Fine-grained descending control of steering in walking Drosophila

Purposeful, directed locomotion requires descending signals from the brain, but
we do not understand which features of locomotion are conveyed nor how these
descending signals are organized. Here, we investigate how descending neurons,
which connect the brain to the ventral nerve cord, control steering in walking
Drosophila melanogaster. By tracking leg movements in freely walking flies, we
found that different steering maneuvers involve different combinations of leg movements.
Specifically, one gesture was more prominent in turns where the fly increased its forward
velocity, whereas another gesture was more prominent in turns where the fly decreased its forward
velocity. Second, focusing on two descending neuron cell types and using optogenetic
manipulation and whole-cell, patch-clamp electrophysiology, we found that DNg13 drives the
first gesture, while DNa02 drives the second gesture. Electron microscopy connectomics
revealed that DNg13 and DNa02 are downstream from largely non-overlapping networks in the
brain, implying that these descending neurons can be recruited independently. We propose that,
by varying the ratio of activity in these two descending neurons, the brain can determine how
the forward velocity changes during the turn and therefore the fly’s overall walking trajectory.
Third, we demonstrated that a single descending neuron can have opposite effects on leg
movement during different phases of the locomotor cycle, and we identified cells in the ventral
nerve cord that are anatomically positioned to implement this phase-specific gating. Taken
together, our results show how the brain can exert detailed but also efficient control of
locomotion via selective recruitment of descending neurons.