Reprogramming the topology of the nociceptive circuit in C. elegans reshapes sexual behavior

Pechuk, Vladyslava; Goldman, Gal; Salzberg, Yehuda; Chaubey, Aditi H.; Bola, R. Aaron; Hoffman, Jonathon R.; Endreson, Morgan L.; Miller, Renee M.; Reger, Noah; Portman, Douglas S.; Ferkey, Denise M.; Schneidman, Elad; Oren‐Suissa, Meital

doi:10.1016/j.cub.2022.08.038

Cited by 26 publications

(43 citation statements)

References 99 publications

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“…Since glutamate secretion from the head ASH and tail PHB sensory cells can be evoked by various stimuli, we predict that different modalities other than osmo-sensation, such as response to touch, toxins and other repellents, will show similar neuronal dynamics and behavioral modulation following exposure to spatially opposing cues 19,21,22,28,52,54,55 .…”

Section: Discussionmentioning

confidence: 99%

Section: Antagonistic Functions Of Head and Tail Signalingmentioning

confidence: 98%

“…Previous work indicated that ASH is the main nociceptive neuron, functioning through a compact circuit that controls nociceptive behaviors 19,28 (Figure 1A). Using a computational model we previously developed, we predicted which connections in the circuit could be inhibitory 28 . To do so, we added PHA and PHB to our previous circuit simulation and tested all the combinations of excitatory and inhibitory connections, such that each connection can be either inhibitory or excitatory (see Methods section for details).…”

Section: Antagonistic Functions Of Head and Tail Signalingmentioning

confidence: 98%

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Integration of spatially opposing cues by a single interneuron guides decision making inC. elegans

Gat

Pechuk

Peedikayil-Kurien

et al. 2023

Preprint

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The capacity of animals to integrate and respond to multiple hazardous stimuli in the surroundings is crucial for their survival. In mammals, complex evaluations of the environment require large numbers and different subtypes of neurons. The nematode C. elegans avoid hazardous chemicals they encounter by reversing their direction of movement. How does the worms compact nervous system processes the spatial information and directs the change of motion? We show here that a single interneuron, AVA, receives glutamatergic excitatory signals from head sensory neurons and glutamatergic inhibitory signals from the tail sensory neurons. AVA integrates the spatially distinct and opposing cues, whose output instructs the animals behavioral decision. We further find that the differential activation of AVA from the head and tail stems from distinct anatomical localization of inhibitory and excitatory glutamate-gated receptors along the AVA process, and from different threshold sensitivities of the sensory neurons to aversive stimuli. Our results thus uncover a cellular mechanism that mediates spatial computation of nociceptive cues for efficient decision-making in C. elegans.

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Section: Discussionmentioning

confidence: 99%

Section: Antagonistic Functions Of Head and Tail Signalingmentioning

confidence: 98%

Section: Antagonistic Functions Of Head and Tail Signalingmentioning

confidence: 98%

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Integration of spatially opposing cues by a single interneuron guides decision making inC. elegans

Gat

Pechuk

Peedikayil-Kurien

et al. 2023

Preprint

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“…For example, hermaphrodites detect foodrelated olfactory cues better than males due to enhanced expression of the odorant receptor ODR-10 in the AWA neuron 1 . Conversely, in the anterior nociceptive circuit, sensory detection of aversive cues seems identical in the two sexes, but the downstream connectivity to interneurons is highly dimorphic 10 . These topographical differences drive sexually dimorphic behavioral responses to nociceptive cues.…”

Section: Discussionmentioning

confidence: 98%

“…The sexually dimorphic behavior in response to the pheromone ESP1, for example, was shown to be mediated through dimorphic processing in third-and fourth-order brain areas 7,8 . Integration downstream to the sensory level is also evident in aggressive behavior in Drosophila and nociceptive behavior in C. elegans, where sexually dimorphic processing by downstream interneurons regulates the dimorphic behavior 9,10 . These examples demonstrate that for different types of sensory modalities, be it olfactory, auditory or chemo-aversion, sex differences can originate from dimorphism in distinct neuronal layers.…”

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confidence: 99%

Sexually dimorphic architecture and function of a mechanosensory circuit in C. elegans

et al. 2022

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How sensory perception is processed by the two sexes of an organism is still only partially understood. Despite some evidence for sexual dimorphism in auditory and olfactory perception, whether touch is sensed in a dimorphic manner has not been addressed. Here we find that the neuronal circuit for tail mechanosensation in C. elegans is wired differently in the two sexes and employs a different combination of sex-shared sensory neurons and interneurons in each sex. Reverse genetic screens uncovered cell- and sex-specific functions of the alpha-tubulin mec-12 and the sodium channel tmc-1 in sensory neurons, and of the glutamate receptors nmr-1 and glr-1 in interneurons, revealing the underlying molecular mechanisms that mediate tail mechanosensation. Moreover, we show that only in males, the sex-shared interneuron AVG is strongly activated by tail mechanical stimulation, and accordingly is crucial for their behavioral response. Importantly, sex reversal experiments demonstrate that the sexual identity of AVG determines both the behavioral output of the mechanosensory response and the molecular pathways controlling it. Our results present extensive sexual dimorphism in a mechanosensory circuit at both the cellular and molecular levels.

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Nematode-Trapping Fungi and Caenorhabditis elegans as a Model System for Predator–Prey Interactions

Vidal-Diez de Ulzurrun,

Juan,

Lin

et al. 2024

Fungal Associations

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Reprogramming the topology of the nociceptive circuit in C. elegans reshapes sexual behavior

Cited by 26 publications

References 99 publications

Integration of spatially opposing cues by a single interneuron guides decision making inC. elegans

Integration of spatially opposing cues by a single interneuron guides decision making inC. elegans

Sexually dimorphic architecture and function of a mechanosensory circuit in C. elegans

Nematode-Trapping Fungi and Caenorhabditis elegans as a Model System for Predator–Prey Interactions

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