Concerted pulsatile and graded neural dynamics enables efficient chemotaxis in C. elegans

Itskovits, Eyal; Ruach, Rotem; Zaslaver, Alon

doi:10.1038/s41467-018-05151-2

Cited by 43 publications

(85 citation statements)

References 58 publications

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“…Such context-dependent behavioral regulation is also observed upon switching between escape and avoidance from noxious heat (35) and switching between reversal and curve during acidic pH avoidance (38). Even during a continuous navigation behavior, distinct behavioral strategies are executed depending on the distance from a destination, each of which is performed via distinct sensory neurons (39). These observations tell us that the discrimination of environmental contexts is a critical step to investigate the nervous system.…”

Section: Discussionmentioning

confidence: 92%

Context-dependent operation of neural circuits underlies a navigation behavior in Caenorhabditis elegans

Ikeda

Nakano

Giles

et al. 2020

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

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The nervous system evaluates environmental cues and adjusts motor output to ensure navigation toward a preferred environment. The nematode Caenorhabditis elegans navigates in the thermal environment and migrates toward its cultivation temperature by moving up or down thermal gradients depending not only on absolute temperature but on relative difference between current and previously experienced cultivation temperature. Although previous studies showed that such thermal context-dependent opposing migration is mediated by bias in frequency and direction of reorientation behavior, the complete neural pathways-from sensory to motor neurons-and their circuit logics underlying the opposing behavioral bias remain elusive. By conducting comprehensive cell ablation, high-resolution behavioral analyses, and computational modeling, we identified multiple neural pathways regulating behavioral components important for thermotaxis, and demonstrate that distinct sets of neurons are required for opposing bias of even single behavioral components. Furthermore, our imaging analyses show that the context-dependent operation is evident in sensory neurons, very early in the neural pathway, and manifested by bidirectional responses of a first-layer interneuron AIB under different thermal contexts. Our results suggest that the contextual differences are encoded among sensory neurons and a first-layer interneuron, processed among different downstream neurons, and lead to the flexible execution of context-dependent behavior.neural circuits | context dependency | C. elegans | navigation behavior | behavioral modeling T he nervous system detects environmental cues and adjusts motor commands for navigation toward preferred environments (1, 2). What constitutes a preference depends on situation and context, thus animals need to integrate environmental stimuli with contextual information for appropriate motor responses. Such context-dependent neural processing is critical for the flexible migration of animals (3, 4). However, the neural circuit basis of context-dependent behavioral regulation is not well understood.Despite having a compact nervous system consisting of only 302 neurons, the nematode Caenorhabditis elegans can navigate thermal gradients, known as thermotaxis. Importantly, their navigation drastically changes depending on thermal context: their position on the thermal gradient relative to a temperature they recently experienced and memorized because they found food in that condition (5)(6)(7)(8). For experimentation, we define this thermal context as the difference between their current temperature on the gradient (T) and their cultivation temperature (T c ), set by cultivating animals with food at a certain temperature. On a thermal gradient without food, animals migrate up the thermal gradient toward T c when T is 1 to 5°C lower than T c (T < T c ) and migrate down the gradient when T is 1 to 5°C higher than T c (T > T c ) ( Fig. 1 A-C). When T is much higher than T c (T >> T c ), animals still manage to migrate toward T c ,...

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Section: Discussionmentioning

confidence: 92%

Context-dependent operation of neural circuits underlies a navigation behavior in Caenorhabditis elegans

Ikeda

Nakano

Giles

et al. 2020

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

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“…While it is ideal to measure activity and behavior at the same time, this is often not possible, and precisely controlling stimuli is difficult in freely-moving animals. With the exception of temperature, the attention paid to C. elegans behavior to stimulus gradients has not been matched by analysis of neural responses to graded stimuli, and it is clear there are important differences in responses to graded versus stepped stimuli (Itskovits et al, 2018; Larsch et al, 2015; Luo et al, 2014). Our approach overcomes this technical barrier to allow easy analysis of neuronal responses to gradients.…”

Section: Resultsmentioning

confidence: 99%

Asymmetric adaptation reveals functional lateralization for graded versus discrete stimuli

