During active exploration, the sensory cue perceived by an animal is constantly patterned by the animal's own movement. Thus, to track the sensory target rapid decisions on locomotory outputs are often generated by integrating the sensory information with the ongoing motor state. However, the neuronal mechanisms that govern sensorimotor integration remains largely unknown. When C. elegans steers towards an attractive odorant, the repeated head undulations allow the nematode to sample the odorant gradient within the space spanned by the head swings. We find that one half head undulation that swings between the most dorsal and the most ventral head positions is the smallest unit to generate the maximum performance on steering. Thus, we characterize how the sensorimotor integration during the half head undulations generates the steering decision. Our previous studies show that the axon of an interneuron RIA exhibits two activity patterns, the compartmentalized activity that encodes and regulates dorsal-ventral head undulations and the synchronized activity that is evoked by sensory stimulations [Hendricks et al., 2012]. We now find that disrupting RIA function alters the rapid steering decisions during chemotaxis. By imaging the calcium transients in the RIA axons in restrained and freely moving animals, we find that the two activity patterns quantitatively encode the concentration of the stimulating odorant versus the amplitude of head undulations and that sensory-evoked synchronized activity suppresses the motor-encoding compartmentalized activity during chemotactic steering. This axonal sensorimotor integration transduces the spatial gradient of the odorant into the asymmetry of the RIA axonal activities. We further show that asymmetric axonal output of RIA biases the steering during movements towards the attractant. In addition, we show that experience modulates chemotactic steering by regulating the sensorimotor integration in RIA. Together, our results characterize how sensorimotor integration gives rise to rapid steering decisions during chemotactic movements.

Affiliation:
- Department of Organismic and Evolutionary Biology, Center for Brain Science, Harvard University, Cambridge, MA 02138, USA