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.

Keywords: 31P MRS; First dorsal interosseous; Muscle energetics; Muscle mechanics.

Conflict of interest statement

Competing interests

The authors declare no competing or financial interests.

© 2015. Published by The Company of Biologists Ltd.

Figures

Fig. 1.

The energy cost of force generation as a function of the force–time integral (FTI) in the first dorsal interosseus (FDI) muscle. When data from all subjects and all trials are combined for shortening (A), isometric (B) and lengthening (C) contractions, the energy cost to produce force during each type of contraction increases linearly with the magnitude of the force produced (all contractions were 0.9 s in duration). Dashed lines represent the 95% confidence intervals of the regression equations shown. When external work is performed during shortening contraction (A) the cost is significantly higher than if no work is done (B) for the identical FTI. When energy is absorbed by the FDI muscle (i.e. ‘negative work’) during lengthening contraction (C), there is a slight but significant reduction in the cost of producing the equivalent amount of force relative to the isometric contraction (B).

Fig. 2.

Test of the Fenn effect. (A) The measured energy cost of isometric contraction combined with the work done by the FDI muscle during a shortening contraction shown as a function of FTI (filled circles). Solid line represents least square regression equation (R2=0.87) and dashed lines represent the 95% confidence intervals of the regression equations. (B) When the external work (force×distance) done by the FDI muscle during shortening contraction is added to the cost of isometrically producing the same force, the result is a direct test of the Fenn effect. Here, we compare the calculated energy cost of external work performed during shortening contractions added to the isometric cost of force production (Iso + work) and the measured cost of shortening contraction and isometric contraction. In short, these results are consistent with the Fenn effect, Cost=W+I.

Fig. 3.

Test of the negative Fenn effect. (A) Theoretic cost of performing negative work during lengthening contraction as a function of FTI (filled circles). Solid line represents least square regression equation (R2=0.06) and dashed lines represent the 95% confidence intervals of the regression equations. When the external work (force×distance) done by the FDI muscle during lengthening contraction is subtracted from the cost of isometrically producing the same force, the result is a direct test of the negative Fenn effect. Because the cost of an isometric contraction is nearly equal to the energy absorbed by the FDI (i.e. ‘negative work’) during lengthening contraction, the predicted cost of lengthening contractions according to the negative Fenn effect was close to zero. (B) The calculated energy cost of external work performed during lengthening contractions subtracted from the isometric cost of force production (Iso – work) and the measured cost of lengthening contraction and isometric contraction. These results suggests that, at least under these experimental conditions in the FDI muscle, there could be no true negative Fenn effect unless there was no energy cost of lengthening contraction.

Fig. 4.

Illustrations demonstrating the force–length apparatus (FLA) and the simple FDI muscle lever system in the starting position for each contraction type. (A) The FLA acts as an in vivo force clamp composed of an electronic length gauge (LG, blue), two force transducers (FT, purple), and latex tubing (yellow) oriented around three low friction pulleys (orange). (B) The starting position (solid lines) and ending position (dashed lines) of the index finger are shown for shortening (top panel), isometric (middle panel) and lengthening (bottom panel) contractions of the FDI muscle. In all three conditions, the resistive force acts in the same direction, as indicated by the force vector arrow. For the shortening and isometric condition, contractions began with the finger in a neutral position (0 deg at center) whereas the starting position of the finger for the lengthening condition was 15 mm abducted from neutral. The illustration also shows how the foot pedal control system was used to set the finger position for a lengthening contraction.

Fig. 5.

Index finger force and position as a function of time during contractions. (A) Shortening, (B) isometric and (C) lengthening contractions. For all three conditions, finger force (red line) was held nearly constant as the finger was concentrically abducted (shortening contraction) 15 mm, held in place (isometric contraction), or eccentrically adducted (lengthening contraction) 15 mm.