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An animal’s current behavior influences its response to sensory stimuli, but the molecular and circuitlevel mechanisms of this context-dependent decision-making are not well understood. Caenorhabditis elegans are less likely to respond to a mechanosensory stimulus by reversing if the stimuli is received while the animal turns. Inhibitory feedback from turning associated neurons are needed for this gating. But until now, it has remained unknown precisely where in the circuit gating occurs and which specific neurons and receptors receive inhibition from the turning circuitry. Here, we use genetic manipulations, single-cell rescue experiments, and high-throughput closed-loop optogenetic perturbations during behavior to reveal the specific neuron and receptor responsible for receiving inhibition and altering sensorimotor processing. Our measurements show that an inhibitory acetylcholine-gated chloride channel comprising LGC-47 and ACC-1 expressed in neuron type RIM disrupts mechanosensory evoked reversals during turns, presumably in response to inhibitory signals from turning-associated neuron SAA.
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Inhibitory feedback from the motor circuit gates mechanosensory processing in Caenorhabditis elegans
Animals must integrate sensory cues with their current behavioral context to generate a suitable response. How this integration occurs is poorly understood. Previously, we developed high-throughput methods to probe neural activity in populations ofCaenorhabditis elegansand discovered that the animal’s mechanosensory processing is rapidly modulated by the animal’s locomotion. Specifically, we found that when the worm turns it suppresses its mechanosensory-evoked reversal response. Here, we report thatC.elegansuse inhibitory feedback from turning-associated neurons to provide this rapid modulation of mechanosensory processing. By performing high-throughput optogenetic perturbations triggered on behavior, we show that turning-associated neurons SAA, RIV, and/or SMB suppress mechanosensory-evoked reversals during turns. We find that activation of the gentle-touch mechanosensory neurons or of any of the interneurons AIZ, RIM, AIB, and AVE during a turn is less likely to evoke a reversal than activation during forward movement. Inhibiting neurons SAA, RIV, and SMB during a turn restores the likelihood with which mechanosensory activation evokes reversals. Separately, activation of premotor interneuron AVA evokes reversals regardless of whether the animal is turning or moving forward. We therefore propose that inhibitory signals from SAA, RIV, and/or SMB gate mechanosensory signals upstream of neuron AVA. We conclude thatC.elegansrely on inhibitory feedback from the motor circuit to modulate its response to sensory stimuli on fast timescales. This need for motor signals in sensory processing may explain the ubiquity in many organisms of motor-related neural activity patterns seen across the brain, including in sensory processing areas.
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- Award ID(s):
- 1845137
- PAR ID:
- 10515211
- Editor(s):
- Sengupta, Piali
- Publisher / Repository:
- Public Library of Science
- Date Published:
- Journal Name:
- PLOS Biology
- Volume:
- 21
- Issue:
- 9
- ISSN:
- 1545-7885
- Page Range / eLocation ID:
- e3002280
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pbio.3002280
