Muscles act through elastic and dissipative elements to mediate movement, which can introduce dissipation and filtering which are important for energetics and control. The high power requirements of flapping flight can be reduced by an insect's exoskeleton, which acts as a spring with frequency-independent material properties under purely sinusoidal deformation. However, this purely sinusoidal dynamic regime does not encompass the asymmetric wing strokes of many insects or non-periodic deformations induced by external perturbations. As such, it remains unknown whether a frequency-independent model applies broadly and what implications it has for control. We used a vibration testing system to measure the mechanical properties of isolated Manduca sexta thoraces under symmetric, asymmetric and band-limited white noise deformations. The asymmetric and white noise conditions represent two types of generalized, multi-frequency deformations that may be encountered during steady-state and perturbed flight. Power savings and dissipation were indistinguishable between symmetric and asymmetric conditions, demonstrating that no additional energy is required to deform the thorax non-sinusoidally. Under white noise conditions, stiffness and damping were invariant with frequency, suggesting that the thorax has no frequency-dependent filtering properties. A simple flat frequency response function fits our measured frequency response. This work demonstrates the potential of materials with frequency-independent damping to simplify motor control by eliminating any velocity-dependent filtering that viscoelastic elements usually impose between muscle and wing.
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Some Challenges of Playing with Power: Does Complex Energy Flow Constrain Neuromuscular Performance?
Many studies of the flow of energy between the body, muscles, and elastic elements highlight advantages of the storage and recovery of elastic energy. The spring-like action of structures associated with muscles allows for movements that are less costly, more powerful and safer than would be possible with contractile elements alone. But these actions also present challenges that might not be present if the pattern of energy flow were simpler, for example, if power were always applied directly from muscle to motions of the body. Muscle is under the direct control of the nervous system, and precise modulation of activity can allow for finely controlled displacement and force. Elastic structures deform under load in a predictable way, but are not under direct control, thus both displacement and the flow of energy act at the mercy of the mechanical interaction of muscle and forces associated with movement. Studies on isolated muscle-tendon units highlight the challenges of controlling such systems. A carefully tuned activation pattern is necessary for effective cycling of energy between tendon and the environment; most activation patterns lead to futile cycling of energy between tendon and muscle. In power-amplified systems, “elastic backfire” sometimes occurs, where energy loaded into tendon acts to lengthen active muscles, rather than accelerate the body. Classic models of proprioception that rely on muscle spindle organs for sensing muscle and joint displacement illustrate how elastic structures might influence sensory feedback by decoupling joint movement from muscle fiber displacements. The significance of the complex flow of energy between muscles, elastic elements and the body for neuromotor control is worth exploring.
more » « less- Award ID(s):
- 1832795
- NSF-PAR ID:
- 10127323
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 59
- Issue:
- 6
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- p. 1619-1628
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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