Desrochers

Lange

Hendricks

2018

Preprint

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150 words 9Animal navigation strategies depend on the nature of the environmental cues used. In the 10 nematode Caenorhabditis elegans, navigation has been studied in the context of gradients of 11 attractive or repellent stimuli as well is in response to acute aversive stimuli. We wanted to 12 better understand how sensory responses to the same stimulus vary between graded and acute 13 stimuli, and how this variation relates to behavioral responses. C. elegans has two salt-sensing 14 neurons, ASEL and ASER, that show opposite responses to stepped changes in stimulus levels, 15 however only ASER has been shown to play a prominent role in salt chemotaxis. We used pre-16 exposure to natural stimuli to manipulate the responsiveness of these neurons and tested their 17 separate contributions to behavior. Our results suggest ASEL is specialized for responses to 18 acute stimulus changes. We also found that ASER remains responsive to graded stimuli under 19 conditions where it is unresponsive to large steps. 20 21 22 attractant my change over orders of magnitude. At the same time, animals must remain 33 sensitive to abrupt changes in stimuli that may require acute behavioral responses. 34 In Caenorhabditis elegans, salt chemotaxis has been used to dissect navigation strategies 35 used at the genetic, cellular, circuit, and behavioral levels . The primary salt sensing neurons in 36 C. elegans, ASEL and ASER, exhibit opposite responses to stepped changes in salt 37 concentration: ASEL is activated by cations and responds to up-steps in salt concentration, 38 while ASER detects anions and responds to down-steps (Pierce-Shimomura et al., 2001; 39 Suzuki et al., 2008). Under most conditions, gradient chemotaxis in the nematode 40 Caenorhabditis elegans can be described as a biased random walk, a strategy identical to that 41 used by single-celled organisms like bacteria, multicellular growth processes observed in plant 42 roots, and even subcellular structures like axonal growth cones (Berg and Brown, 1972; Pierce-43 Shimomura et al., 1999). While C. elegans does respond to salt up-steps and down-steps (Miller 44 et al., 2005), most behavioral analysis is done in the context of gradient navigation. However, 45 the physiological properties of ASEL and ASER are less well-explored in the context of graded 46 stimuli. ASER shows complex calcium responses to gradients that depend both on the direction 47 of salt change and whether salt levels are above or below a memorized cultivation 48 concentration (Luo et al., 2014). While ASEL contributes to forward locomotion during 49 exposure to attractive salt concentrations (Suzuki et al., 2008), ASEL has been found to be 50 largely dispensable for both positive and negative salt gradient chemotaxis (Kunitomo et al., 51 2013; Luo et al., 2014), though recently it was shown that optogenetic stimulation of ASEL can 52 drive fictive positive chemotaxis under specific conditions (Wang et al., 2017). 53We were interested in attempting to reconcile calcium imaging experiments, usually 54 per...

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“…Slow sustained increases in odor concentration caused by the animal's directed locomotion appear more likely to induce spiking in AWA. Indeed, in intact animals, slow odor increases drive pulsatile, self-terminating AWA calcium transients that might correspond to action potential bursts (Larsch et al, 2015;Itskovits et al, 2018).…”

Section: Awa Spiking As a Filter Of Odor Stimulimentioning

confidence: 99%

C. elegans AWA Olfactory Neurons Fire Calcium-Mediated All-or-None Action Potentials

Liu

Kidd

Dobosiewicz

et al. 2018

Cell

110

133

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Neurons in Caenorhabditis elegans and other nematodes have been thought to lack classical action potentials. Unexpectedly, we observe membrane potential spikes with defining characteristics of action potentials in C. elegans AWA olfactory neurons recorded under current-clamp conditions. Ion substitution experiments, mutant analysis, pharmacology, and modeling indicate that AWA fires calcium spikes, which are initiated by EGL-19 voltage-gated CaV1 calcium channels and terminated by SHK-1 Shaker-type potassium channels. AWA action potentials result in characteristic signals in calcium imaging experiments. These calcium signals are also observed when intact animals are exposed to odors, suggesting that natural odor stimuli induce AWA spiking. The stimuli that elicit action potentials match AWA's specialized function in climbing odor gradients. Our results provide evidence that C. elegans neurons can encode information through regenerative all-or-none action potentials, expand the computational repertoire of its nervous system, and inform future modeling of its neural coding and network dynamics.

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Concerted pulsatile and graded neural dynamics enables efficient chemotaxis in C. elegans

Cited by 43 publications

References 58 publications

Context-dependent operation of neural circuits underlies a navigation behavior in Caenorhabditis elegans

Context-dependent operation of neural circuits underlies a navigation behavior in Caenorhabditis elegans

Asymmetric adaptation reveals functional lateralization for graded versus discrete stimuli

C. elegans AWA Olfactory Neurons Fire Calcium-Mediated All-or-None Action Potentials

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