Measurements of behavioral quiescence in Caenorhabditis elegans

Nagy, Stanislav; Raizen, David M.; Biron, David

doi:10.1016/j.ymeth.2014.03.009

Cited by 49 publications

(76 citation statements)

References 40 publications

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“…Recently, a biomechanical model was proposed in which a relaxed body posture with fewer body bends facilitates flipping of worms confined to a plane. Consistent with this result, ectopic flipping could be observed in a V-ATPase mutant that showed a relaxed body posture outside of lethargus (Iwanir et al, 2013; Nagy et al, 2014b; Schwarz et al, 2011, 2012; Tramm et al, 2014). We hence set out to directly test the idea that altered activity levels influence the probability that SIA activation leads to flipping.…”

Section: Resultssupporting

confidence: 76%

“…The occurrence of flips during periods of low mobility may seem counterintuitive at first, as flipping constitutes a motion and a flip could thus be, by definition, regarded as a motion bout. However, x-y movements of the nose and body typically define a motion bout (Iwanir et al, 2013; Nagy et al, 2014b). Flipping consists only of a rotation along the longitudinal axis.…”

Section: Discussionmentioning

confidence: 99%

“…Before shedding the old cuticle, larvae go through a developmental stage and behavioral state called lethargus during which they don’t feed. Locomotion behavior during lethargus can be described as quiescence bouts that are intermitted by motion bouts (Iwanir et al, 2013; Nagy et al, 2014a, 2014b). Developmentally controlled quiescence behavior fulfills the behavioral criteria that define sleep in other organisms, such as decreased voluntary movement, an increased arousal threshold, reversibility, and homeostatic regulation, and is thus called sleep (Iwanir et al, 2013; Nagy et al, 2014a; Raizen et al, 2008; Trojanowski et al, 2015; Trojanowski and Raizen, 2016; Driver et al, 2013; Schwarz et al, 2011, 2012; Turek et al, 2016; Cassada and Russell, 1975).…”

Section: Introductionmentioning

confidence: 99%

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Analysis of the NK2 homeobox gene ceh-24 reveals sublateral motor neuron control of left-right turning during sleep

Schwarz

Bringmann

2017

eLife

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Sleep is a behavior that is found in all animals that have a nervous system and that have been studied carefully. In Caenorhabditis elegans larvae, sleep is associated with a turning behavior, called flipping, in which animals rotate 180° about their longitudinal axis. However, the molecular and neural substrates of this enigmatic behavior are not known. Here, we identified the conserved NK-2 homeobox gene ceh-24 to be crucially required for flipping. ceh-24 is required for the formation of processes and for cholinergic function of sublateral motor neurons, which separately innervate the four body muscle quadrants. Knockdown of cholinergic function in a subset of these sublateral neurons, the SIAs, abolishes flipping. The SIAs depolarize during flipping and their optogenetic activation induces flipping in a fraction of events. Thus, we identified the sublateral SIA neurons to control the three-dimensional movements of flipping. These neurons may also control other types of motion.DOI: http://dx.doi.org/10.7554/eLife.24846.001

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Section: Resultssupporting

confidence: 76%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Analysis of the NK2 homeobox gene ceh-24 reveals sublateral motor neuron control of left-right turning during sleep

Schwarz

Bringmann

2017

eLife

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“…We used specialized microfluidic chambers designed to keep animals confined to an area within a camera field of view for recording the entirety of the lethargus period while still allowing animals to move freely within the chamber (Singh et al 2011). Surprisingly, when we observed locomotory quiescence during lethargus of wild-type animals ( Figure 4A) and vav-1 mutants ( Figure 4B), we found no difference in the total quiescence ( Figure 4D) or the duration of quiescence ( Figure 4E), unlike lethargus quiescence defective egl-30 mutants (Figure 4, C-E) (Schwarz and Bringmann 2013;Nagy et al 2014). Because ALA has been reported to play a minor role in lethargus quiescence (Van Buskirk and Sternberg 2007;Trojanowski et al 2015), we tested a mutant, plc-3, that has been shown previously to have a role in ALA to regulate quiescence during lethargus to determine whether our assay is sensitive enough to detect a minor lethargus quiescence defect.…”

