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Summary Animals need to fine-control the speed and direction of locomotion to navigate complex and dynamic environments. To achieve this, they integrate multimodal sensory inputs with their internal drive to constantly adjust their motor output. This integration involves the interplay of neuronal populations across different hierarchical levels along the sensorimotor axis – from sensory, central, and modulatory neurons in the brain to descending neurons and motor networks in the nerve cord. Here, we characterize two populations of neurons that control distinct aspects of walking on different hierarchical levels inDrosophila. First, we usein-vivoelectrophysiological recordings to demonstrate that moonwalker descending neurons (MDN) integrate antennal touch to drive changes in walking direction from forward to backward. Second, we establish DopaMeander as an important component in the control of forward walking through a combination of optogenetic activation, silencing, connectomics, andin-vivorecordings. These dopaminergic modulatory neurons drive forward walking with increased turning, and the activity of individual neurons is correlated with ipsiversive turning. Hence, MDN and DopaMeander control opposite regimes of walking on different hierarchical levels. Computational models reveal that their activity predicts key parameters of spontaneous walking. Moreover, we find that both MDN and DopaMeander are gated out during flight. This suggests that neuronal populations across levels of control are modulated by the behavioral state to minimize cross-talk between motor programs. 

Technical and methodological advances in recent years have brought new ways to tackle major classical questions in insect motor control. Particularly, significant advancements were achieved in comprehending brain descending control by characterizing descending neurons, their targets in the ventral nerve cord (VNC), and how local networks there integrate sensory information. While physiological experiments in larger insects brought us a better understanding of how sensory modalities are processed locally in the VNC, the development and improvement of genetic tools, principally in Drosophila, opened the door to individually characterize actors at these three levels of information flow in behavioral control. This brief review brings together the names and roles of some of those actors, by highlighting the most significant findings from our perspective.