A single muscle's multifunctional control potential of body dynamics for postural control and running

Abstract

A neuromechanical approach to control requires understanding how mechanics alters the potential of neural feedback to control body dynamics. Here, we rewrite activation of individual motor units of a behaving animal to mimic the effects of neural feedback without concomitant changes in other muscles. We target a putative control muscle in the cockroach, Blaberus discoidalis (L.), and simultaneously capture limb and body dynamics through high-speed videography and a microaccelerometer backpack. We test four neuromechanical control hypotheses. We supported the hypothesis that mechanics linearly translates neural feedback into accelerations and rotations during static postural control. However, during running, the same neural feedback produced a nonlinear acceleration control potential restricted to the vertical plane. Using this, we reject the hypothesis from previous work that this muscle acts primarily to absorb energy from the body. The conversion of the control potential is paralleled by nonlinear changes in limb kinematics, supporting the hypothesis that significant mechanical feedback filters the graded neural feedback for running control. Finally, we insert the same neural feedback signal but at different phases in the dynamics. In this context, mechanical feedback enables turning by changing the timing and direction of the accelerations produced by the graded neural feedback.

Proprioceptive feedback reinforces centrally generated stepping patterns in the cockroach

“…When speed increases, not only does the type of sensory information available during each stride change (Duysens et al, 2000;Zill et al, 2009), but the translation of neural commands into mechanical actions is also affected (Sponberg et al, 2011). The present study and other recent papers indicate that the mechanics of a given task can shape the neural signals delivered to control movement (Dickinson et al, 2000;Holmes et al, 2006;Pearson et al, 2006;Cowan and Fortune, 2007;Pfeifer et al, 2007;Chiel et al, 2009;Tytell et al, 2011).…”

“…The question of whether inputs are integrated similarly at both high and low speeds is a central challenge in research of the motor control of locomotion (Koditschek et al, 2004;Holmes et al, 2006;Sponberg et al, 2011). When speed increases, not only does the type of sensory information available during each stride change (Duysens et al, 2000;Zill et al, 2009), but the translation of neural commands into mechanical actions is also affected (Sponberg et al, 2011).…”

“…Their body and limb mechanics provide stability during rapid running over rough terrain and in the face of impulsive perturbations, without requiring precise changes in motor patterns (Jindrich and Full, 2002;Sponberg and Full, 2008). In the presence of larger perturbations, however, neural feedback modifies the centrally produced patterns to adjust limb movement (Sponberg and Full, 2008;Sponberg et al, 2011). This suggests a combined feedforward-feedback control strategy, in which feedforward pathways from centrally connected central pattern generators (CPGs), in conjunction with nonlinear properties of muscles, suffice to produce basic locomotion (Jindrich and Full, 2002;Holmes et al, 2006;Kukillaya and Holmes, 2007;Kukillaya et al, 2009), whereas proprioception enhances flexibility in response to unexpected perturbations (Sponberg and Full, 2008;.…”

Neuromuscular control of free-flight yaw turns in the hawkmothManduca sexta

“…An investigation, conducted while the moth is engaged in stationary hovering, where the natural activation of the DVM is overwritten with an artificial signal (e.g. Sponberg et al, 2011) would permit correlation of within-wingbeat body and wing kinematics with muscle activation phase. By stimulating only the indirect flight muscles, we may be able to isolate their effects from those of the typically co-activated direct flight muscles.…”

Abdicating power for control: a precision timing strategy to modulate function of flight power muscles

“…However, because these effects operate indirectly, and small strain changes acting at the wing hinge can translate to a variety of wing kinematic changes, it is still important to establish a causal role of left-right timing modulation in producing turning torque. To do this, we use the approach developed in Sponberg et al [9] of altering the timing of individual muscle potentials in the power muscles alone without concomitant changes in other muscles. We thereby isolate one of the animal's 'control knobs', namely left-right timing differences, and explore its role in torque production.…”