Control of walking direction by descending and dopaminergic neurons in Drosophila

Animals fine-control the speed and direction of locomotion to navigate complex and dynamic environments. To achieve this, they integrate multimodal sensory cues with their internal drive to constantly adjust motor output. This 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 in Drosophila. First, we use in vivo electrophysiological recordings to demonstrate that moonwalker descending neurons (MDNs) integrate antennal touch to drive changes in walking direction from forward to backward. Second, we establish DopaMeander neurons as an important component in the control of forward walking by combining optogenetic activation, silencing, connectomics, and in vivo recordings. 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 at different hierarchical levels. Computational models reveal that their activity predicts key parameters of spontaneous walking. Moreover, both MDN and DopaMeander are gated out during flight, suggesting that neuronal populations across levels of control are modulated by the behavioral state to minimize crosstalk between motor programs.