Although many properties of the nervous system are shared among animals and systems, it is not known whether different neuronal circuits use common strategies to guide behaviour. Here we characterize information processing by Caenorhabditis elegans olfactory neurons (AWC) and interneurons (AIB and AIY) that control food- and odour-evoked behaviours. Using calcium imaging and mutations that affect specific neuronal connections, we show that AWC neurons are activated by odour removal and activate the AIB interneurons through AMPA-type glutamate receptors. The level of calcium in AIB interneurons is elevated for several minutes after odour removal, a neuronal correlate to the prolonged behavioural response to odour withdrawal. The AWC neuron inhibits AIY interneurons through glutamate-gated chloride channels; odour presentation relieves this inhibition and results in activation of AIY interneurons. The opposite regulation of AIY and AIB interneurons generates a coordinated behavioural response. Information processing by this circuit resembles information flow from vertebrate photoreceptors to 'OFF' bipolar and 'ON' bipolar neurons, indicating a conserved or convergent strategy for sensory information processing.
There were errors published in J. Cell Sci. 123, 3447-3455. In Fig. 1, the arrows showing enzymatic reactions for MEC-17, HDAC6 and SIRT2 were pointing in the wrong direction. In addition, the C-terminal amino acid on the tail of -tubulin is Y (and not T). The correct figure is shown below. After publication of this Commentary, Shida and colleagues reported independent identification of MEC-17 homologs in diverse organisms as -tubulin acetyltransferases (Shida et al., 2010). Contrary to what we stated in our article and in the referenced paper (Akella et al., 2010), the newest version of the assembled genome of Chlamydomonas reinhardtii contains a sequence encoding an apparent homolog of the MEC-17 -tubulin acetyltransferase (locus ID Cre07.g345150).
Humans and other animals can sense temperature changes as small as 0.1°C. How animals achieve such exquisite sensitivity is poorly understood. By recording from the C. elegans thermosensory neurons AFD in vivo, we found that cooling closes and warming opens ion channels. We found that AFD thermosensitivity, which exceeds that of most biological processes by many orders of magnitude, is achieved by nonlinear signal amplification. Mutations in genes encoding subunits of a cyclic guanosine monophosphate (cGMP)-gated ion channel (tax-4 and tax-2) and transmembrane guanylate cyclases (gcy-8, gcy-18 and gcy-23) eliminated both cooling-and warming-activated thermoreceptor currents, indicating that a cGMP-mediated pathway links variations in temperature to changes in ionic currents. The resemblance of C. elegans thermosensation to vertebrate photosensation and the sequence similarity between TAX-4 and TAX-2 and subunits of the rod phototransduction channel raise the possibility that nematode thermosensation and vertebrate vision are linked by conserved evolution.Sensory abilities have evolved to encourage and support survival in complex natural environments. All animals have the ability to respond to thermal stimuli. As with vision, olfaction, taste and touch sensation, thermosensation relies on the ability of specialized sensory neurons to convert sensory stimuli into changes in ion currents. Given that temperature dependence is a universal feature of ion channel permeation and gating, however, identifying features that set thermosensory neurons apart is a challenge. In principle, these neurons could rely on specialized accessory structures and molecules or on a temperature-dependent enzymatic cascade to enhance thermosensitivity beyond the ordinary temperature dependence that is common to all neurons. Such specialized molecules or structures would act in parallel with the cellular processes that are required for normal neuronal function and whose temperature sensitivity is ordinary.C. elegans is an excellent animal for probing the cellular machinery responsible for temperature sensation and for identifying both shared and specialized aspects of temperature sensitivity. Many of the neurons required for temperature-guided behaviors are known 1,2 and all of them can be identified in living animals. Our work here concentrates on the AFD neurons, a pair of bilaterally symmetric, bipolar sensory neurons that terminate in modified ciliated endings in C. elegans have a complex, temperature-guided behavior that is characterized by experiencedependent plasticity, temperature-dependent migration (thermotaxis) and the ability to accurately track isotherms with 0.1°C precision 9-12 . Thus, C. elegans can detect temperature changes of 0.1°C or less. This stimulus, which carries much less energy than a single visible photon, corresponds to a change in thermal energy of kΔT or only 10 −23 J. Such sensitivity appears to be conferred by the AFD thermosensory neurons, as animals that lack AFD 2 or carry mutations that disrupt it...
Background Caenorhabditis elegans locomotion is a simple behavior that has been widely used to dissect genetic components of behavior, synaptic transmission, and muscle function. Many of the paradigms that have been created to study C. elegans locomotion rely on qualitative experimenter observation. Here we report the implementation of an automated tracking system developed to quantify the locomotion of multiple individual worms in parallel.Methodology/Principal FindingsOur tracking system generates a consistent measurement of locomotion that allows direct comparison of results across experiments and experimenters and provides a standard method to share data between laboratories. The tracker utilizes a video camera attached to a zoom lens and a software package implemented in MATLAB®. We demonstrate several proof-of-principle applications for the tracker including measuring speed in the absence and presence of food and in the presence of serotonin. We further use the tracker to automatically quantify the time course of paralysis of worms exposed to aldicarb and levamisole and show that tracker performance compares favorably to data generated using a hand-scored metric.Conclusions/SignficanceAlthough this is not the first automated tracking system developed to measure C. elegans locomotion, our tracking software package is freely available and provides a simple interface that includes tools for rapid data collection and analysis. By contrast with other tools, it is not dependent on a specific set of hardware. We propose that the tracker may be used for a broad range of additional worm locomotion applications including genetic and chemical screening.
