Thermotaxis of C. elegans as a model for temperature perception, neural information processing and neural plasticity

Kimata, Tsubasa; Sasakura, Hiroyuki; Ohnishi, Noriyuki; Nishio, Nana; Mori, Ikue

doi:10.4161/worm.19504

Cited by 58 publications

(43 citation statements)

References 73 publications

(121 reference statements)

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“…As a close paralog of NPR-1 (de Bono and Bargmann 1998), NPR-2 acts in the AIZ interneurons to regulate C. elegans avoidance to MeSa (Figure 4). AIZs also have a well-defined function in mediating cryophilic migration (Mori and Ohshima 1995;Kimata et al 2012) and are involved in chemotaxis to NaCl (Iino and Yoshida 2009) and aversive olfactory learning (Ha et al 2010). These findings suggest that AIZs might function like RMGs as an integrating site for various sensory stimuli.…”

Section: Discussionmentioning

confidence: 94%

“…A combination of the neural connection diagram with molecular analyses will likely eventually lead to a systematic understanding of the neural regulation of a behavior, from key regulatory molecules to signaling integration in neural circuits. Several examples of such efforts include the dissection of a hub-and-spoke circuit that controls C. elegans social behavior ), the thermotaxis circuit (Kimata et al 2012), the circuit that generates long-lasting roaming and dwelling states , the mechanosensation circuit (Chalfie et al 1985), and the behavioral quiescence circuit (Choi et al 2013).…”

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confidence: 99%

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Neuropeptide Receptors NPR-1 and NPR-2 RegulateCaenorhabditis elegansAvoidance Response to the Plant Stress Hormone Methyl Salicylate

Luo¹,

Xu²,

Tan

et al. 2014

Genetics

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Methyl salicylate (MeSa) is a stress hormone released by plants under attack by pathogens or herbivores . MeSa has been shown to attract predatory insects of herbivores and repel pests. The molecules and neurons underlying animal response to MeSa are not known. Here we found that the nematode Caenorhabditis elegans exhibits a strong avoidance response to MeSa, which requires the activities of two closely related neuropeptide receptors NPR-1 and NPR-2. Molecular analyses suggest that NPR-1 expressed in the RMG inter/motor neurons is required for MeSa avoidance. An NPR-1 ligand FLP-18 is also required. Using a rescuing npr-2 promoter to drive a GFP transgene, we identified that NPR-2 is expressed in multiple sensory and interneurons. Genetic rescue experiments suggest that NPR-2 expressed in the AIZ interneurons is required for MeSa avoidance. We also provide evidence that the AWB sensory neurons might act upstream of RMGs and AIZs to detect MeSa. Our results suggest that NPR-2 has an important role in regulating animal behavior and that NPR-1 and NPR-2 act on distinct interneurons to affect C. elegans avoidance response to MeSa. KEYWORDS C. elegans; methyl salicylate; npr-1; npr-2; interneuron P LANTS emit odorants that can affect animal behaviors. The identification of the molecules and neurons regulating these behaviors remains a central task for understanding an animal's nervous system.Methyl salicylate (MeSa) is a volatile stress hormone released by plants when infected by pathogens (Park et al. Caenorhabditis elegans has been an efficient model for studying the molecular and neural mechanisms underlying odorant-elicited behaviors (Bargmann 2006(Bargmann , 2012. Specifically, the detailed description of the neural connections by reconstructing serial-section electron microscopic pictures of the animals (White et al. 1986) provides a unique map for dissecting the neural correlates of each individual behavior. A combination of the neural connection diagram with molecular analyses will likely eventually lead to a systematic understanding of the neural regulation of a behavior, from key regulatory molecules to signaling integration in neural circuits. Several examples of such efforts include the dissection of a hub-and-spoke circuit that controls C. elegans social behavior ), the thermotaxis circuit (Kimata et al. 2012), the circuit that generates long-lasting roaming and dwelling states , the mechanosensation circuit (Chalfie et al. 1985), and the behavioral quiescence circuit (Choi et al. 2013). We found that C. elegans strongly avoids MeSa, suggesting that this animal can be used for studying the molecular and neuronal mechanisms underlying the behavioral effects of MeSa. In this study we identified multiple genes important for the behavior and analyzed in detail how neuropeptide receptors NPR-1 and NPR-2 and neuropeptide FLP-18 act in different neurons to affect the avoidance behavior. Materials and MethodsStrains are listed in Supporting Information, File S1.MeSa avoidance assay C. elegans avoidance...

