Literature DB >> 34635540

Mechanosensory Stimulation via Nanchung Expressing Neurons Can Induce Daytime Sleep in Drosophila.

Shahnaz Rahman Lone1,2, Sheetal Potdar3, Archana Venkataraman4, Nisha Sharma2, Rutvij Kulkarni3, Sushma Rao3, Sukriti Mishra2, Vasu Sheeba5, Vijay Kumar Sharma4.   

Abstract

The neuronal and genetic bases of sleep, a phenomenon considered crucial for well-being of organisms, has been under investigation using the model organism Drosophila melanogaster Although sleep is a state where sensory threshold for arousal is greater, it is known that certain kinds of repetitive sensory stimuli, such as rocking, can indeed promote sleep in humans. Here we report that orbital motion-aided mechanosensory stimulation promotes sleep of male and female Drosophila, independent of the circadian clock, but controlled by the homeostatic system. Mechanosensory receptor nanchung (Nan)-expressing neurons in the chordotonal organs mediate this sleep induction: flies in which these neurons are either silenced or ablated display significantly reduced sleep induction on mechanosensory stimulation. Transient activation of the Nan-expressing neurons also enhances sleep levels, confirming the role of these neurons in sleep induction. We also reveal that certain regions of the antennal mechanosensory and motor center in the brain are involved in conveying information from the mechanosensory structures to the sleep centers. Thus, we show, for the first time, that a circadian clock-independent pathway originating from peripherally distributed mechanosensors can promote daytime sleep of flies Drosophila melanogaster SIGNIFICANCE STATEMENT Our tendency to fall asleep in moving vehicles or the practice of rocking infants to sleep suggests that slow rhythmic movement can induce sleep, although we do not understand the mechanistic basis of this phenomenon. We find that gentle orbital motion can induce behavioral quiescence even in flies, a highly genetically tractable system for sleep studies. We demonstrate that this is indeed true sleep based on its rapid reversibility by sensory stimulation, enhanced arousal threshold, and homeostatic control. Furthermore, we demonstrate that mechanosensory neurons expressing a TRPV channel nanchung, located in the antennae and chordotonal organs, mediate orbital motion-induced sleep by communicating with antennal mechanosensory motor centers, which in turn may project to sleep centers in the brain.
Copyright © 2021 the authors.

Entities:  

Keywords:  chordotonal organs; mechanosensation; nanchung; orbital motion; sleep; sleep rebound

Mesh:

Substances:

Year:  2021        PMID: 34635540      PMCID: PMC8580144          DOI: 10.1523/JNEUROSCI.0400-21.2021

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  67 in total

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2.  Triggering sleep slow waves by transcranial magnetic stimulation.

Authors:  Marcello Massimini; Fabio Ferrarelli; Steve K Esser; Brady A Riedner; Reto Huber; Michael Murphy; Michael J Peterson; Giulio Tononi
Journal:  Proc Natl Acad Sci U S A       Date:  2007-05-04       Impact factor: 11.205

3.  EEG and behavioral manifestations of sleep induced by cutaneous nerve stimulation in normal cats.

Authors:  O POMPEIANO; J E SWETT
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4.  Circadian clock neurons constantly monitor environmental temperature to set sleep timing.

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Journal:  Nature       Date:  2018-02-21       Impact factor: 49.962

Review 5.  Mechanosensation and Adaptive Motor Control in Insects.

Authors:  John C Tuthill; Rachel I Wilson
Journal:  Curr Biol       Date:  2016-10-24       Impact factor: 10.834

6.  Motion generation by Drosophila mechanosensory neurons.

Authors:  M C Göpfert; D Robert
Journal:  Proc Natl Acad Sci U S A       Date:  2003-03-17       Impact factor: 11.205

7.  Short neuropeptide F is a sleep-promoting inhibitory modulator.

Authors:  Yuhua Shang; Nathan C Donelson; Christopher G Vecsey; Fang Guo; Michael Rosbash; Leslie C Griffith
Journal:  Neuron       Date:  2013-10-02       Impact factor: 17.173

Review 8.  Unearthing the phylogenetic roots of sleep.

Authors:  Ravi Allada; Jerome M Siegel
Journal:  Curr Biol       Date:  2008-08-05       Impact factor: 10.834

9.  PDF cells are a GABA-responsive wake-promoting component of the Drosophila sleep circuit.

Authors:  Katherine M Parisky; Jose Agosto; Stefan R Pulver; Yuhua Shang; Elena Kuklin; James J L Hodge; Kyeongjin Kang; Keongjin Kang; Xu Liu; Paul A Garrity; Michael Rosbash; Leslie C Griffith
Journal:  Neuron       Date:  2008-11-26       Impact factor: 17.173

10.  Enhancement of sleep slow waves: underlying mechanisms and practical consequences.

Authors:  Michele Bellesi; Brady A Riedner; Gary N Garcia-Molina; Chiara Cirelli; Giulio Tononi
Journal:  Front Syst Neurosci       Date:  2014-10-28
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  1 in total

1.  Inputs to the sleep homeostat originate outside the brain.

Authors:  Lawrence K Satterfield; Joydeep De; Meilin Wu; Tianhao Qiu; William J Joiner
Journal:  J Neurosci       Date:  2022-06-09       Impact factor: 6.709

  1 in total

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