Investigation of mechanosensation in C elegans using light field calcium imaging

Shaw, Michael J.; Elmi, Muna; Pawar, Vijay; Srinivasan, Mandayam A.

doi:10.1364/boe.7.002877

Cited by 6 publications

(5 citation statements)

References 30 publications

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“…Although our experiments were done under steady state conditions, it is to be expected that the organism exhibits viscoelasticity 17 under non-static conditions. The micromanipulation system used here, offers the possibility of measuring the time dependence of spatial deformation and force-displacement responses 28 . By again matching empirical data to model predictions, it would be possible to determine viscoelastic parameter values to the layers in our model and investigate temporal aspects of MeT channel activation.…”

Section: Discussionmentioning

confidence: 99%

Determining the biomechanics of touch sensation in C. elegans

Elmi

Pawar

Shaw

et al. 2017

Sci Rep

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The sense of touch is a fundamental mechanism that nearly all organisms use to interact with their surroundings. However, the process of mechanotransduction whereby a mechanical stimulus gives rise to a neuronal response is not well understood. In this paper we present an investigation of the biomechanics of touch using the model organism C. elegans. By developing a custom micromanipulation and force sensing system around a high resolution optical microscope, we measured the spatial deformation of the organism’s cuticle and force response to controlled uniaxial indentations. We combined these experimental results with anatomical data to create a multilayer computational biomechanical model of the organism and accurately derive its material properties such as the elastic modulus and poisson’s ratio. We demonstrate the utility of this model by combining it with previously published electrophysiological data to provide quantitative insights into different biomechanical states for mechanotransduction, including the first estimate of the sensitivity of an individual mechanoreceptor to an applied stimulus (parameterised as strain energy density). We also interpret empirical behavioural data to estimate the minimum number of mechanoreceptors which must be activated to elicit a behavioural response.

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Section: Discussionmentioning

confidence: 99%

Determining the biomechanics of touch sensation in C. elegans

Elmi

Pawar

Shaw

et al. 2017

Sci Rep

Self Cite

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“…Force-sensing devices provide this information and can be operated under feedback control to deliver a user-specified force or indentation. By contrast with open-loop systems, these closed-loop systems automatically regulate the applied force or indentation and two have been reported for use with C. elegans nematodes: one is based on custom-fabricated microforce-sensing probes (Park et al 2007; Petzold et al 2011, 2013; Eastwood et al 2015) (Table 2) or other commercially available microforce sensing probes (Shaw et al 2016; Elmi et al 2017). Intracellular calcium responses generated in response to mechanical stimuli delivered by open-loop mechanical stimulators pushed into the ventral or dorsal side (TRNs, OLQ, CEP, FLP, PVD), down on the lateral aspect (ADL, ADE, PHB, ALA), or the tip of the nose (ASH) of animals immobilized by superglue are illustrated in Figure 2, A, B, and E, respectively.…”

Section: Laboratory Methods For Delivering Physical Stimuli To C Elementioning

confidence: 99%

How Caenorhabditis elegans Senses Mechanical Stress, Temperature, and Other Physical Stimuli

2019

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Caenorhabditis elegans lives in a complex habitat in which they routinely experience large fluctuations in temperature, and encounter physical obstacles that vary in size and composition. Their habitat is shared by other nematodes, by beneficial and harmful bacteria, and nematode-trapping fungi. Not surprisingly, these nematodes can detect and discriminate among diverse environmental cues, and exhibit sensory-evoked behaviors that are readily quantifiable in the laboratory at high resolution. Their ability to perform these behaviors depends on <100 sensory neurons, and this compact sensory nervous system together with powerful molecular genetic tools has allowed individual neuron types to be linked to specific sensory responses. Here, we describe the sensory neurons and molecules that enable C. elegans to sense and respond to physical stimuli. We focus primarily on the pathways that allow sensation of mechanical and thermal stimuli, and briefly consider this animal’s ability to sense magnetic and electrical fields, light, and relative humidity. As the study of sensory transduction is critically dependent upon the techniques for stimulus delivery, we also include a section on appropriate laboratory methods for such studies. This chapter summarizes current knowledge about the sensitivity and response dynamics of individual classes of C. elegans mechano- and thermosensory neurons from in vivo calcium imaging and whole-cell patch-clamp electrophysiology studies. We also describe the roles of conserved molecules and signaling pathways in mediating the remarkably sensitive responses of these nematodes to mechanical and thermal cues. These studies have shown that the protein partners that form mechanotransduction channels are drawn from multiple superfamilies of ion channel proteins, and that signal transduction pathways responsible for temperature sensing in C. elegans share many features with those responsible for phototransduction in vertebrates.

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“…17 Loss of MEC-4, the key pore-forming subunit of the mechanoelectrical transduction channel responsible for detection of gentle touch in C. elegans , eliminates mechanoreceptor currents in TRNs 12 and causes in-sensitivity to touch stimuli. 18 In addition to electrical recordings, TRN physiology has been investigated using genetically encoded calcium indicators in vitro 19 and in vivo , 11,20–22 mainly by gluing live animals to agar pads using cyanoacrylate glue. 11,12,20,22 Although this strategy is compatible with mechanical stimulation via calibrated glass needles or other probes, 12,13 animals cannot be recovered for subsequent long-term studies.…”

Section: Introductionmentioning

confidence: 99%

Pneumatic stimulation of C. elegans mechanoreceptor neurons in a microfluidic trap

et al. 2017

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New tools for applying force to animals, tissues, and cells are critically needed in order to advance the field of mechanobiology, as few existing tools enable simultaneous imaging of tissue and cell deformation as well as cellular activity in live animals. Here, we introduce a novel microfluidic device that enables high-resolution optical imaging of cellular deformations and activity while applying precise mechanical stimuli to the surface of the worm’s cuticle with a pneumatic pressure reservoir. To evaluate device performance, we compared analytical and numerical simulations conducted during the design process to empirical measurements made with fabricated devices. Leveraging the well-characterized touch receptor neurons (TRNs) with an optogenetic calcium indicator as a model mechanoreceptor neuron, we established that individual neurons can be stimulated and that the device can effectively deliver steps as well as more complex stimulus patterns. This microfluidic device is therefore a valuable platform for investigating the mechanobiology of living animals and their mechanosensitive neurons.

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Investigation of mechanosensation in C elegans using light field calcium imaging

Cited by 6 publications

References 30 publications

Determining the biomechanics of touch sensation in C. elegans

Determining the biomechanics of touch sensation in C. elegans

How Caenorhabditis elegans Senses Mechanical Stress, Temperature, and Other Physical Stimuli

Pneumatic stimulation of C. elegans mechanoreceptor neurons in a microfluidic trap

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