The ability to sense and respond to mechanical stimuli emanates from sensory neurons and is shared by most, if not all animals. Exactly how such neurons receive and distribute mechanical signals during touch sensation remains mysterious. Here, we show that sensation of mechanical forces depends on a continuous, pre-stressed spectrin cytoskeleton inside neurons. Mutations in the tetramerization domain of C. elegans β-spectrin (UNC-70), an actin-membrane cross-linker, cause defects in sensory neuron morphology under compressive stress in moving animals. Through AFM force spectroscopy experiments on isolated neurons, in vivo laser axotomy and FRET imaging to measure force across single cells and molecules, we show that spectrin is held under constitutive tension in living animals, which contributes to an elevated pre-stress in touch receptor neurons. Genetic manipulations that decrease such spectrin-dependent tension also selectively impair touch sensation, suggesting that such pretension is essential for efficient responses to external mechanical stimuli.
Like other ectotherms, the roundworm Caenorhabditis elegans and the fruit fly Drosophila melanogaster rely on behavioral strategies to stabilize their body temperature. Both animals use specialized sensory neurons to detect small changes in temperature, and the activity of these thermosensors governs the neural circuits that control migration and accumulation at preferred temperatures. Despite these similarities, the underlying molecular, neuronal, and computational mechanisms responsible for thermotaxis are distinct in these organisms. Here, we discuss the role of thermosensation in the development and survival of C. elegans and Drosophila, and review the behavioral strategies, neuronal circuits, and molecular networks responsible for thermotaxis behavior.The ability to sense and respond to ambient temperature is crucial for the survival and fitness of all animals. Endotherms such as birds and mammals maintain a relatively constant body temperature regardless of ambient temperature via a number of mechanisms, including behavioral modification, as well as central regulation of autonomic nervous system functions (Hensel 1973;Simon et al. 1986). However, for ectotherms like Caenorhabditis elegans and Drosophila melanogaster, whose body temperature varies with ambient temperature, behavioral strategies are the primary mechanism for regulating optimal internal temperature (Stevenson 1985;Huey et al. 2003). In this review, we describe the known neuronal and molecular strategies used by C. elegans and Drosophila to detect and behaviorally respond to changes in temperature, focusing particularly on temperatureguided behaviors that operate within each animal's normal thermal zone. A note on terminologyVarious terms have been used to describe patterns of thermotactic movement in C. elegans and Drosophila. For instance, worms moving down temperature gradients toward cooler temperatures are said to be ''cryophilic'' (Fig. 1A), while the same behavior executed by flies is called ''warmth avoidance.'' By the same logic, movements up temperature gradients have been called ''thermophilic'' in worms and ''cold avoidance'' behavior in flies (Fig. 1B). Here, movement down and up temperature gradients will be referred to as ''negative thermotaxis'' and ''positive thermotaxis,'' respectively. In addition to positive and negative thermotaxis, worms have a robust tendency to move along isothermal contours when they are near their preferred temperature, a behavior referred to as ''isothermal tracking'' (Fig. 1E). Isothermal tracking has not been observed in flies. The ethology of thermotaxis in C. elegans and D. melanogasterTemperature is an environmental variable that affects the rate and nature of all chemical reactions, and hence has dramatic effects on animal physiology. At the extremes of the temperature spectrum, exposure to excessive heat or cold causes dramatic perturbations in cellular physiology that rapidly lead to the failure of nervous system function and to serious tissue damage. Thus, thermal nociception-the ability to ...
Focused ultrasound has been shown to stimulate excitable cells, but the biophysical mechanisms behind this phenomenon remain poorly understood. To provide additional insight, we devised a behavioral-genetic assay applied to the well-characterized nervous system of nematodes. We found that pulsed ultrasound elicits robust reversal behavior in wild-type animals in a pressure-, duration-, and pulse protocol-dependent manner. Responses were preserved in mutants unable to sense thermal fluctuations and absent in mutants lacking neurons required for mechanosensation. Additionally, we found that the worm's response to ultrasound pulses rests on the expression of MEC-4, a DEG/ENaC/ASIC ion channel required for touch sensation. Consistent with prior studies of MEC-4-dependent currents, the worm's response was optimal for pulses repeated 300-1000 times per second. Based on these findings, we conclude that mechanical, rather than thermal, stimulation accounts for behavioral responses. Further, we propose that acoustic radiation force governs the response to ultrasound in a manner that depends on the touch receptor neurons and MEC-4-dependent ion channels. Our findings illuminate a complete pathway of ultrasound action, from the forces generated by propagating ultrasound to an activation of a specific ion channel. The findings further highlight the importance of optimizing ultrasound pulsing protocols when stimulating neurons via ion channels with mechanosensitive properties. How ultrasound influences neurons and other excitable cells has remained a mystery for decades. Although it is widely understood that ultrasound can heat tissues and induce mechanical strain, whether or not neuronal activation depends on heat, mechanical force, or both physical factors is not known. We harnessed nematodes and their extraordinary sensitivity to thermal and mechanical stimuli to address this question. Whereas thermosensory mutants respond to ultrasound similar to wild-type animals, mechanosensory mutants were insensitive to ultrasound stimulation. Additionally, stimulus parameters that accentuate mechanical effects were more effective than those producing more heat. These findings highlight a mechanical nature of the effect of ultrasound on neurons and suggest specific ways to optimize stimulation protocols in specific tissues.
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