Muscle force, work and cost: a novel technique to revisit the Fenn Effect

Abstract

Muscle produces force by forming cross-bridges, using energy released from ATP. While the magnitude and duration of force production primarily determine the energy requirement, nearly a century ago Fenn observed that muscle shortening or lengthening influenced energetic cost of contraction. When work is done by the muscle, the energy cost is increased and when work is done on the muscle the energy cost is reduced. However, the magnitude of the 'Fenn effect' and its mirror ('negative Fenn effect') have not been quantitatively resolved. We describe a new technique coupling magnetic resonance spectroscopy with an in vivo force clamp that can directly quantify the Fenn effect [E=I+W, energy liberated (E) equals the energy cost of isometric force production (I ) plus the work done (W )] and the negative Fenn effect (E=I−W ) for one muscle, the first dorsal interosseous (FDI). ATP cost was measured during a series of contractions, each of which occurred at a constant force and for a constant duration, thus constant force-time integral (FTI). In all subjects, as the FTI increased with load, there was a proportional linear increase in energy cost. In addition, the cost of producing force greatly increased when the muscle shortened, and was slightly reduced during lengthening contraction. These results, though limited to a single muscle, contraction velocity and muscle length change, do quantitatively support the Fenn effect. We speculate that they also suggest that an elastic element within the FDI muscle functions to preserve the force generated within the cross-bridges.

The metabolic cost of in vivo constant muscle force production at zero net mechanical work

“…Submaximally activated muscle fibres in vivo require about 3.6 times more metabolic energy per unit force when shortening and doing positive mechanical work, compared with when lengthening and doing negative mechanical work (Abbott et al, 1952). For both maximally activated muscle fibres in vitro (Beltman et al, 2004) and submaximally activated muscle fibres in vivo (Ortega et al, 2015;Ryschon et al, 1997), there is little or no difference between the metabolic cost per unit force when contracting isometrically and the metabolic cost per unit force when doing negative mechanical work. During many in vivo periodic movements, muscle-tendon complexes do alternating positive and negative mechanical work.…”

“…the 'metabolic cost'). Apart from consuming metabolic energy when doing mechanical work, muscle fibres consume metabolic energy when delivering force during isometric contraction (Ryschon et al, 1997;Beltman et al, 2004;Ortega et al, 2015). Maximally activated muscle fibres in vitro consume substantially more metabolic energy per unit force when shortening (doing positive mechanical work) compared with when contracting isometrically (doing no positive mechanical work) (Fenn, 1924;Hill, 1938).…”

Muscle Functional Morphology in Paleobiology: The Past, Present, and Future of “Paleomyology”

“…Because muscle is metabolically expensive to build and run, evidence that an extinct taxon has invested in an especially large muscle (say, for chewing, or for pelvic balance) is a strong signal for the functional importance of that muscle. Several anatomical and physiological variables are likely linked to the costs of using muscle (Fenn, ; Hill, ; Taylor et al, ; Griffin et al, ; Alexander, ; Pontzer, ; Ortega et al, ; Muchlinski et al, in review). The cost of contracting muscle concentrically (while it is shortening) is greater than the cost of contracting it eccentrically (while it is lengthening), likely due to elastic energy recovery in eccentric contraction (see Ortega et al, ).…”

Skeletal muscle tissue in movement and health: positives and negatives

“…The cost of force production was the least when the muscle was stretched (Fig. 2B) (Ortega et al, 2015). The minimal energy difference observed in lengthening contractions may have been increased if the muscle had been actively, rather than passively stretched.…”

“…We recently tested the Fenn effect quantitatively (Ortega et al, 2015). By coupling magnetic resonance spectroscopy with in vivo length and force measurements in the first dorsal interosseous (FDI) muscle in humans, we were able to control the magnitude and duration of force production.…”