scholarly journals A quiescent state following mild sensory arousal in Caenorhabditis elegans is potentiated by stress

2019 ◽  
Author(s):  
Patrick D. McClanahan ◽  
Jessica M. Dubuque ◽  
Daphne Kontogiorgos-Heintz ◽  
Ben F. Habermeyer ◽  
Joyce H. Xu ◽  
...  

AbstractAn animal’s behavioral and physiological response to stressors includes changes to its responses to stimuli. How such changes occur is not well understood. Here we describe a Caenorhabditis elegans quiescent behavior, post-response quiescence (PRQ), which is modulated by the C. elegans response to cellular stressors. Following an aversive mechanical or blue light stimulus, worms respond first by briefly moving, and then become more quiescent for a period lasting tens of seconds. PRQ occurs at low frequency in unstressed animals, but is more frequent in animals that have experienced cellular stress due to ultraviolet light exposure as well as in animals following overexpression of epidermal growth factor (EGF). PRQ requires the function of the carboxypeptidase EGL-21 and the calcium-activated protein for secretion (CAPS) UNC-31, suggesting it has a neuropeptidergic mechanism. Although PRQ requires the sleep-promoting neurons RIS and ALA, it is not accompanied by decreased arousability, and does not appear to be homeostatically regulated, suggesting that it is not a sleep state. PRQ represents a simple, tractable model for studying how neuromodulatory states like stress alter behavioral responses to stimuli.

BMC Biology ◽  
2021 ◽  
Vol 19 (1) ◽  
Author(s):  
M. Koopman ◽  
L. Janssen ◽  
E. A. A. Nollen

Abstract Background Optogenetics allows the experimental manipulation of excitable cells by a light stimulus without the need for technically challenging and invasive procedures. The high degree of spatial, temporal, and intensity control that can be achieved with a light stimulus, combined with cell type-specific expression of light-sensitive ion channels, enables highly specific and precise stimulation of excitable cells. Optogenetic tools have therefore revolutionized the study of neuronal circuits in a number of models, including Caenorhabditis elegans. Despite the existence of several optogenetic systems that allow spatial and temporal photoactivation of light-sensitive actuators in C. elegans, their high costs and low flexibility have limited wide access to optogenetics. Here, we developed an inexpensive, easy-to-build, modular, and adjustable optogenetics device for use on different microscopes and worm trackers, which we called the OptoArm. Results The OptoArm allows for single- and multiple-worm illumination and is adaptable in terms of light intensity, lighting profiles, and light color. We demonstrate OptoArm’s power in a population-based multi-parameter study on the contributions of motor circuit cells to age-related motility decline. We found that individual components of the neuromuscular system display different rates of age-dependent deterioration. The functional decline of cholinergic neurons mirrors motor decline, while GABAergic neurons and muscle cells are relatively age-resilient, suggesting that rate-limiting cells exist and determine neuronal circuit ageing. Conclusion We have assembled an economical, reliable, and highly adaptable optogenetics system which can be deployed to address diverse biological questions. We provide a detailed description of the construction as well as technical and biological validation of our set-up. Importantly, use of the OptoArm is not limited to C. elegans and may benefit studies in multiple model organisms, making optogenetics more accessible to the broader research community.


2019 ◽  
Vol 10 (1) ◽  
Author(s):  
Daniel L. Gonzales ◽  
Jasmine Zhou ◽  
Bo Fan ◽  
Jacob T. Robinson

Abstract An important feature of animal behavior is the ability to switch rapidly between activity states, however, how the brain regulates these spontaneous transitions based on the animal’s perceived environment is not well understood. Here we show a C. elegans sleep-like state on a scalable platform that enables simultaneous control of multiple environmental factors including temperature, mechanical stress, and food availability. This brief quiescent state, which we refer to as microfluidic-induced sleep, occurs spontaneously in microfluidic chambers, which allows us to track animal movement and perform whole-brain imaging. With these capabilities, we establish that microfluidic-induced sleep meets the behavioral requirements of C. elegans sleep and depends on multiple factors, such as satiety and temperature. Additionally, we show that C. elegans sleep can be induced through mechanosensory pathways. Together, these results establish a model system for studying how animals process multiple sensory pathways to regulate behavioral states.


2018 ◽  
Author(s):  
E. A. Mazzochette ◽  
A. L. Nekimken ◽  
F. Loizeau ◽  
J. Whitworth ◽  
B. Huynh ◽  
...  

