Slowpoke functions in circadian output cells to regulate rest:activity rhythms.

The circadian system produces ~24-hr oscillations in behavioral and physiological processes to ensure that they occur at optimal times of day and in the correct temporal order. At its core, the circadian system is composed of dedicated central clock neurons that keep time through a cell-autonomous m...

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Main Authors: Daniela Ruiz, Saffia T Bajwa, Naisarg Vanani, Tanvir A Bajwa, Daniel J Cavanaugh
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0249215
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author Daniela Ruiz
Saffia T Bajwa
Naisarg Vanani
Tanvir A Bajwa
Daniel J Cavanaugh
author_facet Daniela Ruiz
Saffia T Bajwa
Naisarg Vanani
Tanvir A Bajwa
Daniel J Cavanaugh
author_sort Daniela Ruiz
collection DOAJ
description The circadian system produces ~24-hr oscillations in behavioral and physiological processes to ensure that they occur at optimal times of day and in the correct temporal order. At its core, the circadian system is composed of dedicated central clock neurons that keep time through a cell-autonomous molecular clock. To produce rhythmic behaviors, time-of-day information generated by clock neurons must be transmitted across output pathways to regulate the downstream neuronal populations that control the relevant behaviors. An understanding of the manner through which the circadian system enacts behavioral rhythms therefore requires the identification of the cells and molecules that make up the output pathways. To that end, we recently characterized the Drosophila pars intercerebralis (PI) as a major circadian output center that lies downstream of central clock neurons in a circuit controlling rest:activity rhythms. We have conducted single-cell RNA sequencing (scRNAseq) to identify potential circadian output genes expressed by PI cells, and used cell-specific RNA interference (RNAi) to knock down expression of ~40 of these candidate genes selectively within subsets of PI cells. We demonstrate that knockdown of the slowpoke (slo) potassium channel in PI cells reliably decreases circadian rest:activity rhythm strength. Interestingly, slo mutants have previously been shown to have aberrant rest:activity rhythms, in part due to a necessary function of slo within central clock cells. However, rescue of slo in all clock cells does not fully reestablish behavioral rhythms, indicating that expression in non-clock neurons is also necessary. Our results demonstrate that slo exerts its effects in multiple components of the circadian circuit, including PI output cells in addition to clock neurons, and we hypothesize that it does so by contributing to the generation of daily neuronal activity rhythms that allow for the propagation of circadian information throughout output circuits.
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spelling doaj.art-b583b59cdbcf47828625eaf99c8b16d62022-12-22T03:00:22ZengPublic Library of Science (PLoS)PLoS ONE1932-62032021-01-01163e024921510.1371/journal.pone.0249215Slowpoke functions in circadian output cells to regulate rest:activity rhythms.Daniela RuizSaffia T BajwaNaisarg VananiTanvir A BajwaDaniel J CavanaughThe circadian system produces ~24-hr oscillations in behavioral and physiological processes to ensure that they occur at optimal times of day and in the correct temporal order. At its core, the circadian system is composed of dedicated central clock neurons that keep time through a cell-autonomous molecular clock. To produce rhythmic behaviors, time-of-day information generated by clock neurons must be transmitted across output pathways to regulate the downstream neuronal populations that control the relevant behaviors. An understanding of the manner through which the circadian system enacts behavioral rhythms therefore requires the identification of the cells and molecules that make up the output pathways. To that end, we recently characterized the Drosophila pars intercerebralis (PI) as a major circadian output center that lies downstream of central clock neurons in a circuit controlling rest:activity rhythms. We have conducted single-cell RNA sequencing (scRNAseq) to identify potential circadian output genes expressed by PI cells, and used cell-specific RNA interference (RNAi) to knock down expression of ~40 of these candidate genes selectively within subsets of PI cells. We demonstrate that knockdown of the slowpoke (slo) potassium channel in PI cells reliably decreases circadian rest:activity rhythm strength. Interestingly, slo mutants have previously been shown to have aberrant rest:activity rhythms, in part due to a necessary function of slo within central clock cells. However, rescue of slo in all clock cells does not fully reestablish behavioral rhythms, indicating that expression in non-clock neurons is also necessary. Our results demonstrate that slo exerts its effects in multiple components of the circadian circuit, including PI output cells in addition to clock neurons, and we hypothesize that it does so by contributing to the generation of daily neuronal activity rhythms that allow for the propagation of circadian information throughout output circuits.https://doi.org/10.1371/journal.pone.0249215
spellingShingle Daniela Ruiz
Saffia T Bajwa
Naisarg Vanani
Tanvir A Bajwa
Daniel J Cavanaugh
Slowpoke functions in circadian output cells to regulate rest:activity rhythms.
PLoS ONE
title Slowpoke functions in circadian output cells to regulate rest:activity rhythms.
title_full Slowpoke functions in circadian output cells to regulate rest:activity rhythms.
title_fullStr Slowpoke functions in circadian output cells to regulate rest:activity rhythms.
title_full_unstemmed Slowpoke functions in circadian output cells to regulate rest:activity rhythms.
title_short Slowpoke functions in circadian output cells to regulate rest:activity rhythms.
title_sort slowpoke functions in circadian output cells to regulate rest activity rhythms
url https://doi.org/10.1371/journal.pone.0249215
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AT naisargvanani slowpokefunctionsincircadianoutputcellstoregulaterestactivityrhythms
AT tanvirabajwa slowpokefunctionsincircadianoutputcellstoregulaterestactivityrhythms
AT danieljcavanaugh slowpokefunctionsincircadianoutputcellstoregulaterestactivityrhythms