skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: In vivo x-ray diffraction and simultaneous EMG reveal the time course of myofilament lattice dilation and filament stretch

Journal Article · · Journal of Experimental Biology
DOI:https://doi.org/10.1242/jeb.224188· OSTI ID:1643143

Muscle's function within an organism depends on the feedback between molecular to meter-scale processes. While the motions of muscle's contractile machinery are well described in isolated preparations, only a handful of experiments have documented the kinematics of the lattice occurring when multi-scale interactions are fully intact. We used time-resolved x-ray diffraction to record the kinematics of the myofilament lattice within a normal operating context: the tethered flight of Manduca sexta. Since the primary flight muscles of Manduca sexta are synchronous, we used these results to reveal the timing of in vivo cross-bridge recruitment, which occurred 24 (s.d. 26) ms following activation. In addition, the thick filaments stretched an average of 0.75 (s.d. 0.32)% and thin filaments stretched 1.11 (s.d. 0.65)%. In contrast to other in vivo preparations, lattice spacing changed an average of 2.72 (s.d. 1.47)%. Lattice dilation of this magnitude significantly impacts shortening velocity and force generation, and filament stretching tunes force generation. While kinematics were consistent within individual trials, there was extensive variation between trials. Using a mechanism-free machine learning model we searched for patterns within and across trials. While lattice kinematics were predictable within trials, the model could not create predictions across trials. This indicates that the variability we see across trials may be explained by latent variables occurring in this naturally functioning system. The diverse kinematic combinations we documented mirror muscle's adaptability and may facilitate its robust function in unpredictable conditions.

Sponsoring Organization:
USDOE
Grant/Contract Number:
AC02-06CH11357
OSTI ID:
1643143
Journal Information:
Journal of Experimental Biology, Journal Name: Journal of Experimental Biology; ISSN 0022-0949
Publisher:
The Company of BiologistsCopyright Statement
Country of Publication:
United Kingdom
Language:
English

References (45)

Elastic Energy Storage and Radial Forces in the Myofilament Lattice Depend on Sarcomere Length journal November 2012
The Life of Behavior journal October 2019
Titin-based modulation of active tension and interfilament lattice spacing in skinned rat cardiac muscle journal November 2004
Shortening velocity in skinned single muscle fibers. Influence of filament lattice spacing journal July 1987
Compliant Realignment of Binding Sites in Muscle: Transient Behavior and Mechanical Tuning journal April 1998
The Cross-Bridge Spring: Can Cool Muscles Store Elastic Energy? journal April 2013
The Filament Lattice of Striated Muscle journal April 1998
Insight into the actin-myosin motor from x-ray diffraction on muscle journal January 2009
Geometrical factors influencing muscle force development. II. Radial forces journal April 1980
Lattice spacing changes accompanying isometric tension development in intact single muscle fibers journal November 1994
An Analysis of Pre-Flight Warm-Up in the Sphinx Moth, Manduca Sexta journal August 1971
How Animals Move: An Integrative View journal April 2000
Structure of myosin filaments from relaxed Lethocerus flight muscle by cryo-EM at 6 Å resolution journal September 2016
Ablation of Myosin-Binding Protein-C Accelerates Force Development in Mouse Myocardium journal June 2006
Cardiac-like behavior of an insect flight muscle journal June 2004
Elastic proteins in the flight muscle of Manduca sexta journal February 2015
Molecular dynamics of cyclically contracting insect flight muscle in vivo journal January 2005
How to Build Fast Muscles: Synchronous and Asynchronous Designs journal August 2002
Evidence for structurally different attached states of myosin cross-bridges on actin during contraction of fish muscle journal August 1992
X-ray diffraction evidence for myosin-troponin connections and tropomyosin movement during stretch activation of insect flight muscle journal December 2010
Temperature gradients drive mechanical energy gradients in the flight muscle of Manduca sexta journal January 2012
Thick-Filament Strain and Interfilament Spacing in Passive Muscle: Effect of Titin-Based Passive Tension journal March 2011
Interference fine structure and sarcomere length dependence of the axial x-ray pattern from active single muscle fibers journal June 2000
XGBoost: A Scalable Tree Boosting System conference January 2016
The Molecular Trigger for High-Speed Wing Beats in a Bee journal August 2013
A new look at thin filament regulation in vertebrate skeletal muscle journal July 1998
The BioCAT undulator beamline 18ID: a facility for biological non-crystalline diffraction and X-ray absorption spectroscopy at the Advanced Photon Source journal August 2004
Regulation of Contraction in Striated Muscle journal January 2000
Motion of myosin head domains during activation and force development in skeletal muscle journal April 2011
X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction journal December 1994
A Spatially Explicit Model Shows How Titin Stiffness Modulates Muscle Mechanics and Energetics journal June 2018
Elasticity and unfolding of single molecules of the giant muscle protein titin journal May 1997
X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle journal December 1994
Thick Filament Mechano-Sensing in Skeletal and Cardiac Muscles: A Common Mechanism Able to Adapt the Energetic Cost of the Contraction to the Task journal June 2018
In vivo x-ray diffraction and simultaneous EMG reveal the timecourse of myofilament lattice dilation and filament stretch dataset January 2020
Architecture and function in the muscle sarcomere journal April 1997
In Vivo X-Ray Diffraction of Indirect Flight Muscle from Drosophila melanogaster journal May 2000
Axial and Radial Forces of Cross-Bridges Depend on Lattice Spacing journal December 2010
Frank-Starling Relationship: Long on Importance, Short on Mechanism journal January 2002
The length–tension curve in muscle depends on lattice spacing journal September 2013
Structural changes in the myosin filament and cross-bridges during active force development in single intact frog muscle fibres: stiffness and X-ray diffraction measurements: Myosin filament structure and force development journal December 2006
The molecular elasticity of the insect flight muscle proteins projectin and kettin journal March 2006
Electrostatic forces or structural scaffolding: What stabilizes the lattice spacing of relaxed skinned muscle fibers? journal August 2014
Cytoskeleton: Titin as a scaffold and spring journal March 1996
Thick-Filament Extensibility in Intact Skeletal Muscle journal October 2018