TheDrosophilaCircadian Clock Gates Sleep through Time-of-Day Dependent Modulation of Sleep-Promoting Neurons

Sep 10, 2015Sleep

The Fruit Fly's Internal Clock Controls Sleep by Changing Sleep Neuron Activity at Different Times of Day

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Abstract

Activation or inhibition of specific neurons in Drosophila can control sleep, with effects varying significantly depending on the time of day.

Bidirectional control of sleep was achieved by manipulating a population of neurons that connect to the sleep-promoting dorsal Fan-Shaped Body.
The effectiveness of activating sleep-promoting neurons was highest during the middle of the day and night.
Inhibition of these neurons was particularly effective in preventing sleep onset during late evening hours.
Time-of-day specific effects of neuronal manipulation were absent in flies lacking functional circadian clocks.
The circadian system may play a role in regulating sleep timing by actively inhibiting sleep at certain times.

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STUDY OBJECTIVES: Sleep is under the control of homeostatic and circadian processes, which interact to determine sleep timing and duration, but the mechanisms through which the circadian system modulates sleep are largely unknown. We therefore used adult-specific, temporally controlled neuronal activation and inhibition to identify an interaction between the circadian clock and a novel population of sleep-promoting neurons in Drosophila.

METHODS: Transgenic flies expressed either dTRPA1, a neuronal activator, or Shibire(ts1), an inhibitor of synaptic release, in small subsets of neurons. Sleep, as determined by activity monitoring and video tracking, was assessed before and after temperature-induced activation or inhibition using these effector molecules. We compared the effect of these manipulations in control flies and in mutant flies that lacked components of the molecular circadian clock.

RESULTS: Adult-specific activation or inhibition of a population of neurons that projects to the sleep-promoting dorsal Fan-Shaped Body resulted in bidirectional control over sleep. Interestingly, the magnitude of the sleep changes were time-of-day dependent. Activation of sleep-promoting neurons was maximally effective during the middle of the day and night, and was relatively ineffective during the day-to-night and night-to-day transitions. These time-ofday specific effects were absent in flies that lacked functional circadian clocks.

CONCLUSIONS: We conclude that the circadian system functions to gate sleep through active inhibition at specific times of day. These data identify a mechanism through which the circadian system prevents premature sleep onset in the late evening, when homeostatic sleep drive is high.

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TheDrosophilaCircadian Clock Gates Sleep through Time-of-Day Dependent Modulation of Sleep-Promoting Neurons

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