Parallel sensorimotor pathways control landing in Drosophila
1 Julius-Maximilians-University of Würzburg, Neurobiology and Genetics, Theodor-Boveri-Institute, Würzburg, Germany
2 HHMI Janelia Research Campus, VA, USA
3 Zuckerman Institute, Columbia University in the City of New York, Greene Science Center, NY, USA
Landing is the final and arguably most critical stage of flight. To avoid impact injuries, animals decelerate by modulating wing and body kinematics and extend their legs in a well-coordinated movement sequence before touchdown. This is a challenging motor task, which depends on the integration of different sensory modalities, in particular visual cues. However, how visual cues are integrated by peripheral and central networks in the brain and conveyed to lower-level motor networks in the ventral nerve cord (VNC) to control landing is largely unknown. Here, we analyzed the distributed control of landing in the nervous system of Drosophila. Previous work has characterized early visual processing circuits, the landing behavior, and two descending neurons (DNs) controlling landing. Using a combination of light microscopy and connectomics approaches, we now identified complete neuronal pathways for landing from the brain to motor neurons in the VNC. By combining genetic activation and silencing with behavioral tracking, we then validated their functionality. We identified four classes of visual projection neurons (VPNs) that consistently drove landing upon optogenetic activation. Silencing three of these significantly impaired visually evoked landing responses. Hence, these VPNs are core components of the landing circuitry. The VPNs synapse directly onto a population of DNs which project to motor circuits in the VNC. Activating different VPNs and DNs drove landing responses with distinct leg, body, and wing kinematics. Finally, we used a connectome of the VNC to identify novel DNs based on their shared synaptic outputs in the VNC with previously described landing DNs. Different types of landing DNs recruit distinct sets of leg and wing motor neurons and drive different landing responses. Together, our findings elucidate parallel sensorimotor pathways from the brain to the VNC that enable flexible landing responses involving coordinated movements of all body appendages.