Network synchrony creates neural filters promoting quiescence in Drosophila.

Journal: Nature
Published Date:

Abstract

Animals require undisturbed periods of rest during which they undergo recuperative processes. However, it is unclear how brain states arise that are able to dissociate an animal from its external world, enabling quiescent behaviours, while retaining vigilance to salient sensory cues. Here we describe a neural mechanism in Drosophila that creates neural filters that engender a brain state that enables quiescent behaviour by generating coherent slow-wave activity (SWA) between sleep-need (R5)- and locomotion-promoting neural networks. The coherence of SWA is subject to circadian and homeostatic control and can be modulated by sensory experience. Mimicry of coherent SWA reveals that R5 oscillations reduce responsiveness to visual stimuli by rhythmically associating neural activity of locomotion-promoting cells, effectively overruling their output. These networks can regulate behavioural responsiveness by providing antagonistic inputs to downstream head-direction cells. Thus, coherent oscillations provide the mechanistic basis for a neural filter by temporally associating opposing signals, resulting in reduced functional connectivity between locomotion-gating and navigational networks. We propose that the temporal pattern of SWA provides the structure to create a 'breakable' filter, permitting the animal to enter a quiescent state, while providing the architecture for strong or salient stimuli to 'break' the neural interaction, consequently allowing the animal to react.

Authors

  • Davide Raccuglia
    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany. davide.raccuglia@charite.de.
  • Raquel Suárez-Grimalt
    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.
  • Laura Krumm
    Computational Neurology, Department of Neurology and Berlin Institute of Health, Charité - Universitätsmedizin Berlin, Berlin, Germany.
  • Anatoli Ender
    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.
  • Cédric B Brodersen
    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.
  • Sridhar R Jagannathan
    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.
  • Martin Freire Krück
    Bernstein Center for Computational Neuroscience Berlin, Berlin, Germany.
  • Niccolò P Pampaloni
    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.
  • Carolin Rauch
    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.
  • York Winter
    Humboldt Universität, Berlin 10117, Germany york.winter@hu-berlin.de.
  • Genevieve Yvon-Durocher
    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.
  • Richard Kempter
    Institute for Theoretical Biology, Department of Biology, Humboldt-Universität zu Berlin, Berlin, Germany.
  • Jörg R P Geiger
    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany.
  • David Owald
    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany. david.owald@charite.de.

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