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Research Articles, Systems/Circuits

Dopamine Signaling in Wake-Promoting Clock Neurons Is Not Required for the Normal Regulation of Sleep in Drosophila

Florencia Fernandez-Chiappe, Christiane Hermann-Luibl, Alina Peteranderl, Nils Reinhard, Pingkalai R. Senthilan, Marie Hieke, Mareike Selcho, Taishi Yoshii, Orie T. Shafer, Nara I. Muraro and Charlotte Helfrich-Förster
Journal of Neuroscience 9 December 2020, 40 (50) 9617-9633; DOI: https://doi.org/10.1523/JNEUROSCI.1488-20.2020
Florencia Fernandez-Chiappe
2Instituto de Investigación en Biomedicina de Buenos Aires (IBioBA), CONICET-Partner Institute of the Max Planck Society, C1425FQD Buenos Aires, Argentina
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Christiane Hermann-Luibl
1Neurobiology and Genetics, Biocenter, University of Würzburg, 97074 Würzburg, Germany
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Alina Peteranderl
1Neurobiology and Genetics, Biocenter, University of Würzburg, 97074 Würzburg, Germany
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Nils Reinhard
1Neurobiology and Genetics, Biocenter, University of Würzburg, 97074 Würzburg, Germany
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Pingkalai R. Senthilan
1Neurobiology and Genetics, Biocenter, University of Würzburg, 97074 Würzburg, Germany
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Marie Hieke
1Neurobiology and Genetics, Biocenter, University of Würzburg, 97074 Würzburg, Germany
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Mareike Selcho
1Neurobiology and Genetics, Biocenter, University of Würzburg, 97074 Würzburg, Germany
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Taishi Yoshii
3Graduate School of Natural Science and Technology, Okayama University, Okayama 700-8530, Japan
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Orie T. Shafer
4Advance Science Research Center, The City University of New York, New York 10031
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Nara I. Muraro
2Instituto de Investigación en Biomedicina de Buenos Aires (IBioBA), CONICET-Partner Institute of the Max Planck Society, C1425FQD Buenos Aires, Argentina
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Charlotte Helfrich-Förster
1Neurobiology and Genetics, Biocenter, University of Würzburg, 97074 Würzburg, Germany
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Abstract

Dopamine is a wake-promoting neuromodulator in mammals and fruit flies. In Drosophila melanogaster, the network of clock neurons that drives sleep/activity cycles comprises both wake-promoting and sleep-promoting cell types. The large ventrolateral neurons (l-LNvs) and small ventrolateral neurons (s-LNvs) have been identified as wake-promoting neurons within the clock neuron network. The l-LNvs are innervated by dopaminergic neurons, and earlier work proposed that dopamine signaling raises cAMP levels in the l-LNvs and thus induces excitatory electrical activity (action potential firing), which results in wakefulness and inhibits sleep. Here, we test this hypothesis by combining cAMP imaging and patch-clamp recordings in isolated brains. We find that dopamine application indeed increases cAMP levels and depolarizes the l-LNvs, but, surprisingly, it does not result in increased firing rates. Downregulation of the excitatory D1-like dopamine receptor (Dop1R1) in the l-LNvs and s-LNvs, but not of Dop1R2, abolished the depolarization of l-LNvs in response to dopamine. This indicates that dopamine signals via Dop1R1 to the l-LNvs. Downregulation of Dop1R1 or Dop1R2 in the l-LNvs and s-LNvs does not affect sleep in males. Unexpectedly, we find a moderate decrease of daytime sleep with downregulation of Dop1R1 and of nighttime sleep with downregulation of Dop1R2. Since the l-LNvs do not use Dop1R2 receptors and the s-LNvs also respond to dopamine, we conclude that the s-LNvs are responsible for the observed decrease in nighttime sleep. In summary, dopamine signaling in the wake-promoting LNvs is not required for daytime arousal, but likely promotes nighttime sleep via the s-LNvs.

SIGNIFICANCE STATEMENT In insect and mammalian brains, sleep-promoting networks are intimately linked to the circadian clock, and the mechanisms underlying sleep and circadian timekeeping are evolutionarily ancient and highly conserved. Here we show that dopamine, one important sleep modulator in flies and mammals, plays surprisingly complex roles in the regulation of sleep by clock-containing neurons. Dopamine inhibits neurons in a central brain sleep center to promote sleep and excites wake-promoting circadian clock neurons. It is therefore predicted to promote wakefulness through both of these networks. Nevertheless, our results reveal that dopamine acting on wake-promoting clock neurons promotes sleep, revealing a previously unappreciated complexity in the dopaminergic control of sleep.

  • cAMP
  • clock neurons
  • dopamine
  • patch-clamp recording
  • sleep
  • wakefulness

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The Journal of Neuroscience: 40 (50)
Journal of Neuroscience
Vol. 40, Issue 50
9 Dec 2020
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Dopamine Signaling in Wake-Promoting Clock Neurons Is Not Required for the Normal Regulation of Sleep in Drosophila
Florencia Fernandez-Chiappe, Christiane Hermann-Luibl, Alina Peteranderl, Nils Reinhard, Pingkalai R. Senthilan, Marie Hieke, Mareike Selcho, Taishi Yoshii, Orie T. Shafer, Nara I. Muraro, Charlotte Helfrich-Förster
Journal of Neuroscience 9 December 2020, 40 (50) 9617-9633; DOI: 10.1523/JNEUROSCI.1488-20.2020

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Dopamine Signaling in Wake-Promoting Clock Neurons Is Not Required for the Normal Regulation of Sleep in Drosophila
Florencia Fernandez-Chiappe, Christiane Hermann-Luibl, Alina Peteranderl, Nils Reinhard, Pingkalai R. Senthilan, Marie Hieke, Mareike Selcho, Taishi Yoshii, Orie T. Shafer, Nara I. Muraro, Charlotte Helfrich-Förster
Journal of Neuroscience 9 December 2020, 40 (50) 9617-9633; DOI: 10.1523/JNEUROSCI.1488-20.2020
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Keywords

  • cAMP
  • clock neurons
  • dopamine
  • patch-clamp recording
  • sleep
  • wakefulness

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