The extraordinary AFD thermosensor of C. elegans

Goodman, Miriam B.; Sengupta, Piali

doi:10.1007/s00424-017-2089-5

Cited by 51 publications

(62 citation statements)

References 96 publications

(214 reference statements)

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“…Behavioral plasticity linked to prolonged changes in temperature has been previously studied in C. elegans in a variety of contexts, both in the innocuous [29,34,35] and noxious [28,36] range of temperatures. However, nothing is known about the impact of repeated acute thermal stimuli occurring over the hour time range.…”

Section: Long-term Adaptation Effect Upon Repeated Acute Thermal Stimmentioning

confidence: 99%

A system for the high-throughput analysis of acute thermal avoidance and adaptation in C. elegans

Lia

Glauser

2020

J Biol Methods

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Nociception and its plasticity are essential biological processes controlling adaptive behavioral responses in animals. These processes are also linked to different pain conditions in human and have received considerable attention, notably via studies in rodent models and the use of heat-evoked withdrawal behavior assays as a readout of unpleasant experience. More recently, invertebrates have also emerged as useful complementary models, with their own set of advantages, including their amenability to genetic manipulations, the accessibility and relative simplicity of their nervous system and ethical concerns linked to animal suffering. Like humans, the nematode Caenorhabditis elegans (C. elegans) can detect noxious heat and produce avoidance responses such as reversals. Here, we present a methodology suitable for the high-throughput analysis of C. elegans heat-evoked reversals and the adaptation to repeated stimuli. We introduce two platforms: the INFERNO (for infrared-evoked reversal analysis platform), allowing the quantification of the thermal sensitivity in a petri dish containing a large population (> 100 animals), and the ThermINATOR (for thermal adaptation multiplexed induction platform), allowing the mass-adaptation of up to 18 worm populations at the same time. We show that wild type animals progressively desensitize in response to repeated noxious heat pulses. Furthermore, analyzing the phenotype of mutant animals, we show that the mechanisms underlying baseline sensitivity and adaptation, respectively, are supported by genetically separable molecular pathways. In conclusion, the presented method enables the high-throughput evaluation of thermal avoidance in C. elegans and will contribute to accelerate studies in the field with this invertebrate model.

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Section: Long-term Adaptation Effect Upon Repeated Acute Thermal Stimmentioning

confidence: 99%

A system for the high-throughput analysis of acute thermal avoidance and adaptation in C. elegans

Lia

Glauser

2020

J Biol Methods

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“…This response requires two thermosensory neuron pairs in the head: AFD and FLP. The AFD neurons also contribute to thermotaxis in the innocuous temperature range (Aoki and Mori, 2015;Liu et al, 2012;Goodman and Sengupta, 2018). AFD mostly responds to thermal changes when they reach a certain threshold, and this response adapts relatively quickly (Hawk et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Specific Ion Channels Control Sensory Gain, Sensitivity, and Kinetics in a Tonic Thermonociceptor

et al. 2020

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Pain sensation and aversive behaviors entail the activation of nociceptor neurons, whose function is largely conserved across animals. The functional heterogeneity of nociceptors and ethical concerns are challenges for their study in mammalian models. Here, we investigate the function of a single type of genetically identified C. elegans thermonociceptor named FLP. Using calcium imaging in vivo, we demonstrate that FLP encodes thermal information in a tonic and graded manner over a wide thermal range spanning from noxious cold to noxious heat (8 C-36 C). This tonic-signaling mode allows FLP to trigger sustained behavioral changes necessary for escape behavior. Furthermore, we identify specific transient receptor potential, voltage-gated calcium, and sodium ''leak'' channels controlling sensory gain, thermal sensitivity, and signal kinetics, respectively, and show that the ryanodine receptor is required for long-lasting activation. Our work elucidates the task distribution among specific ion channels to achieve remarkable sensory properties in a tonic thermonociceptor in vivo.

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“…With the maximum-likelihood parameter values (see Table 3), the model can be interpreted as follows. The hidden variable x2 is a linear leaky integrator of the heat signal, storing the average recent value of the stimulus over about 1 s. While we do not know which exact neuron can be identified with x2, the thermosensory neurons AFD and FLP located in the head of the worm are strong candidates (30,31). The thermosensory neurons AFD respond to changes in temperature and are the primary sensors responsible for thermotaxis (30).…”

Section: B C Amentioning

confidence: 99%

Automated, predictive, and interpretable inference of Caenorhabditis elegans escape dynamics

Daniels

Ryu

Nemenman

2019

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

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The roundworm Caenorhabditis elegans exhibits robust escape behavior in response to rapidly rising temperature. The behavior lasts for a few seconds, shows history dependence, involves both sensory and motor systems, and is too complicated to model mechanistically using currently available knowledge. Instead we model the process phenomenologically, and we use the Sir Isaac dynamical inference platform to infer the model in a fully automated fashion directly from experimental data. The inferred model requires incorporation of an unobserved dynamical variable and is biologically interpretable. The model makes accurate predictions about the dynamics of the worm behavior, and it can be used to characterize the functional logic of the dynamical system underlying the escape response. This work illustrates the power of modern artificial intelligence to aid in discovery of accurate and interpretable models of complex natural systems.

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The extraordinary AFD thermosensor of C. elegans

Cited by 51 publications

References 96 publications

A system for the high-throughput analysis of acute thermal avoidance and adaptation in C. elegans

A system for the high-throughput analysis of acute thermal avoidance and adaptation in C. elegans

Specific Ion Channels Control Sensory Gain, Sensitivity, and Kinetics in a Tonic Thermonociceptor

Automated, predictive, and interpretable inference of Caenorhabditis elegans escape dynamics

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