Abstract

Aerobic physical activity triggers adaptations in skeletal muscle including a fast-to-slow shift in myosin heavy chain (MHC) isoforms, an enhanced capillary network, and mitochondrial biogenesis to meet increased demands placed upon this tissue. Although the magnitude of these responses appears to be dependent on muscle phenotype as well as training volume and/or intensity, the whole-muscle response to detraining remains mostly unexplored. Here, we hypothesized that the shifts toward slower MHC phentotype and the increased capillarity and mitochondrial oxidative markers induced with training would return toward sedentary (SED) control levels sooner in the fast plantaris than in the slow soleus muscle as a result of detraining. Soleus and plantaris muscles from 8-week (TR 8wk) voluntarily running adult female Sprague–Dawley rats were compared to muscles from SED and detrained rats (DETR) (4 weeks voluntary running followed by 4 weeks of reduced activity), which were subdivided into low- (DETR Lo) and high-running-distance (DETR Hi) groups. We show that maintaining the fast-to-slow MHC isoform shift required consistent aerobic training in the soleus and plantaris muscles: detraining clearly abolished any fast-to-slow gains in the plantaris, whereas the training volume in DETR Hi rats appeared to influence the MHC return to basal levels in the soleus. Total capillary number (per mm2) in the plantaris increased in all groups compared to SED levels, but, in the soleus, this enhancement was observed only in the TR 8wk rats. Generally, increased mitochondrial markers for aerobicitiy were observed in TR 8wk plantaris, but not soleus, muscles. In a second experiment, we show that the muscle-specific adaptations were similar after 4 weeks of voluntary exercise (TR 4wk) as in 4 weeks (TR 8wk). Taken together, our findings suggest that the plantaris muscle is more sensitive to voluntary physical activity and detraining than the soleus muscle; these results also demonstrate that the soleus muscle requires a greater aerobic challenge (i.e., intensity, duration) to trigger phenotypic, angiogenic, or aerobic enzyme adaptations. Our findings generally suggest that muscular aerobic fitness to voluntary running, or its loss during detraining, manifests as changes occurring primarily within fast, rather than slow, muscle phenotypes.

Highlights

  • Skeletal muscle adaptation to aerobic-endurance training is, in part, characterized by enhancements in oxygen consumption, blood flow, and a propensity for myosin heavy chain (MHC) isoforms to shift from fast-glycolytic to slow-oxidative phenotypes (Holloszy, 1967; Armstrong and Laughlin, 1984; Coyle et al, 1984; Ishihara et al, 1991; Montero et al, 2015)

  • The mean soleus absolute muscle mass was lower in detrained rats (DETR) Lo than DETR Hi (p < 0.05) and the mean soleus mass relative to body mass was lower in DETR Lo rats than SED, DETR Hi, and TR 8wk rats (p < 0.05)

  • Mean plantaris absolute mass was lower in TR 8wk rats than SED, DETR Lo, and DETR Hi rats (p < 0.05), whereas plantaris masses relative to body mass were similar among groups

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Summary

Introduction

Skeletal muscle adaptation to aerobic-endurance training is, in part, characterized by enhancements in oxygen consumption, blood flow, and a propensity for myosin heavy chain (MHC) isoforms to shift from fast-glycolytic to slow-oxidative phenotypes (Holloszy, 1967; Armstrong and Laughlin, 1984; Coyle et al, 1984; Ishihara et al, 1991; Montero et al, 2015). The rodent soleus muscle is characteristically fatigue-resistant and exhibits a greater capacity for oxidative metabolism, which is attributed to a high proportion of type I MHC and greater capillary and mitochondrial densities compared to other hindlimb muscles. These contractile and metabolic properties support the high levels of soleus recruitment in rats; the soleus is, by far, the most active hindlimb muscle during routine daily cage activity compared to other plantarflexors (Alford et al, 1987; Hodgson et al, 2005). The forces required for locomotion, as well as to change velocities for walking, running or sprinting are generated from phenotypically faster hindimb muscles, including the tibialis anterior, medial gastrocnemius, and plantaris muscles (Gardiner et al, 1986; Hodgson et al, 2005)

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