The manifold structure of limb coordination in walking Drosophila

Abstract

Terrestrial locomotion requires animals to coordinate their limb movements to efficiently traverse their environment. While previous studies in hexapods have reported that limb coordination patterns can vary substantially, the structure of this variability is not yet well understood. Here, we characterized the symmetric and asymmetric components of variation in walking kinematics in the genetic model organism Drosophila. We found that Drosophila use a single continuum of coordination patterns without evidence for preferred configurations. Spontaneous symmetric variability was associated with modulation of a single control parameter—stance duration—while asymmetric variability consisted of small, limb-specific modulations along multiple dimensions of the underlying symmetric pattern. Commands that modulated walking speed, originating from artificial neural activation or from the visual system, evoked modulations consistent with spontaneous behavior. Our findings suggest that Drosophila employ a low-dimensional control architecture, which provides a framework for understanding the neural circuits that regulate hexapod legged locomotion.

Decentralized Control of Insect Walking – a simple neural network explains a wide range of behavioral and neurophysiological results

“…Eventually, mirror image patterns are possible with phase coupling among contralateral legs deviating from phase values of 0.5. Patterns recently described as non-canonical by DeAngelis et al (2019) can be observed, too (e.g. Fig 3C).…”

“…As has been shown neuroWalknet is able to produce footfall patterns that include "tripod" patterns, "tetrapod" patterns, "pentapod" patterns as well as various stable intermediate patterns. These patterns form a continuous multitude as has been observed in stick insects (Graham 1972) and in Drosophila (Wosnitza et al 2013;DeAngelis et al 2019) and to some extent in cockroaches (e.g. Hughes 1952;Bender et al 2011).…”

“…This suggests that there is a continuum of intermediate stable stepping patterns observed in probably all insects, at least in cockroaches and in stick insects, both representing the group of hemimetabolic insects, as well as in Drosophila (Wosnitza et al 2013), representing a holometabolic insect. Recently, this view has been strongly supported by an excellent study of DeAngelis et al (2019).…”

Two brain pathways initiate distinct forward walking programs inDrosophila

“…Critically, high resolution analyses of walking gait in freely walking flies revealed that BPN-TeTx flies were not uncoordinated ( Figure S7) but instead walked slowly as a result of an increased step period, specifically due to an increased stance duration ( Figure 7E). Previous work has shown that flies typically vary walking speed by varying stance duration (DeAngelis et al, 2019;Wosnitza et al, 2013). Therefore, the gait of BPN silenced flies resembles that of slow walking flies.…”

A size principle for leg motor control inDrosophila

“…Here, we use in vivo calcium imaging, whole-cell patch clamp electrophysiology, and optogenetics during walking behavior to investigate motor control of the Drosophila tibia (Figure 1A). The femur-tibia joint of a walking fly flexes and extends 10-20 times per second, reaching swing speeds of several thousand degrees per second (DeAngelis et al, 2019;Gowda et al, 2018;Mendes et al, 2013;Strauss and Heisenberg, 1990;Wosnitza et al, 2013). Flies also use their legs to target other body parts during grooming (Hampel et al, 2015;Seeds et al, 2014).…”