Passive Joint Forces Are Tuned to Limb Use in Insects and Drive Movements without Motor Activity

Abstract

SummaryBackgroundLimb movements are generally driven by active muscular contractions working with and against passive forces arising in muscles and other structures. In relatively heavy limbs, the effects of gravity and inertia predominate, whereas in lighter limbs, passive forces intrinsic to the limb are of greater consequence. The roles of passive forces generated by muscles and tendons are well understood, but there has been little recognition that forces originating within joints themselves may also be important, and less still that these joint forces may be adapted through evolution to complement active muscle forces acting at the same joint.ResultsWe examined the roles of passive joint forces in insect legs with different arrangements of antagonist muscles. We first show that passive forces modify actively generated movements of a joint across its working range, and that they can be sufficiently strong to generate completely passive movements that are faster than active movements observed in natural behaviors. We further demonstrate that some of these forces originate within the joint itself. In legs of different species adapted to different uses (walking, jumping), these passive joint forces complement the balance of strength of the antagonist muscles acting on the joint. We show that passive joint forces are stronger where they assist the weaker of two antagonist muscles.ConclusionsIn limbs where the dictates of a key behavior produce asymmetry in muscle forces, passive joint forces can be coadapted to provide the balance needed for the effective generation of other behaviors.

A Synthetic Nervous System Controls a Simulated Cockroach

“…To determine the stiffness of every spring, we assumed that the animat could support its weight using the passive spring alone. This is consistent with the observation that insects' exoskeletons are stiff even when their muscles are cut from them [35,36]. Each leg is assumed to hold an equal amount of the weight.…”

“…In addition to the two muscles acting on each joint, there is also a passive spring with damping attached to each joint to mimic the viscoelasticity of insects' joints [35,36]. This stabilizes the motion of each joint, but makes the relationship between muscle activation and joint rotation more complicated.…”

Muscles: Non-linear Transformers of Motor Neuron Activity

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

“…In revising current models of walking control, it will thus be helpful to understand how torques are related to antagonistic muscle activity at the joints, and how torques are shaped by passive forces from muscles [11] and skeletal structures [12]. As joint torques represent the net effect of active and passive forces [1], future studies will need to combine inverse dynamics with electromyographic recordings in freely walking insects to reveal the relationship between motor input and motor output at the joints.…”