Muscle-specific economy of force generation and efficiency of work production during human running

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    Evaluation Summary:

    This paper is of interest to scientists within the field of motor control and biomechanics studying human locomotion. The work provides evidence for the optimization of muscle function during locomotion depending on the specific biomechanical constraints. The overall methodology is sound and data are properly analyzed, although the in vivo measurements required a complex experimental setup together with sophisticated modeling which on the one hand conclusively support the key claims of the paper for the experiment within this paper, on the other hand weakens the generalizability of the results.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)

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Abstract

Human running features a spring-like interaction of body and ground, enabled by elastic tendons that store mechanical energy and facilitate muscle operating conditions to minimize the metabolic cost. By experimentally assessing the operating conditions of two important muscles for running, the soleus and vastus lateralis, we investigated physiological mechanisms of muscle work production and muscle force generation. We found that the soleus continuously shortened throughout the stance phase, operating as work generator under conditions that are considered optimal for work production: high force-length potential and high enthalpy efficiency. The vastus lateralis promoted tendon energy storage and contracted nearly isometrically close to optimal length, resulting in a high force-length-velocity potential beneficial for economical force generation. The favorable operating conditions of both muscles were a result of an effective length and velocity-decoupling of fascicles and muscle-tendon unit, mostly due to tendon compliance and, in the soleus, marginally by fascicle rotation.

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  1. Joint Public Review:

    Bohm et al. investigated the operating conditions of the soleus and the vastus lateralis muscle during running. They report different roles for the two muscles. The soleus acts as an energy generator characterized by a high force-length potential and enthalpy efficiency whereas the vastus lateralis acts as an energy conservator, characterized by a high force-length and force-velocity potential. The authors show how the decoupling of the muscle-tendon-unit length and the fascicle length, mainly attributable to tendon compliance, allows both muscles to work at a high, almost optimal , force-length potential. Beside this similarity the soleus shortens throughout stance phase (concentric mode) whereas the vastus lateralis shows almost no length changes (isometric mode) and is activated primarily in the first part of the stance phase. These observations in combination with the calculated enthalpy efficiency for soleus and the estimated force-velocity potential for vastus lateralis clarify the role of the two muscles in the optimization of muscle energy production and force generation during the experimental condition. The authors use a complex methodology and calculate the variables of interest in the most sophisticated way. The results of the present study contribute in a comprehensive way to the ongoing discussion on muscle and tendon interaction during human locomotion. The conclusions of this paper are mostly well supported by measured and modeled data, but some aspects of the experimental setup and data modeling need clarification and a more thorough discussion.

  2. Evaluation Summary:

    This paper is of interest to scientists within the field of motor control and biomechanics studying human locomotion. The work provides evidence for the optimization of muscle function during locomotion depending on the specific biomechanical constraints. The overall methodology is sound and data are properly analyzed, although the in vivo measurements required a complex experimental setup together with sophisticated modeling which on the one hand conclusively support the key claims of the paper for the experiment within this paper, on the other hand weakens the generalizability of the results.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)