Section: Vav-1 Function Is Dispensable For Sleep-like Behavior Duringmentioning

confidence: 75%

A Conserved GEF for Rho-Family GTPases Acts in an EGF Signaling Pathway to Promote Sleep-like Quiescence inCaenorhabditis elegans

et al. 2016

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Sleep is evolutionarily conserved and required for organism homeostasis and survival. Despite this importance, the molecular and cellular mechanisms underlying sleep are not well understood. Caenorhabditis elegans exhibits sleep-like behavioral quiescence and thus provides a valuable, simple model system for the study of cellular and molecular regulators of this process. In C. elegans, epidermal growth factor receptor (EGFR) signaling is required in the neurosecretory neuron ALA to promote sleep-like behavioral quiescence after cellular stress. We describe a novel role for VAV-1, a conserved guanine nucleotide exchange factor (GEF) for Rho-family GTPases, in regulation of sleep-like behavioral quiescence. VAV-1, in a GEF-dependent manner, acts in ALA to suppress locomotion and feeding during sleep-like behavioral quiescence in response to cellular stress. Additionally, VAV-1 activity is required for EGF-induced sleep-like quiescence and normal levels of EGFR and secretory dense core vesicles in ALA. Importantly, the role of VAV-1 in promoting cellular stress-induced behavioral quiescence is vital for organism health because VAV-1 is required for normal survival after cellular stress.KEYWORDS behavioral quiescence; Caenorhabditis elegans; sleep; Vav D ESPITE being a subject of formal study for over 150 years, sleep is not clearly understood. Moreover, various explanations for the functional role of sleep have been proposed, such as allowing "recharging" of cells following high metabolic activity (Benington and Heller 1995;Tu and McKnight 2006;Scharf et al. 2008) and remodeling of synapses built during wakefulness (Tononi and Cirelli 2006). Yet sleep problems have a significant impact on human health and are a leading reason for seeking medical attention (Mahowald and Schenck 2005). Therefore, there is a great need for understanding the cellular and molecular mechanisms that regulate sleep-wake cycles.Simple model organisms such as Caenorhabditis elegans have the potential to provide valuable information regarding sleep regulation. C. elegans is known for its easily manipulated genetics, small nervous system with mapped neuronal connectivity, stereotypical behaviors, and the ability to be studied efficiently in large numbers. Numerous studies have shown that C. elegans lethargus, a restful period that occurs before each molt of the cuticle during larval development, is neuronally regulated and likely orthologous to sleep in mammals (Van Buskirk and Sternberg 2007;Raizen et al. 2008;Van Buskirk and Sternberg 2010;Choi et al. 2013;Iwanir et al. 2013;Turek et al. 2013;Cho and Sternberg 2014;Singh et al. 2014). Lethargus quiescence in C. elegans shares several characteristics with mammalian sleep: inactivity (decreased locomotion and cessation of pharyngeal pumping, or feeding), a specific posture, reduced response to aversive stimuli, and rapid reversibility (Cassada and Russell 1975;Raizen et al. 2008;Schwarz et al. 2012;Iwanir et al. 2013;Cho and Sternberg 2014). In addition, lethargus quiescence is under ...

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“…This concerns mice [12]- [14], Caenorhabditis elegans [15]- [17], as well as Drosophila flies [18]- [22]. However, to the best of our knowledge there is no system available for monitoring the behaviour of Drosophila at the larval states in culture vials for a long time period.…”

Section: Introductionmentioning

confidence: 99%

An FIM-Based Long-Term In-Vial Monitoring System for Drosophila Larvae

Berh

Risse

Michels

et al. 2017

IEEE Trans. Biomed. Eng.

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Abstract-Drosophila larvae are an insightful model and the automated analysis of their behaviour is an integral readout in behavioural biology. Current tracking systems, however, entail a disturbance of the animals, are labour-intensive, and cannot be easily used for long-term monitoring purposes. Here we present a novel monitoring system for Drosophila larvae which allows us to analyse the animals in cylindrical culture vials. By utilizing frustrated total internal reflection in combination with a multicamera/microcomputer setup we image the complete housing vial surface and thus the larvae for days. We introduce a calibration scheme to stitch the images from the multi-camera system and unfold arbitrary cylindrical surfaces to support different vials. As a result, imaging and analysis of a whole population can be done implicitly. For the first time, this allows to extract long-term activity quantities of larvae without disturbing the animals. We demonstrate the capabilities of this new setup by automatically quantifying the activity of multiple larvae moving in a vial. The accuracy of the system and the spatio-temporal resolution is sufficient to obtain motion trajectories and higher level features like body bending. This new setup can be used for in-vial activity monitoring and behavioural analysis and is capable of gathering millions of data points without both disturbing the animals and additional labour time. In total we have analysed 107, 671 frames resulting in 8, 650 trajectories, which are longer than 30 seconds, and obtained more than 4.2 ⇥ 10 6 measurements.

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Measurements of behavioral quiescence in Caenorhabditis elegans

Cited by 49 publications

References 40 publications

Analysis of the NK2 homeobox gene ceh-24 reveals sublateral motor neuron control of left-right turning during sleep

Analysis of the NK2 homeobox gene ceh-24 reveals sublateral motor neuron control of left-right turning during sleep

A Conserved GEF for Rho-Family GTPases Acts in an EGF Signaling Pathway to Promote Sleep-like Quiescence inCaenorhabditis elegans

An FIM-Based Long-Term In-Vial Monitoring System for Drosophila Larvae

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