The mysteries of eccentric muscle action

Muscle actions are typically divided into 3 categories: concentric, isometric, and eccentric. An active muscle that is shortening and produces positive mechanical work is said to work concentrically; an active muscle that is not changing its length, and thus does not produce net work, is said to work isometrically; and an active muscle that is elongated by external forces, and thus absorbs work, or produces negative work, is said to work eccentrically.¹

Concentric and isometric muscle actions are well studied and well understood, and they fit well into the way we think about muscle contraction on the molecular level: the sliding filament2, 3 and the cross-bridge theory.⁴ In contrast, eccentric muscle actions are not nearly as much studied as concentric and isometric actions, and they do not fit well into the cross-bridge theory thinking (e.g., Herzog⁵). Muscles working eccentrically can produce much greater forces than muscles working concentrically or isometrically,6, 7 they remain stronger following the eccentric action (residual force enhancement, e.g., Edman et al.,⁸ Herzog and Leonard⁹), they require less energy per unit of force,¹⁰ and eccentric muscle actions are occurring in everyday life all the time.¹¹ Eccentric muscle actions have also been associated with increased risks for muscle injury (e.g., Brooks et al.,¹² Armstrong et al.¹³), instability of force production and sarcomere lengths (e.g., Morgan¹⁴), and inhibition of voluntary activation (e.g., Westing et al.¹⁵). However, eccentric muscle actions remain understudied, and many of the phenomena associated with eccentric actions have eluded satisfactory explanation. Eccentric muscle actions, the properties associated with them, and the underlying mechanistic explanations remain poorly understood.

In this special issue of the Journal of Sport and Health Science (JSHS), experts in the field have tackled some of the mysteries surrounding eccentric muscle actions. They have addressed the mechanical properties of eccentric muscle action (force production and residual force enhancement), the neural control and muscle inhibitions associated with eccentric muscle actions, and issues associated with eccentric muscle action and injuries as a tool for rehabilitation.

Herzog discusses why muscles are stronger when they are actively lengthened compared to when they are shortening, using the cross-bridge theory. He then identifies the shortcomings of the cross-bridge theory in explaining eccentric muscle actions and discusses how sarcomere length nonuniformity and passive structural elements have been used to fill the gap left by the cross-bridge theory. He continues by explaining phenomena such as the residual force enhancement and reduced energetic cost in eccentric muscle action using a model that includes the engagement of a structural element in eccentric muscle actions.

Nishikawa et al. explore the topic of eccentric action and residual force enhancement further using a historical context, making a strong argument for eccentric muscle work as a tool in rehabilitation settings, specifically for patient populations with compromised oxygen uptake capacities. They also use a comparative approach between mammalian and molluscan skeletal muscles that may explain some of the mysteries surrounding the residual force enhancement property.

Schappacher-Tilp proposes an exciting new model of how eccentric muscle actions and the associated residual force enhancement properties can be explained and accommodated using a force-dependent activation of the myosin filament. She introduces a newly discovered cross-bridge state, the so-called super-relaxed state, which offers surprising possibilities for stabilizing skeletal muscles and explaining eccentric properties.

Liber expands on the issue of muscle injury associated with eccentric muscle actions and elaborates on experiments using desmin-deficient muscles. Desmin is not only an essential structural sarcomeric protein but is also a sensitive biological indicator of muscle injury. He proposes ways of how muscle injury can be prevented, expanding on the theme of Nishikawa et al. viewing eccentric muscle action as a rehabilitation tool.

The preceding 4 articles rely on muscle contraction theory, molecular and cellular research, and animal models, whereas the remaining 4 articles focus on applied research in humans using voluntary muscle contraction.

This theme is launched by an excellent review of the control aspects of eccentric muscle action by Aagaard. He focuses on the suppressed neuromuscular activity in eccentric contractions in untrained individuals, demonstrating that this inhibition in eccentric muscle action can be overcome by specific, heavy-load resistance training over weeks and months. He discusses the neural adaptations that occur with such training and how they affect muscle activation in eccentric action.

Hahn continues the argument on inhibition in voluntary eccentric muscle action and addresses the issue of reduced muscle force in voluntary eccentric contractions. He argues that this may not be an “inhibition” of muscle activity per se but rather an unfamiliarity with laboratory-based eccentric muscle tests that can be overcome by familiarization of the subjects with the eccentric tasks prior to testing.

De Brito Fontana et al. demonstrate in a rare assessment of residual force enhancement following eccentric action of upper arm flexor muscles that neuromuscular efficiency increases for a variety of different eccentric actions, but that neuromuscular efficiency is achieved in different ways depending on muscle lengths. These length-dependent differences result in a force–length curve that is flattened across the elbow range of motion following eccentric action, thus enhancing muscle function at very short and very long lengths, where the elbow flexors are naturally weak.

Finally, Mazara et al. study neuromuscular efficiency following eccentric muscle action in the human ankle plantar flexor group. They demonstrate an increase in force and a decrease in activation following eccentric muscle action compared to the purely isometric reference contraction. They observed that this apparent increase in muscle efficiency came at a cost: subjects had reduced muscle force control, suggesting that muscular efficiency following eccentric action comes at the cost of loss in fine motor control.

Summarizing, in this special issue of JSHS, we re-emphasize that eccentric muscle actions are not well captured by the traditional cross-bridge theory, that eccentric muscle actions are controlled with different activation strategies than concentric or isometric contractions, that these activation strategies are plastic and can be adapted by training and task familiarization, that eccentric actions change the mechanical properties of muscles, that they are not an injury risk (if performed properly), and that they offer benefits for rehabilitation and training programs in patients and athletes that go beyond (and have distinct advantages over) those of concentric and isometric contractions.

Needless to say, not all mysteries of eccentric muscle actions have been solved in this special issue. There is still the need to explain and understand the molecular mechanisms underlying the increase in force and decrease in metabolic cost during and following eccentric muscle actions, a need to understand inhibitory pathways in eccentric muscle action and their adaptation with training and familiarization, and a need for implementing and fully understanding the benefits of eccentric muscle action in training and rehabilitation, while avoiding injuries. I believe that studying eccentric muscle actions holds many more challenges and surprises for us, just as it did in the past decade. I also believe that structural proteins, such as titin, will emerge as crucial regulators of eccentric force and that studying eccentric muscle actions will help in our understanding of the molecular mechanisms underlying contraction.