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.
Previous work has characterized how walking Drosophila coordinate the movements of individual limbs (DeAngelis et al., 2019). To understand the circuit basis of this coordination, one must characterize how sensory feedback from each limb affects walking behavior. However, it has remained difficult to manipulate neural activity in individual limbs of freely moving animals. Here, we demonstrate a simple method for optogenetic stimulation with body side-, body segment-, and limb-specificity that does not require real-time tracking. Instead, we activate at random, precise locations in time and space and use post hoc analysis to determine behavioral responses to specific activations. Using this method, we have characterized limb coordination and walking behavior in response to transient activation of mechanosensitive bristle neurons and sweet-sensing chemoreceptor neurons. Our findings reveal that activating these neurons has opposite effects on turning, and that activations in different limbs and body regions produce distinct behaviors.
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