Spatial coordination of foot contacts in unrestrained climbing insects

Abstract

Animals that live in a spatially complex environment such as the canopy of a tree, constantly need to find reliable foothold in threedimensional (3D) space. In multi-legged animals, spatial co-ordination among legs is thought to improve efficiency of finding foothold by avoiding searching-movements in trailing legs. In stick insects, a 'targeting mechanism' has been described that guides foot-placement of hind-and middle legs according to the position of their leading ipsilateral leg. So far, this mechanism has been shown for standing and tethered walking animals on horizontal surfaces. Here, we investigate the efficiency of this mechanism in spatial limb coordination of unrestrained climbing animals. For this, we recorded whole-body kinematics of freely climbing stick insects and analysed foot placement in 3D space. We found that touch-down positions of adjacent legs were highly correlated in all three spatial dimensions, revealing 3D co-ordinate transfer among legs. Furthermore, targeting precision depended on the position of the leading leg. A second objective was to test the importance of sensory information transfer between legs. For this, we ablated a proprioceptive hair field signaling the levation of the leg. After ablation, the operated leg swung higher and performed unexpected searching movements. Furthermore, targeting of the ipsilateral trailing leg was less precise in anteroposterior and dorsoventral directions. Our results reveal that the targeting mechanism is used by unrestrained climbing stick insects in 3D space and that information from the trochanteral hair field is used in ipsilateral spatial co-ordination among legs.

Motor control of an insect leg during level and incline walking

“…For example, hair plates at proximal leg joints monitor the movement ranges of insect legs (Cruse et al, 1984;Markl, 1962;Schmitz, 1986;Wendler, 1964;Wong and Pearson, 1976), and chordotonal organs monitor the current position and movement of individual leg segments (Burns, 1974;Field and Matheson, 1998;Hofmann et al, 1985;Mamiya et al, 2018;Zill, 1985). Signals from these proprioceptors are critical for the spatial coordination of the leg (Bässler, 1977;Couzin-Fuchs et al, 2015;Mendes et al, 2013;Theunissen et al, 2014). The few changes in kinematics observed in the present study, such as the magnitude of the extension angle ( Fig.…”

“…As in level walking, the hindleg closely followed the middle leg on the same side of the body, which in turn followed the front leg ( Fig. 2B; see also Cruse, 1979;Dean and Wendler, 1983;Theunissen et al, 2014). Walking speeds ranged from 23 to 85 mm s −1 (∼0.3-1.1 body lengths s −1 ; defined as the mean speed of the COM over the step cycle).…”

Comparative whole-body kinematics of closely related insect species with different body morphology

“…In a recent study, we have shown that a 'targeting mechanism' is part of the spatial coordination of legs in three-dimensional space in Carausius (Theunissen et al, 2014c). A preliminary look at the accuracy and precision of hind leg targeting towards the position of the middle leg in other species suggests that this mechanism works the same in climbing Aretaon and Medauroidea (Theunissen et al, 2014b).…”

“…Ground contact was determined based on the velocity of the tibia-tarsus joints and the distance to the surface (see also, Theunissen et al, 2014c), The velocity had to decrease below a certain threshold for at least eight consecutive frames (40 ms). The threshold was set to 25 mm s −1 for Carausius and Aretaon, and to 50 mm s −1 for Medauroidea.…”

Transfer of Spatial Contact Information Among Limbs and the Notion of Peripersonal Space in Insects

“…Regarding coordinate transformation among limbs, several studies have demonstrated this to occur in stick insects, including standing (Cruse, 1979), walking (Dean and Wendler, 1983) and climbing animals (Theunissen et al, 2014). Targeting behavior of legs has been transferred into models of motor control.…”