Load compensation in targeted limb movements of an insect

Abstract

SUMMARYThe task of a multi-jointed limb making an aimed movement towards a target requires that the movement is regulated against external perturbations such as changing load. In particular, loading one part of a limb leads to altered static forces on all proximal segments, and to additional dynamic joint interaction forces when the limb moves. We have addressed the question of load compensation in an insect preparation in which a locust makes aimed scratching movements with a hind leg in response to tactile stimulation of a wing.We show that loading the femur or tibia with the equivalent of 8.5 times the mass of the tibia (corresponding to an increase of up to 11.6 times the rotational moment of inertia at the femur–tibia joint) does not impair the animal's ability to make well-coordinated, aimed movements of that leg towards different targets. The kinematics of the movements are the same, and animals aim the same part of their distal tibia at the target, regardless of loading. The movements are carried out with equal accuracy and at the same initial velocity under all load conditions. Because loading of the leg does not change the behavioural performance, there is no indication of a change in aiming strategy. This implies high leg joint stiffness and/or the existence of high gain proprioceptive control loops. We have previously shown that in the unloaded condition, movements elicited by stimuli to different places on the wing are driven by a single underlying movement pattern that shifts depending on stimulus location along the wing surface. Our present data show that leg proprioceptive inputs are also integrated into the leg motor networks,rendering hind limb targeting robust against large changes in moment of inertia.

Co-Contraction and Passive Forces Facilitate Load Compensation of Aimed Limb Movements

“…By modeling this transformation for aimed scratching movements in the locust (Berkowitz and Laurent, 1996;Dürr and Matheson, 2003;Matheson and Dürr, 2003), we show that the dynamic range of joint torques is increased by co-contraction. Passive properties of the musculoskeletal system cause large joint stiffness in this invertebrate model system.…”

Functional Recovery of Aimed Scratching Movements after a Graded Proprioceptive Manipulation

“…After shortening of the apodeme, locusts responded to touches on the wing with scratching movements that resembled qualitatively those made by intact animals and described in detail previously (Dürr and Matheson, 2003). We refer to movements made in response to touches at the anterior stimulus site (Fig.…”

“…Experiments were performed on 15 female locusts (Schistocerca gregaria; Forskål) taken from a crowded colony at the Department of Zoology, University of Cambridge (Cambridge, UK). Locusts were tethered in an experimental setup in the same way as described by Matheson and Dürr (2003). Tactile stimuli were applied to the posterior and anterior forewing randomly until at least 10 scratches were recorded for each of the stimulus sites.…”

“…Bayes' theorem (Quinn and Keough, 2002) was then applied to determine which of the experimental conditions had most likely given rise to a movement in which the leg moved across a given point during a single video frame. By assuming a binomial distribution of n independent observations and knowing the calculated error probability (formulae given by Dürr and Matheson, 2003), a critical number of observations was calculated that was necessary to allow no more than n/2 Ϫ 1 wrong decisions in 95% of cases. If this critical value (in frames) was smaller than the average number of video frames in the total set of measured trajectories under consideration, the two distributions were considered statistically different.…”

“…The similarity between pairs of these distributions is presented as a percentage overlap and as a critical value that is the number of video frames that would need to be observed to distinguish between them at a 95% confidence level (see Materials and Methods). When this critical value is smaller than the mean number of frames in the dataset of scratches being compared, we consider the distributions significantly different (Dürr and Matheson, 2003). Even for distributions that did not differ significantly on this criterion, both the percentage overlap and the critical values provide a measure of relative similarity, with larger values indicating more similar distributions.…”