AbstractSensory neurons embedded in skin are responsible for the sense of touch. In humans and other mammals, touch sensation depends on thousands of diverse somatosensory neurons. By contrast, Caenorhabditis elegans nematodes have six gentle touch receptor neurons linked to simple behaviors. The classical touch assay uses an eyebrow hair to stimulate freely moving C. elegans, evoking evasive behavioral responses. While this assay has led to the discovery of genes required for touch sensation, it does not provide control over stimulus strength or position. Here, we present an integrated system for performing automated, quantitative touch assays that circumvents these limitations and incorporates automated measurements of behavioral responses. Highly Automated Worm Kicker (HAWK) unites microfabricated silicon force sensors and video analysis with real-time force and position control. Using this system, we stimulated animals along the anterior-posterior axis and compared responses in wild-type and spc-1(dn) transgenic animals, which have a touch defect due to expression of a dominant-negative α spectrin protein fragment. As expected from prior studies, delivering large stimuli anterior to the mid-point of the body evoked a reversal, but such a stimulus applied posterior to the mid-point evoked a speed-up. The probability of evoking a response of either kind depended on stimulus strength and location; once initiated, the magnitude and quality of both reversal and speed-up behavioral responses were uncorrelated with stimulus location, strength, or the absence or presence of the spc-1(dn) transgene. Wild-type animals failed to respond when the stimulus was applied near the mid-point. These results establish that stimulus strength and location govern the activation of a stereotyped motor program and that the C. elegans body surface consists of two receptive fields separated by a gap.


Genetics ◽  
2002 ◽  
Vol 160 (3) ◽  
pp. 983-994
Author(s):  
J R Chasnov ◽  
King L Chow

Abstract The free-living nematode worm Caenorhabditis elegans reproduces primarily as a self-fertilizing hermaphrodite, yet males are maintained in wild-type populations at low frequency. To determine the role of males in C. elegans, we develop a mathematical model for the genetic system of hermaphrodites that can either self-fertilize or be fertilized by males and we perform laboratory observations and experiments on both C. elegans and a related dioecious species C. remanei. We show that the mating efficiency of C. elegans is poor compared to a dioecious species and that C. elegans males are more attracted to C. remanei females than they are to their conspecific hermaphrodites. We postulate that a genetic mutation occurred during the evolution of C. elegans hermaphrodites, resulting in the loss of an attracting sex pheromone present in the ancestor of both C. elegans and C. remanei. Our findings suggest that males are maintained in C. elegans because of the particular genetic system inherited from its dioecious ancestor and because of nonadaptive spontaneous nondisjunction of sex chromosomes, which occurs during meiosis in the hermaphrodite. A theoretical argument shows that the low frequency of male mating observed in C. elegans can support male-specific genes against mutational degeneration. This results in the continuing presence of functional males in a 99.9% hermaphroditic species in which outcrossing is disadvantageous to hermaphrodites.


Genetics ◽  
1999 ◽  
Vol 153 (3) ◽  
pp. 1257-1269
Author(s):  
Jing Liu ◽  
Phoebe Tzou ◽  
Russell J Hill ◽  
Paul W Sternberg

Abstract Caenorhabditis elegans lin-3 encodes a homolog of the epidermal growth factor (EGF) family of growth factors. LIN-3 is the inductive signal for hermaphrodite vulval differentiation, and it is required for animal viability, hermaphrodite fertility, and the specification of anterior cell fates in the male B cell lineage. We describe the cloning of a lin-3 homolog from C. briggsae, sequence comparison of C. elegans lin-3 with C. briggsae lin-3, and the determination of molecular lesions in alleles of C. elegans lin-3, including three new alleles. We also analyzed the severity of phenotypes caused by the new and existing alleles of lin-3. Correlation of mutant phenotypes and their molecular lesions, as well as sequence comparison between two species, reveal that the EGF motif and the N-terminal portion of the cytoplasmic domain are important for the functions of LIN-3 in all tissues, while the C-terminal portion of the cytoplasmic domain is involved in the tissue-specific functions of lin-3. We discuss how the structure of lin-3 contributes to its functions in multiple developmental processes.


2020 ◽  
Author(s):  
M. Dal Bello ◽  
A. Pérez-Escudero ◽  
F. C. Schroeder ◽  
J. Gore

SummaryForaging animals have to locate food sources that are usually patchily distributed and subject to competition. Deciding when to leave a food patch is challenging and requires the animal to integrate information about food availability with cues signaling the presence of other individuals (e.g. pheromones). To study how social information transmitted via pheromones can aid foraging decisions, we investigated the behavioral responses of the model nematode Caenorhabditis elegans to food depletion and pheromone accumulation in food patches. We experimentally show that animals consuming a food patch leave it at different times and that the leaving time affects the animal preference for its pheromones. In particular, worms leaving early are attracted to their pheromones, while worms leaving later are repelled by them. We further demonstrate that the inversion from attraction to repulsion depends on associative learning and, by implementing a simple model, we highlight that it is an adaptive solution to optimize food intake during foraging.


Genetics ◽  
2021 ◽  
Author(s):  
Emily A Bayer ◽  
Katarina M Liberatore ◽  
Jordan R Schneider ◽  
Evan Schlesinger ◽  
Zhengying He ◽  
...  

