Significance: Terrestrial locomotion is thought to be generated by the actions of a circuit of interconnected interneurons (central pattern generator) in the spinal cord that drive the patterned activity of pools of motor neurons, causing sequential contraction of dozens of leg muscles. Sensory feedback exerts a strong modulatory influence on this pattern; nevertheless, it remains unclear whether sensory feedback also plays a role in the generation of the normal locomotor pattern. Through the use of a combination of electrophysiology, behavior, and mouse genetics, we provide evidence that the absence of proprioceptive sensory feedback degrades locomotor pattern, indicating that proprioceptive feedback is required for the construction of locomotor pattern.

Coordinated walking in vertebrates and multi-legged invertebrates such as Drosophila melanogaster requires a complex neural network coupled to sensory feedback. An understanding of this network will benefit from systems such as Drosophila that have the ability to genetically manipulate neural activities. However, the fly's small size makes it challenging to analyze walking in this system. In order to overcome this limitation, we developed an optical method coupled with high-speed imaging that allows the tracking and quantification of gait parameters in freely walking flies with high temporal and spatial resolution. Using this method, we present a comprehensive description of many locomotion parameters, such as gait, tarsal positioning, and intersegmental and left-right coordination for wild type fruit flies. Surprisingly, we find that inactivation of sensory neurons in the fly's legs, to block proprioceptive feedback, led to deficient step precision, but interleg coordination and the ability to execute a tripod gait were unaffected.