Clock-Generated Temporal Codes Determine Synaptic Plasticity to Control Sleep

Cell. 2018 Nov 15;175(5):1213-1227.e18. doi: 10.1016/j.cell.2018.09.016. Epub 2018 Oct 11.

Abstract

Neurons use two main schemes to encode information: rate coding (frequency of firing) and temporal coding (timing or pattern of firing). While the importance of rate coding is well established, it remains controversial whether temporal codes alone are sufficient for controlling behavior. Moreover, the molecular mechanisms underlying the generation of specific temporal codes are enigmatic. Here, we show in Drosophila clock neurons that distinct temporal spike patterns, dissociated from changes in firing rate, encode time-dependent arousal and regulate sleep. From a large-scale genetic screen, we identify the molecular pathways mediating the circadian-dependent changes in ionic flux and spike morphology that rhythmically modulate spike timing. Remarkably, the daytime spiking pattern alone is sufficient to drive plasticity in downstream arousal neurons, leading to increased firing of these cells. These findings demonstrate a causal role for temporal coding in behavior and define a form of synaptic plasticity triggered solely by temporal spike patterns.

Keywords: Drosophila; circadian clock; sleep; synaptic plasticity; temporal coding.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials
  • Animals
  • Circadian Clocks / physiology
  • Drosophila
  • Drosophila Proteins / antagonists & inhibitors
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Models, Neurological
  • Neuronal Plasticity*
  • Neurons / metabolism
  • Optogenetics
  • Potassium Channels / genetics
  • Potassium Channels / metabolism
  • Potassium Channels, Calcium-Activated / metabolism
  • RNA Interference
  • RNA, Small Interfering / metabolism
  • Receptors, N-Methyl-D-Aspartate / metabolism
  • Signal Transduction
  • Sleep / physiology*
  • Sodium-Potassium-Exchanging ATPase / antagonists & inhibitors
  • Sodium-Potassium-Exchanging ATPase / genetics
  • Sodium-Potassium-Exchanging ATPase / metabolism
  • Synaptic Transmission

Substances

  • Drosophila Proteins
  • Potassium Channels
  • Potassium Channels, Calcium-Activated
  • RNA, Small Interfering
  • Receptors, N-Methyl-D-Aspartate
  • Slob protein, Drosophila
  • Sodium-Potassium-Exchanging ATPase