Post-exercise intramuscular O₂ supply is tightly coupled with a higher proximal-to-distal ATP synthesis rate in human tibialis anterior

Heskamp, Linda, Lebbink, Franciska, van Uden, Mark J, Maas, Marnix C, Claassen, Jurgen AHR, Froeling, Martijn, Kemp, Graham J ORCID: 0000-0002-8324-9666, Boss, Andreas and Heerschap, Arend (2021) Post-exercise intramuscular O₂ supply is tightly coupled with a higher proximal-to-distal ATP synthesis rate in human tibialis anterior. JOURNAL OF PHYSIOLOGY-LONDON, 599 (5). pp. 1533-1550.

Text Heskamp 2021 J Physiol.pdf - Author Accepted Manuscript Download (2MB) | Preview

Abstract

<h4>Key points</h4>The post-exercise recovery of phosphocreatine, a measure of the oxidative capacity of muscles, as assessed by ³¹ P MR spectroscopy, shows a striking increase from distal to proximal along the human tibialis anterior muscle. To investigate why this muscle exhibits a greater oxidative capacity proximally, we tested whether the spatial variation in phosphocreatine recovery rate is related to oxygen supply, muscle fibre type or type of exercise. We revealed that oxygen supply also increases from distal to proximal along the tibialis anterior, and that it strongly correlated with phosphocreatine recovery. Carnosine level, a surrogate measure for muscle fibre type was not different between proximal and distal, and type of exercise did not affect the gradient in phosphocreatine recovery rate. Taken together, the findings of this study suggest that the post-exercise spatial gradients in oxygen supply and phosphocreatine recovery are driven by a higher intrinsic mitochondrial oxidative capacity proximally.<h4>Abstract</h4>Phosphorus magnetic resonance spectroscopy (³¹ P MRS) of human tibialis anterior (TA) revealed a strong proximo-distal gradient in the post-exercise phosphocreatine (PCr) recovery rate constant (k_PCr ), a measure of muscle oxidative capacity. The aim of this study was to investigate whether this k_PCr gradient is related to O₂ supply, resting phosphorylation potential, muscle fibre type, or type of exercise. Fifteen male volunteers performed continuous isometric ankle dorsiflexion at 30% maximum force until exhaustion. At multiple locations along the TA, we measured the oxidative PCr resynthesis rate (V_PCr = k_PCr × PCr depletion) by ³¹ P MRS, the oxyhaemoglobin recovery rate constant (k_O2Hb ) by near infrared spectroscopy, and muscle perfusion with MR intravoxel incoherent motion imaging. The k_O2Hb , k_PCr , V_PCr and muscle perfusion depended on measurement location (P < 0.001, P < 0.001, P = 0.032 and P = 0.003, respectively), all being greater proximally. The k_O2Hb and muscle perfusion correlated with k_PCr (r = 0.956 and r = 0.852, respectively) and V_PCr (r = 0.932 and r = 0.985, respectively), the latter reflecting metabolic O₂ consumption. Resting phosphorylation potential (PCr/inorganic phosphate) was also higher proximally (P < 0.001). The surrogate for fibre type, carnosine content measured by ¹ H MRS, did not differ between distal and proximal TA (P = 0.884). Performing intermittent exercise to avoid exercise ischaemia, still led to larger k_PCr proximally than distally (P = 0.013). In conclusion, the spatial k_PCr gradient is strongly associated with the spatial variation in O₂ supply. It cannot be explained by exercise-induced ischaemia nor by fibre type. Our findings suggest it is driven by a higher proximal intrinsic mitochondrial oxidative capacity, apparently to support contractile performance of the TA.

Item Type:	Article
Uncontrolled Keywords:	P-31 magnetic resonance spectroscopy, magnetic resonance imaging, oxidative metabolism, phosphocreatine recovery, skeletal muscle
Divisions:	Faculty of Health and Life Sciences Faculty of Health and Life Sciences > Faculty of Health and Life Sciences Faculty of Health and Life Sciences > Institute of Life Courses and Medical Sciences
Depositing User:	Symplectic Admin
Date Deposited:	12 Mar 2021 08:03
Last Modified:	16 Oct 2023 22:46
DOI:	10.1113/JP280771
Related URLs:	Author Publisher
URI:	https://livrepository.liverpool.ac.uk/id/eprint/3117055