Turning neurons RIV, SMB, and SAAD gates mechanosensory response in C. elegans upstream of AVA

An important goal of the nervous system is to integrate sensory cues with an animal’s current behavior state to generate a suitable motor response. However, the underlying neuronal mechanism behind how neural circuits integrate sensory and behavior signals remains unknown. To answer this question, we performed a systematic high-throughput optogenetic interrogation of the neural circuits underlying mechanosensorimotor processing in the nematode C. elegans. When C. elegans detects gentle touch from the environment, it usually responds by moving backward, also known as reversals. The likelihood of reversing depends on the current behavior state of the worm. A worm is less likely to reverse in response to a touch stimulus delivered during turning than one delivered when moving forward. To understand the underlying circuit mechanism, we optogenetically activated downstream interneurons in the mechanosensory processing pathway when the animal was either moving forward or turning. Activation of interneurons AIZ, RIM, AIB, or AVE, during forward locomotion, were much more likely to evoke reversals than did activation during turning. In contrast, activation of neuron AVA evoked reversals with similar likelihood regardless of whether the worm was moving forward or turning, suggesting that AVA lies functionally downstream of the integration of turning and mechanosensory related signals. We propose that turning neurons RIV, SMB, and SAAD send turning-related signals that inhibit or disrupt mechanosensory signals. When we inhibited these turning-related neurons, it restored the animal’s evoked reversal response to mechanosensory stimuli, even during turns. Taken together, these results suggest a potential circuit mechanism in which signals from turning neurons RIV, SMB, and SAAD act as a gate to inhibit or impede the propagation of mechanosensory-related signals, and that these turning related signals act somewhere upstream of neuron AVA.