In Vivo Time-Resolved Microtomography Reveals the Mechanics of the Blowfly Flight Motor

Walker, Simon; Schwyn, Daniel A.; Mokso, Rajmund; Wicklein, Martina; Müller, Tonya; Doube, Michael; Stampanoni, Marco; Krapp, Holger G.; Taylor, Graham K.

doi:10.1371/journal.pbio.1001823

Cited by 143 publications

(136 citation statements)

References 41 publications

(69 reference statements)

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“…Froghoppers power their jumps with torques about the CTr joint and steer by controlling jump azimuth with the FTi joint [33]. In a similar vein, large indirect flight power muscles of most insects provide the mechanical energy required for flapping the wings, while smaller steering muscles determine its transformation into lift and drag by adjusting the stroke plane and the wing's angle of attack [34,35]. Our findings provide the prospect that such a control strategy is also common in walking insects with distinctly different leg posture and kinematics.…”

Section: Discussionmentioning

confidence: 99%

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

2016

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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.

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Section: Discussionmentioning

confidence: 99%

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

2016

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“…This suggests that high-amplitude wing motion is not achieved by the pulling of Ax1 because of contraction of I1 at the end of upstroke. Rather, I1 contraction acts to restrict amplitude at the end of downstroke (Walker et al, 2014); these results explain why I1 is active when stroke amplitude decreases (Heide, 1975 , the troponin complex goes through a conformational shift inducing tropomyosin to release the block on the active site. Myosin heads then bind to these active sites and induce actinmyosin filaments to slide over one another, causing muscle contraction.…”

Section: Axillary Sclerite 1 and Associated Musclesmentioning

confidence: 98%

“…The base of the I1 muscle is attached to the anepisternal ridge, whereas I2 is more internal and sits on the pleural apophysis (for apophysis, see Glossary) (Figs 5B, 6A, Movie 2). A recent X-ray tomography study (Walker et al, 2014) showed that the tendon connecting the I1 muscle to Ax1 is in a buckled state at the onset of downstroke, when the wing is above the wing hinge. It transitions from a buckled to a taut state as it approaches the end of the downstroke.…”

Section: Axillary Sclerite 1 and Associated Musclesmentioning

confidence: 99%

“…The synchrotron-coupled X-ray imaging of live flapping flies has been used to visualize the small motion of these tiny structures during active wing motion. In addition to the motion of internal sclerites, these techniques also allow visualization of the direct steering muscles during flight (Walker et al, 2014). In parallel, recent breakthroughs in Drosophila genetics also show great promise in revealing the role of specific direct steering muscles both individually and in combination with other muscles in different behaviors (Shirangi et al, 2013;Lindsay et al, 2017).…”

Section: The Wing Hinge Translates Muscle Contraction Into Wing Motionmentioning

confidence: 99%

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Mechanics of the thorax in flies

Deora

Gundiah

Sane

2017

Journal of Experimental Biology

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Insects represent more than 60% of all multicellular life forms, and are easily among the most diverse and abundant organisms on earth. They evolved functional wings and the ability to fly, which enabled them to occupy diverse niches. Insects of the hyper-diverse orders show extreme miniaturization of their body size. The reduced body size, however, imposes steep constraints on flight ability, as their wings must flap faster to generate sufficient forces to stay aloft. Here, we discuss the various physiological and biomechanical adaptations of the thorax in flies which enabled them to overcome the myriad constraints of small body size, while ensuring very precise control of their wing motion. One such adaptation is the evolution of specialized myogenic or asynchronous muscles that power the high-frequency wing motion, in combination with neurogenic or synchronous steering muscles that control higher-order wing kinematic patterns. Additionally, passive cuticular linkages within the thorax coordinate fast and yet precise bilateral wing movement, in combination with an actively controlled clutch and gear system that enables flexible flight patterns. Thus, the study of thoracic biomechanics, along with the underlying sensory-motor processing, is central in understanding how the insect body form is adapted for flight.

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“…Their size allows for micro-sensor access to the inner organs, such as the heart, accessory pulsatile organs and tracheal system, in contrast to the preferred fly model organism, Drosophila. In Calliphoridae, the structural basis and mechanics of the flight apparatus, its control and energetics have been investigated in detail (Miyan and Ewing, 1985;Nachtigall, 1985;Ennos, 1987;Wisser, 1988;Nalbach, 1989;Dickinson and Tu, 1997;Walker et al, 2014). There is a disproportion of thorough research on the flight mechanism in flies in contrast to the aspect of gas exchange during flight.…”

Section: Introductionmentioning

confidence: 99%

Flight-motor-driven respiratory airflow increases tracheal oxygen to nearly atmospheric level in blowflies (Calliphora vicina)

Wasserthal

2015

Journal of Experimental Biology

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It is widely accepted that an efficient oxygen supply and removal of CO 2 in small flying insects are sufficiently performed by diffusion with open spiracles. This paper shows that in the tethered flying blowfly, gas exchange occurs by autoventilation and unidirectional airflow. The air is inspired through the mesothoracic spiracles (Sp1) during the downstroke of the wings and is expired through the metathoracic spiracles (Sp2) during the upstroke. This directed airflow through the thoracic tracheal system was documented by pre-atrial pressure measurements at the Sp1 and Sp2, revealing a sub-atmospheric mean pressure at the Sp1 and an over-atmospheric mean pressure at the Sp2. In the mesothoracic air sacs, the mean pressure is subatmospheric, conditioned by the only slightly open spiracles. In a split flow-through chamber experiment, the CO 2 released through the Sp2 confirmed this unidirectional respiratory gas flow, implicating an inner tracheal valve. In the thoracic tracheal system, the P O2 during flight exceeds the high resting P O2 by 1-2 kPa, reaching nearly atmospheric values. In the abdominal large air sacs, the P O2 drops during flight, probably due to the accumulation of CO 2 . Periodic heartbeat reversals continue during flight, with a higher period frequency than at rest, supporting the transport of CO 2 via the haemolymph towards the metathoracic tracheae and abdominal air sacs.

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In Vivo Time-Resolved Microtomography Reveals the Mechanics of the Blowfly Flight Motor

Abstract: Time-resolved X-ray microtomography permits a real-time view of the blowfly in flight at a previously unprecedented level of detail, revealing how the tiny steering muscles work.

Cited by 143 publications

References 41 publications

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

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

Mechanics of the thorax in flies

Flight-motor-driven respiratory airflow increases tracheal oxygen to nearly atmospheric level in blowflies (Calliphora vicina)

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