Lower energy cost of skeletal muscle contractions in older humans

Abstract

Recent studies suggest that the cost of muscle contraction may be reduced in old age, which could be an important mediator of age-related differences in muscle fatigue under some circumstances. We used phosphorus magnetic resonance spectroscopy and electrically elicited contractions to examine the energetic cost of ankle dorsiflexion in 9 young (Y; 26 +/- 3.8 yr; mean +/- SD) and 9 older healthy men (O; 72 +/- 4.6). We hypothesized that the energy cost of twitch and tetanic contractions would be lower in O and that this difference would be greater during tetanic contractions at f(50) (frequency at 50% of peak force from force-frequency relationship) than at 25 Hz. The energy costs of a twitch (O = 0.13 +/- 0.04 mM ATP/twitch, Y = 0.18 +/- 0.06; P = 0.045) and a 60-s tetanus at 25 Hz (O = 1.5 +/- 0.4 mM ATP/s, Y = 2.0 +/- 0.2; P = 0.01) were 27% and 26% lower in O, respectively, while the respective force.time integrals were not different. In contrast, energy cost during a 90-s tetanus at f(50) (O = 10.9 +/- 2.0 Hz, Y = 14.8 +/- 2.1 Hz; P = 0.002) was 49% lower in O (1.0 +/- 0.2 mM ATP/s) compared with Y (1.9 +/- 0.2; P < 0.001). Y had greater force potentiation during the f(50) protocol, which accounted for the greater age difference in energy cost at f(50) compared with 25 Hz. These results provide novel evidence of an age-related difference in human contractile energy cost in vivo and suggest that intramuscular changes contribute to the lower cost of contraction in older muscle. This difference in energetics may provide an important mechanism for the enhanced fatigue resistance often observed in older individuals.

Fig. 1.

Dorsiflexor muscle force-frequency relationship for seven young (solid symbols) and eight older men (open symbols). Force is expressed in absolute units (top) and relative to peak force obtained during 75 Hz stimulation (bottom). Note the relative leftward shift in the relationship for the older men, which resulted in a significantly lower f₅₀ (Table 1). Data are expressed as mean ± SE; *P ≤ 0.001 between groups.

Fig. 2.

Twitch protocol. PCr (top), pH (middle), and ATP cost of a single twitch (bottom) in young (solid symbols, black line) and older (open symbols, gray line) men. Top, inset: FTI for all 600 twitches. Data are presented as means ± SE. *P = 0.05.

Fig. 3.

Representative stack plots (top) and changes in PCr (bottom) during a 2-Hz twitch protocol for 1 young (A, C) and 1 older (B, D) participant. Exponential fits are shown. Twitch cost = 0.24 and 0.15 mM·twitch^-1 for the young and older man, respectively.

Fig. 4.

Associations between twitch cost and contractile and metabolic properties. Associations between twitch cost and tetanic rate of force relaxation (n = 17; RFR not available for one O) (A), and end-contraction pH in Y (solid symbols) and O (open symbols) (B).

Fig. 5.

Force, PCr, and pH during tetanic protocols. Force, relative to 25 Hz peak (top), PCr (middle), and pH (bottom) for the 25 Hz (left) and f₅₀ (right) protocols in Y (solid symbols, black line) and O (open symbols, gray line), respectively. Note the different duration for the two contractions. f₅₀ = 14.8 ± 2.1 and 10.9 ± 2.0 Hz for Y and O, respectively. Data are presented as means ± SE. *P = 0.001.

Fig. 6.

Force and ATP cost during tetanic protocols. ATP cost (A) and mean force (B), averaged over the duration of the contraction, for the 25 Hz (left) and f₅₀ (right) protocols in Y (solid bars) and O (open bars). Data are presented as means ± SE. *P < 0.05.

Fig. 7.

Relative contribution of ATP-producing pathways. The relative contribution of oxidative phosphorylation (ATP_OX; black), the creatine kinase reaction (ATP_CK; gray), and glycolysis (ATP_GLY; open) for the 25 Hz (left) and f₅₀ (right) protocols. There were no age-related differences in the relative contribution of each of the pathways to total ATP production during the 25-Hz contraction, while older muscle generated relatively more ATP by oxidative phosphorylation and the creatine kinase reaction, and relatively less by glycolysis, compared with young during the f₅₀ contraction (P ≤ 0.002).