From sarcomeres to organisms: the role of muscle-tendon architecture in determining locomotor performance

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1 From sarcomeres to organisms: the role of muscle-tendon architecture in determining locomotor performance Manny Azizi Dept. of Ecology and Evolutionary Biology University of California, Irvine

2 integrative approach A. Northcut Mechanics Physiology Morphology

3 musculoskeletal organization Movement A. Northcut Sarcomere Graham Johnson Medical Media

4 force-length

5 force-velocity 100 Relative Force (% max) Relative Velocity (% max)

6 musculoskeletal organization Movement A. Northcut Fiber Architecture Tendon Elasticity Skeletal Levers Sarcomere Graham Johnson Medical Media

7 talk outline Effect of fiber architecture on muscle performance Optimal force production during frog jumping

8 fiber architecture Parallel Pinnate Long Fibers Short Fibers Large displacements Specialized for velocity More fibers Specialized for force

9 fiber architecture Relaxed Contracted Fiber = 1 cm Shortening α = 30 β = cm β α 3 cm 4 cm Muscle Shortening Gear Ratio Force Ratio = 1.3 cm = 1.3/1= 1.3 = cos θ= 0.77

10 muscle shape changes Bulging Masseter

11 muscle shape changes Thickness increases Lateral Thickness decreases Lateral Top Top

12 muscle shape changes Thickness increases Lateral Thickness decreases Lateral Top Top

13 muscle shape changes Thickness increases Lateral Thickness decreases Lateral Top Top

14 muscle shape changes Thickness increases Thickness decreases Δ Fiber =13% Δ Fiber =13% Δθ = 20 Δθ = 0 Gear ratio= 2 Gear ratio= 1 Dorsal Dorsal Do muscle shape changes favor force or velocity?

15 in situ preparation Stimulus Sonomicrometry Fiber Velocity Pinnation Angle Muscle Thickness Ergometer Muscle Force Muscle Velocity

16 results n=5 p < Azizi et al. Proc. Nat. Acad. Sciences, 2008

17 results n=5 p < Azizi et al. Proc. Nat. Acad. Sciences, 2008

18 results n=5 p < Azizi et al. Proc. Nat. Acad. Sciences, 2008

19 results favors V favors F Similar to an automatic transmission system, gear ratio in pinnate muscles is self-regulated to better match the mechanical demands of a contraction

20 force-velocity Fiber Force (P/Po) Shortening Velocity (V/Vmax)

21 force-velocity Fiber Muscle (fixed gear =1.2) Force (P/Po) Shortening Velocity (V/Vmax)

22 force-velocity Fiber Muscle (variable gear) Force (P/Po) Shortening Velocity (V/Vmax)

23 in vivo function Image from Roberts et al. 1997

24 in vivo function swing stance 60 Force (N) Length (mm) Time (s)

25 Conclusion Muscle shape changes can act as an automatic transmission system to allow a single muscle to function effectively across a range of mechanical actions Mechanics Physiology Morphology

26 talk outline Effect of fiber architecture on muscle performance Optimal force production during frog jumping

27 anuran jumping Roberts, Azizi and Abbott, Phil. Trans. Royal Society, 2011

28 anuran jumping Roberts, Azizi and Abbott, Phil. Trans. Royal Society, 2011

29 anuran jumping d d muscle work muscle work= muscle force shortening

30 hypothesis Significant muscle shortening will reduce force production due to muscle s force-length properties

31 methods: in vivo Sonomicrometry Electromyography in plantaris muscle High-speed video (500 fps)

32 methods: in vitro Isolated muscle prep sonomicrometry (fiber length) Ergometer (muscle force)

33 sample jump 10.0 Takeoff 9.5 Fiber length (mm) EMG (V) Time (s)

34 force-length data Relative force (P/Po) Relative fiber length (L/Lo) Azizi and Roberts Proc. of the Royal Society, 2010

35 in vivo operating lengths Relative force (P/Po) Relative fiber length (L/Lo)

36 in vivo operating lengths

37 in vivo operating lengths

38 optimal force production Relative Force (P/Po) Time (s) Relative Force (P/Po) Relative Length (L/Lo)

39 optimal force production Relative Force (P/Po) Time (s) Relative Force (P/Po) Relative Length (L/Lo)

40 in vivo operating lengths

41 passive force Relative force (P/Po) Relative fiber length (L/Lo)

42 passive force Relative force (P/Po) Mammals Anurans Relative length (L/L o ) Azizi and Roberts Proc. of the Royal Society, 2010

43 Conclusion Lower passive stiffness enhances muscle force production during a behavior that requires significant muscle shortening Mechanics Physiology Morphology

44 significance Studies at intermediate levels of organization can help bridge the gap in our understanding of muscle powered movements An integrative approach can reveal novel features of the musculoskeletal system, which allow organisms to circumvent the constraints of the sarcomere

45 acknowledgements Collaborators Gary Gillis Tobias Landberg Nicolai Konow Greg Sawicki Mason Dean Andie Ward Adam Summers Emily Abbott Matt McHenry Gavin Crynes Greg Halenda Jaquan Horton Beth Brainerd Tom Roberts Funding

46 current focus Is this difference related to phylogeny or function? Relative force (P/Po) Mammals Anurans Relative length (L/Lo)

47 current focus 1.0 Is this difference related to phylogeny or function? Relative force (P/Po) Mammals 0.8 Anurans Relative length (L/Lo) 1.6

48 current focus What are the structural determinant of stiffness variation in muscles? Relative force (P/Po) Mammals Anurans Relative length (L/Lo) titin ECM collagen Z-disk Actin M-line Ig domain Myosin PEVK Extensible region Actin

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