Abstract The progression of animal development from embryonic to juvenile life depends on the coordination of organism-wide responses with environmental conditions. We found that two transcription factors that function in interneuron differentiation in Caenorhabditis elegans, fax-1 and unc-42, are required for arousal and progression from embryogenesis to larval life by potentiating insulin signaling. The combination of mutations in either transcription factor and a mutation in daf-2 insulin receptor results in a novel peri-hatching arrest phenotype; embryos are fully-developed but inactive, often remaining trapped within the eggshell, and fail to initiate pharyngeal pumping. This pathway is opposed by an osmotic sensory response pathway that promotes developmental arrest and a sleep state at the end of embryogenesis in response to elevated salt concentration. The quiescent state induced by loss of insulin signaling or by osmotic stress can be reversed by mutations in genes that are required for sleep. Therefore, countervailing signals regulate late embryonic arousal and developmental progression to larval life, mechanistically linking the two responses. Our findings demonstrate a role for insulin signaling in an arousal circuit, consistent with evidence that insulin-related regulation may function in control of sleep states in many animals. The opposing quiescent arrest state may serve as an adaptive response to the osmotic threat from high salinity environments.


2018 ◽  
Author(s):  
Melanie Desrochers ◽  
Marianne Lang ◽  
Michael Hendricks

Abstract 150 wordsAnimal navigation strategies depend on the nature of the environmental cues used. In the nematode Caenorhabditis elegans, navigation has been studied in the context of gradients of attractive or repellent stimuli as well is in response to acute aversive stimuli. We wanted to better understand how sensory responses to the same stimulus vary between graded and acute stimuli, and how this variation relates to behavioral responses. C. elegans has two salt-sensing neurons, ASEL and ASER, that show opposite responses to stepped changes in stimulus levels, however only ASER has been shown to play a prominent role in salt chemotaxis. We used pre-exposure to natural stimuli to manipulate the responsiveness of these neurons and tested their separate contributions to behavior. Our results suggest ASEL is specialized for responses to acute stimulus changes. We also found that ASER remains responsive to graded stimuli under conditions where it is unresponsive to large steps.


2002 ◽  
Vol 69 ◽  
pp. 117-134 ◽  
Author(s):  
Stuart M. Haslam ◽  
David Gems ◽  
Howard R. Morris ◽  
Anne Dell

There is no doubt that the immense amount of information that is being generated by the initial sequencing and secondary interrogation of various genomes will change the face of glycobiological research. However, a major area of concern is that detailed structural knowledge of the ultimate products of genes that are identified as being involved in glycoconjugate biosynthesis is still limited. This is illustrated clearly by the nematode worm Caenorhabditis elegans, which was the first multicellular organism to have its entire genome sequenced. To date, only limited structural data on the glycosylated molecules of this organism have been reported. Our laboratory is addressing this problem by performing detailed MS structural characterization of the N-linked glycans of C. elegans; high-mannose structures dominate, with only minor amounts of complex-type structures. Novel, highly fucosylated truncated structures are also present which are difucosylated on the proximal N-acetylglucosamine of the chitobiose core as well as containing unusual Fucα1–2Gal1–2Man as peripheral structures. The implications of these results in terms of the identification of ligands for genomically predicted lectins and potential glycosyltransferases are discussed in this chapter. Current knowledge on the glycomes of other model organisms such as Dictyostelium discoideum, Saccharomyces cerevisiae and Drosophila melanogaster is also discussed briefly.


2021 ◽  
Vol 13 ◽  
Author(s):  
Abdullah Almotayri ◽  
Jency Thomas ◽  
Mihiri Munasinghe ◽  
Markandeya Jois

Background: The antidepressant mianserin has been shown to extend the lifespan of Caenorhabditis elegans (C. elegans), a well-established model organism used in aging research. The extension of lifespan in C. elegans was shown to be dependent on increased expression of the scaffolding protein (ANK3/unc-44). In contrast, antidepressant use in humans is associated with an increased risk of death. The C. elegans in the laboratory are fed Escherichia coli (E. coli), a diet high in protein and low in carbohydrate, whereas a typical human diet is high in carbohydrates. We hypothesized that dietary carbohydrates might mitigate the lifespan-extension effect of mianserin. Objective: To investigate the effect of glucose added to the diet of C. elegans on the lifespan-extension effect of mianserin. Methods: Wild-type Bristol N2 and ANK3/unc-44 inactivating mutants were cultured on agar plates containing nematode growth medium and fed E. coli. Treatment groups included (C) control, (M50) 50 μM mianserin, (G) 73 mM glucose, and (M50G) 50 μM mianserin and 73 mM glucose. Lifespan was determined by monitoring the worms until they died. Statistical analysis was performed using the Kaplan-Meier version of the log-rank test. Results: Mianserin treatment resulted in a 12% increase in lifespan (P<0.05) of wild-type Bristol N2 worms but reduced lifespan by 6% in ANK3/unc-44 mutants, consistent with previous research. The addition of glucose to the diet reduced the lifespan of both strains of worms and abolished the lifespan-extension by mianserin. Conclusion: The addition of glucose to the diet of C. elegans abolishes the lifespan-extension effects of mianserin.


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