Abstract
Walking behavior is context-dependent, resulting from the integration of internal and external influences by specialized motor and pre-motor centers. Neuronal programs must be sufficiently flexible to the locomotive challenges inherent in different environments. Although insect studies have contributed substantially to the identification of the components and rules that determine locomotion, we still lack an understanding of how multi-jointed walking insects respond to changes in walking orientation and direction and strength of the gravitational force. In order to answer these questions we measured with high temporal and spatial resolution the kinematic properties of untethered Drosophila during inverted and vertical walking. In addition, we also examined the kinematic responses to increases in gravitational load. We find that animals are capable of shifting their step, spatial and inter-leg parameters in order to cope with more challenging walking conditions. For example, flies walking in an inverted orientation decreased the duration of their swing phase leading to increased contact with the substrate and, as a result, greater stability. We also find that when flies carry additional weight, thereby increasing their gravitational load, some changes in step parameters vary over time, providing evidence for adaptation. However, above a threshold that is between 1 and 2 times their body weight flies display locomotion parameters that suggest they are no longer capable of walking in a coordinated manner. Finally, we find that functional chordotonal organs are required for flies to cope with additional weight, as animals deficient in these proprioceptors display increased sensitivity to load bearing as well as other locomotive defects.
Highlights
Multi-jointed organisms move through their environment with a remarkable ability to adapt to internal physiological conditions, as well as to variations in terrain and other external forces such as wind or gravity
Animals were allowed to walk freely and the walking kinematics were quantified as previously described [39]. This method is based on the reflection of light within an optical glass through an optical effect termed Total Internal Reflection (TIR)
Leg contacts disrupt this effect causing frustrated TIR, which generates scattered light that can be detected by a high-speed camera
Summary
Multi-jointed organisms move through their environment with a remarkable ability to adapt to internal physiological conditions, as well as to variations in terrain and other external forces such as wind or gravity. A complex neuronal architecture is able to receive and integrate internal and external sensory stimuli and produce an appropriately fine-tuned motor response. Some of these responses are reflex-based, comprising simple circuits such as the giant fiber system of insects that is responsible for visually induced escape behavior [5,6,7,8]. The protocerebral bridge, a central complex neuropil in the central brain, is required for the motor output used for crossing gaps in the terrain [9,10]
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