Literature DB >> 23486171

Calcium signalling indicates bilateral power balancing in the Drosophila flight muscle during manoeuvring flight.

Fritz-Olaf Lehmann1, Dimitri A Skandalis, Ruben Berthé.   

Abstract

Manoeuvring flight in animals requires precise adjustments of mechanical power output produced by the flight musculature. In many insects such as fruit flies, power generation is most likely varied by altering stretch-activated tension, that is set by sarcoplasmic calcium levels. The muscles reside in a thoracic shell that simultaneously drives both wings during wing flapping. Using a genetically expressed muscle calcium indicator, we here demonstrate in vivo the ability of this animal to bilaterally adjust its calcium activation to the mechanical power output required to sustain aerodynamic costs during flight. Motoneuron-specific comparisons of calcium activation during lift modulation and yaw turning behaviour suggest slightly higher calcium activation for dorso-longitudinal than for dorsoventral muscle fibres, which corroborates the elevated need for muscle mechanical power during the wings' downstroke. During turning flight, calcium activation explains only up to 54 per cent of the required changes in mechanical power, suggesting substantial power transmission between both sides of the thoracic shell. The bilateral control of muscle calcium runs counter to the hypothesis that the thorax of flies acts as a single, equally proportional source for mechanical power production for both flapping wings. Collectively, power balancing highlights the precision with which insects adjust their flight motor to changing energetic requirements during aerial steering. This potentially enhances flight efficiency and is thus of interest for the development of technical vehicles that employ bioinspired strategies of power delivery to flapping wings.

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Year:  2013        PMID: 23486171      PMCID: PMC3627081          DOI: 10.1098/rsif.2012.1050

Source DB:  PubMed          Journal:  J R Soc Interface        ISSN: 1742-5662            Impact factor:   4.118


  57 in total

1.  Monitoring protein conformations and interactions by fluorescence resonance energy transfer between mutants of green fluorescent protein.

Authors:  A Miyawaki; R Y Tsien
Journal:  Methods Enzymol       Date:  2000       Impact factor: 1.600

2.  Fast x-ray recordings reveal dynamic action of contractile and regulatory proteins in stretch-activated insect flight muscle.

Authors:  Hiroyuki Iwamoto; Katsuaki Inoue; Naoto Yagi
Journal:  Biophys J       Date:  2010-07-07       Impact factor: 4.033

3.  The aerodynamic effects of wing-wing interaction in flapping insect wings.

Authors:  Fritz-Olaf Lehmann; Sanjay P Sane; Michael Dickinson
Journal:  J Exp Biol       Date:  2005-08       Impact factor: 3.312

4.  Disrupting the myosin converter-relay interface impairs Drosophila indirect flight muscle performance.

Authors:  Seemanti Ramanath; Qian Wang; Sanford I Bernstein; Douglas M Swank
Journal:  Biophys J       Date:  2011-09-07       Impact factor: 4.033

5.  A theory of tension fluctuations due to muscle cross-bridges.

Authors:  N Thomas; R A Thornhill
Journal:  Proc Biol Sci       Date:  1995-03-22       Impact factor: 5.349

6.  The supply of oxygen to the flight muscles of insects: a theory of tracheole physiology.

Authors:  V B Wigglesworth; W M Lee
Journal:  Tissue Cell       Date:  1982       Impact factor: 2.466

7.  Paramyosin phosphorylation site disruption affects indirect flight muscle stiffness and power generation in Drosophila melanogaster.

Authors:  Hongjun Liu; Mark S Miller; Douglas M Swank; William A Kronert; David W Maughan; Sanford I Bernstein
Journal:  Proc Natl Acad Sci U S A       Date:  2005-07-14       Impact factor: 11.205

8.  The correlation between wing kinematics and steering muscle activity in the blowfly Calliphora vicina.

Authors:  C N Balint; M H Dickinson
Journal:  J Exp Biol       Date:  2001-12       Impact factor: 3.312

9.  The supply of oxygen to the active flight muscles of some large beetles.

Authors:  P L Miller
Journal:  J Exp Biol       Date:  1966-10       Impact factor: 3.312

10.  [Optomoter studies of the visual system of several eye mutants of the fruit fly Drosophila].

Authors:  K G Götz
Journal:  Kybernetik       Date:  1964-06
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  11 in total

1.  Flexibility and control of thorax deformation during hawkmoth flight.

Authors:  Noriyasu Ando; Ryohei Kanzaki
Journal:  Biol Lett       Date:  2016-01       Impact factor: 3.703

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

Authors:  Chris J Dallmann; Volker Dürr; Josef Schmitz
Journal:  Proc Biol Sci       Date:  2016-01-27       Impact factor: 5.349

3.  Flight and seizure motor patterns in Drosophila mutants: simultaneous acoustic and electrophysiological recordings of wing beats and flight muscle activity.

Authors:  Atulya Iyengar; Chun-Fang Wu
Journal:  J Neurogenet       Date:  2014 Sep-Dec       Impact factor: 1.250

4.  Distinctions among electroconvulsion- and proconvulsant-induced seizure discharges and native motor patterns during flight and grooming: quantitative spike pattern analysis in Drosophila flight muscles.

Authors:  Jisue Lee; Atulya Iyengar; Chun-Fang Wu
Journal:  J Neurogenet       Date:  2019-04-13       Impact factor: 1.250

Review 5.  The aerodynamics and control of free flight manoeuvres in Drosophila.

Authors:  Michael H Dickinson; Florian T Muijres
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2016-09-26       Impact factor: 6.237

6.  Preference and detrimental effects of high fat, sugar, and salt diet in wild-caught Drosophila simulans are reversed by flight exercise.

Authors:  Alexander K Murashov; Elena S Pak; Chien-Te Lin; Ilya N Boykov; Katherine A Buddo; Jordan Mar; Krishna M Bhat; Peter Darrell Neufer
Journal:  FASEB Bioadv       Date:  2020-12-04

7.  Wings and halteres act as coupled dual oscillators in flies.

Authors:  Tanvi Deora; Siddharth S Sane; Sanjay P Sane
Journal:  Elife       Date:  2021-11-16       Impact factor: 8.140

8.  In vivo time-resolved microtomography reveals the mechanics of the blowfly flight motor.

Authors:  Simon M Walker; Daniel A Schwyn; Rajmund Mokso; Martina Wicklein; Tonya Müller; Michael Doube; Marco Stampanoni; Holger G Krapp; Graham K Taylor
Journal:  PLoS Biol       Date:  2014-03-25       Impact factor: 8.029

9.  Mutations of the Drosophila myosin regulatory light chain affect courtship song and reduce reproductive success.

Authors:  Samya Chakravorty; Hien Vu; Veronica Foelber; Jim O Vigoreaux
Journal:  PLoS One       Date:  2014-02-26       Impact factor: 3.240

Review 10.  Neural control and precision of flight muscle activation in Drosophila.

Authors:  Fritz-Olaf Lehmann; Jan Bartussek
Journal:  J Comp Physiol A Neuroethol Sens Neural Behav Physiol       Date:  2016-12-09       Impact factor: 1.836

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