Integration of spatially opposing cues by a single interneuron guides decision-making in C. elegans

• Published in: Cell reports (Cambridge) Vol. 42; no. 9; p. 113075
• Main Authors: Gat, Asaf, Pechuk, Vladyslava, Peedikayil-Kurien, Sonu, Karimi, Shadi, Goldman, Gal, Sela, Sapir, Lubliner, Jazz, Krieg, Michael, Oren-Suissa, Meital
• Format: Journal Article
• Language: English
• Published: Elsevier Inc 26.09.2023; Elsevier
• Subjects: CP: Neuroscience; sensory integration, nociception, avoidance behaviors, glutamate-gated chloride channels, microfluidics, spatial decision-making, AVR-14, C. elegans; CP: Neuroscience; sensory integration, nociception, avoidance behaviors, glutamate-gated chloride channels, microfluidics, spatial decision-making, AVR-14, C. elegans
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2023.113075

The capacity of animals to respond to hazardous stimuli in their 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 avoids hazardous chemicals they encounter by reversing their direction of movement. How does the worms’ compact nervous system process the spatial information and direct motion change? We show here that a single interneuron, AVA, receives glutamatergic excitatory and inhibitory signals from head and tail sensory neurons, respectively. AVA integrates the spatially distinct and opposing cues, whose output instructs the animal’s behavioral decision. We further find that the differential activation of AVA stems from distinct localization of inhibitory and excitatory glutamate-gated receptors along AVA’s process and from different threshold sensitivities of the sensory neurons. Our results thus uncover a cellular mechanism that mediates spatial computation of nociceptive cues for efficient decision-making in C. elegans. [Display omitted] •Tail sensation of nociceptive cues antagonizes head-induced neuronal responses•A single neuron, AVA, receives spatially distinct and opposing signals•Excitatory and inhibitory glutamate-gated channels are spatially partitioned•Glutamatergic E/I information is integrated by AVA and directs decision-making Gat et al. discover a cellular mechanism that mediates spatial computation of nociceptive cues for efficient decision-making in C. elegans. Head and tail sensory neurons show different threshold sensitivities to aversive stimuli and elicit AVA excitation or inhibition, respectively, by activating distinct glutamate signaling pathways.