Joint torques in a freely walking insect reveal distinct functions of leg joints in propulsion and posture control

Abstract

Determining the mechanical output of limb joints is critical for understanding the control of complex motor behaviours such as walking. In the case of insect walking, the neural infrastructure for single-joint control is well described. However, a detailed description of the motor output in form of time-varying joint torques is lacking. Here, we determine joint torques in the stick insect to identify leg joint function in the control of body height and propulsion. Torques were determined by measuring whole-body kinematics and ground reaction forces in freely walking animals. We demonstrate that despite strong differences in morphology and posture, stick insects show a functional division of joints similar to other insect model systems. Propulsion was generated by strong depression torques about the coxatrochanter joint, not by retraction or flexion/extension torques. Torques about the respective thorax-coxa and femur-tibia joints were often directed opposite to fore-aft forces and joint movements. This suggests a posturedependent mechanism that counteracts collapse of the leg under body load and directs the resultant force vector such that strong depression torques can control both body height and propulsion. Our findings parallel propulsive mechanisms described in other walking, jumping and flying insects, and challenge current control models of insect walking.

Effects of force detecting sense organs on muscle synergies are correlated with their response properties

“…Instead, the articulation of the trochanter and femur interlocks the segments, particularly on its dorsal aspect (Schindler, 1979). These features should provide high stability, which may be essential as the body coxa joints in stick insects are highly mobile (Cruse and Bartling, 1995; Dallmann et al, 2016). This mobility permits the forces generated by legs to be directed in a number of orientations relative to the body.…”

“…This mobility permits the forces generated by legs to be directed in a number of orientations relative to the body. Recent studies, that have measured the ground reaction forces in freely moving stick insects, have shown that, unexpectedly, the largest torques generated in walking occur at the CTr joint (Dallmann et al, 2016). Extensive rotational forces also occur (pronation/supination) that could be damaging if the TrF joint were mobile.…”

“…However, it is important to note that the orientation of the ventral subgroups of receptors (~45°) could make these sensilla sensitive to forces that produce twisting (rotation about the long axis) of the femur (Higdon et al, 1967). These types of forces may occur during supination/pronation movements (Dallmann et al, 2016) although this was not directly tested due to technical constraints.…”

“…While the legs are of different body segments, the distribution, number and responses of campaniform sensilla are quite similar in middle and hind legs in both species (Hofmann and Bässler, 1982, 1986; Keller et al, 2007; Zill et al, 2009). Studies of the functions and forces generated by the legs also indicate that they serve similar functions in support and propulsion, although the hind legs are normally the major source of propulsive forces in the cockroach escape reaction (Hughes, 1952; Dallmann et al, 2016). In addition, recordings were found to be most viable in the cockroach hind legs due to their large size.…”

“…Recordings of stick insect trochanteral campaniform sensilla suggested that the motor effects of individual groups of receptors depend upon their sensitivity to forces in the plane of action of the main coxal muscles (coxo-trochanteral (CTr) joint plane) that generate forces in support and propulsion (Cruse and Bartling, 1995; Zill et al, 2012; Dallmann et al, 2016). Although many groups of campaniform sensilla have previously been characterized, the specific structure, responses and directional sensitivities of the femoral groups are poorly understood (Pringle, 1938; Schmitz et al, 1991; Akay et al, 2001).…”