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Section: Discussionmentioning

confidence: 94%

mentioning

confidence: 99%

Neuropeptide Receptors NPR-1 and NPR-2 RegulateCaenorhabditis elegansAvoidance Response to the Plant Stress Hormone Methyl Salicylate

Luo¹,

Xu²,

Tan

et al. 2014

Genetics

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“…Previous studies established C. elegans thermotaxis as a model for experience-dependent navigation (2)(3)(4)(5)(6). When worms are exposed to specific temperatures between 15°C and 25°C for at least 4 h, they adopt those temperatures as their thermotactic setpoint (T s ) (2,3,5,7).…”

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confidence: 99%

Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons

Luo

Cook

Venkatachalam

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

103

116

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The nematode Caenorhabditis elegans navigates toward a preferred temperature setpoint (T s ) determined by long-term temperature exposure. During thermotaxis, the worm migrates down temperature gradients at temperatures above T s (negative thermotaxis) and performs isothermal tracking near T s . Under some conditions, the worm migrates up temperature gradients below T s (positive thermotaxis). Here, we analyze positive and negative thermotaxis toward T s to study the role of specific neurons that have been proposed to be involved in thermotaxis using genetic ablation, behavioral tracking, and calcium imaging. We find differences in the strategies for positive and negative thermotaxis. Negative thermotaxis is achieved through biasing the frequency of reorientation maneuvers (turns and reversal turns) and biasing the direction of reorientation maneuvers toward colder temperatures. Positive thermotaxis, in contrast, biases only the direction of reorientation maneuvers toward warmer temperatures. We find that the AFD thermosensory neuron drives both positive and negative thermotaxis. The AIY interneuron, which is postsynaptic to AFD, may mediate the switch from negative to positive thermotaxis below T s . We propose that multiple thermotactic behaviors, each defined by a distinct set of sensorimotor transformations, emanate from the AFD thermosensory neurons. AFD learns and stores the memory of preferred temperatures, detects temperature gradients, and drives the appropriate thermotactic behavior in each temperature regime by the flexible use of downstream circuits.N avigational behaviors provide a framework for exploring the interplay among sensorimotor circuits, learning, and memory. During a navigational task, animals eventually reach their goals by implementing strategies composed of sensorimotor rules. Experience can modify navigational goals, so memory can also be integrated into sensorimotor pathways. Studying navigation in the nematode Caenorhabditis elegans offers the possibility of understanding the plasticity and programming of sensorimotor circuits from input to output in a small nervous system (1).Previous studies established C. elegans thermotaxis as a model for experience-dependent navigation (2-6). When worms are exposed to specific temperatures between 15°C and 25°C for at least 4 h, they adopt those temperatures as their thermotactic setpoint (T s ) (2, 3, 5, 7). When placed on a spatial temperature gradient, worms seek the T s . When arriving near T s , worms track isotherms. Genetic analysis of thermotaxis has yielded mutants that are athermotactic (crawling randomly on temperature gradients), cryophilic (crawling to the coldest point on a temperature gradient irrespective of T s ), or thermophilic (crawling to the warmest point on a temperature gradient). This observation led to the suggestion that thermotaxis might involve separate circuits for negative thermotaxis (movement down gradients) and positive thermotaxis (movement up gradients) that balance near T s (2, 4).Systematic laser ablation a...

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“…17,18 The steepness of the temperature gradient is an important factor for the thermotaxis of C. elegans. 19 When the temperature gradient is over 1 C/cm, the worms with low cultivation temperature show normal thermotaxis. On the contrary, the worms with high cultivation temperature show an athermotactic response.…”

Section: Introductionmentioning

confidence: 99%

Microfluidic Platform for Analyzing the Thermotaxis of C. elegans in a Linear Temperature Gradient

et al. 2017

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Caenorhabditis elegans (C. elegans), which shares a considerable amount of characteristics with human genes is one of the important model organisms for the study of behavioral responses. Thermotaxis is a representative behavior response of C. elegans; C. elegans stores the cultivation temperature in thermosensory neurons and moves to the cultivation temperature region in a temperature variation. In this study, we developed a microfluidic system for effective thermotaxis analysis of C. elegans. The microfluidic channel was fabricated using polydimethylsiloxane (PDMS) by soft lithography process. The temperature gradient (15 -20 C) was generated in the microchannel and controlled by Peltier modules attached to the bottom of the channel. The thermotaxis of wild type (N2), tax-4(p678) and ttx-7(nj50) mutants were effectively analyzed using this microfluidic system. We believe that this system can be employed as a basic platform for studying the neural circuit of C. elegans responding to external stimuli.

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Thermotaxis of C. elegans as a model for temperature perception, neural information processing and neural plasticity

Cited by 58 publications

References 73 publications

Neuropeptide Receptors NPR-1 and NPR-2 RegulateCaenorhabditis elegansAvoidance Response to the Plant Stress Hormone Methyl Salicylate

Neuropeptide Receptors NPR-1 and NPR-2 RegulateCaenorhabditis elegansAvoidance Response to the Plant Stress Hormone Methyl Salicylate

Bidirectional thermotaxis in Caenorhabditis elegans is mediated by distinct sensorimotor strategies driven by the AFD thermosensory neurons

Microfluidic Platform for Analyzing the Thermotaxis of C. elegans in a Linear Temperature Gradient

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