Oxidative capacity varies along the length of healthy human tibialis anterior

Abstract

Key points: During exercise skeletal muscles use the energy buffer phosphocreatine. The post-exercise recovery of phosphocreatine is a measure of the oxidative capacity of muscles and is traditionally assessed by ³¹ P magnetic resonance spectroscopy of a large tissue region, assuming homogeneous energy metabolism. To test this assumption, we collected spatially resolved spectra along the length of human tibialis anterior using a home-built array of ³¹ P detection coils, and observed a striking gradient in the recovery rate of phosphocreatine, decreasing along the proximo-distal axis of the muscle. A similar gradient along this muscle was observed in signal changes recorded by ¹ H muscle functional MRI. These findings identify intra-muscular variation in the physiology of muscles in action and highlight the importance of localized sampling for any methodology investigating oxidative metabolism of this, and potentially other muscles.

Abstract: The rate of phosphocreatine (PCr) recovery (k_PCr ) after exercise, characterizing muscle oxidative capacity, is traditionally assessed with unlocalized ³¹ P magnetic resonance spectroscopy (MRS) using a single surface coil. However, because of intramuscular variation in fibre type and oxygen supply, k_PCr may be non-uniform within muscles. We tested this along the length of the tibialis anterior (TA) muscle in 10 male volunteers. For this purpose, we employed a 3T MR system with a ³¹ P/¹ H volume transmit coil combined with a home-built ³¹ P phased-array receive probe, consisting of five coil elements covering the TA muscle length. Mono-exponential k_PCr was determined for all coil elements after 40 s of submaximal isometric dorsiflexion (SUBMAX) and incremental exercise to exhaustion (EXH). In addition, muscle functional MRI (¹ H mfMRI) was performed using the volume coil after another 40 s of SUBMAX. A strong gradient in k_PCr was observed along the TA (P < 0.001), being two times higher proximally vs. distally during SUBMAX and EXH. Statistical analysis showed that this gradient cannot be explained by pH variations. A similar gradient was seen in the slope of the initial post-exercise ¹ H mfMRI signal change, which was higher proximally than distally in both the TA and the extensor digitorum longus (P < 0.001) and strongly correlated with k_PCr . The pronounced differences along the TA in functional oxidative capacity identify regional variation in the physiological demand of this muscle during everyday activities and have implications for the bio-energetic assessment of interventions to modify its performance and of neuromuscular disorders involving the TA.

Keywords: 31P magnetic resonance spectroscopy; magnetic resonance imaging; oxidative metabolism; phosphocreatine recovery; skeletal muscle.