
  • Period Circadian Proteins
  • Potassium Channels
  • Potassium Channels, Inwardly Rectifying
  • tim protein, Drosophila