Influence of group III/IV muscle afferents on small muscle mass exercise performance: a bioenergetics perspective

Abstract

Key points: This investigation assessed the influence of group III/IV muscle afferents on small muscle mass exercise performance from a skeletal muscle bioenergetics perspective. Group III/IV muscle afferent feedback was attenuated with lumbar intrathecal fentanyl during intermittent isometric single-leg knee-extensor all-out exercise, while ³¹ P-MRS was used to assess skeletal muscle bioenergetics. Attenuation of group III/IV muscle afferent feedback improved exercise performance during the first minute of exercise, due to an increase in total ATP production with no change in the ATP cost of contraction. However, exercise performance was not altered during the remainder of the protocol, despite a sustained increase in total ATP production, due to an exacerbated ATP cost of contraction. These findings reveal that group III/IV muscle afferents directly limit exercise performance during small muscle mass exercise, but, due to their critical role in maintaining skeletal muscle contractile efficiency, with time, the benefit of attenuating the muscle afferents is negated.

Abstract: The direct influence of group III/IV muscle afferents on exercise performance remains equivocal. Therefore, all-out intermittent isometric single-leg knee-extensor exercise and phosphorous magnetic resonance spectroscopy (³¹ P-MRS) were utilized to provide a high time resolution assessment of exercise performance and skeletal muscle bioenergetics in control conditions (CTRL) and with the attenuation of group III/IV muscle afferent feedback via lumbar intrathecal fentanyl (FENT). In both conditions, seven recreationally active men performed 60 maximal voluntary quadriceps contractions (MVC; 3 s contraction, 2 s relaxation), while knee-extensor force and ³¹ P-MRS were assessed during each MVC. The cumulative integrated force was significantly greater (8 ± 6%) in FENT than CTRL for the first minute of the all-out protocol, but was not significantly different for the second to fifth minutes. Total ATP production was significantly greater (16 ± 21%) in FENT than CTRL throughout the all-out exercise protocol, due to a significantly greater anaerobic ATP production (11 ± 13%) in FENT than CTRL with no significant difference in oxidative ATP production. The ATP cost of contraction was not significantly different between FENT and CTRL for the first minute of the all-out protocol, but was significantly greater (29 ± 34%) in FENT than in CTRL for the second to fifth minutes. These findings reveal that group III/IV muscle afferents directly limit exercise performance during small muscle mass exercise, but, due to their critical role in maintaining skeletal muscle contractile efficiency, with time, the benefit from muscle afferent attenuation is negated.

Keywords: intrathecal fentanyl; magnetic resonance spectroscopy; muscle metabolism.

Figure 1. Force production during the all‐out intermittent isometric single‐leg knee‐extensor exercise protocol

Seven subjects performed a series of 60 intermittent maximal voluntary contractions (3 s contraction, 2 s relaxation) over 5 min in both control (CTRL) and lumbar intrathecal fentanyl (FENT) conditions. The integrated force was determined per maximal voluntary contraction. Inset, the cumulative integrated force production for the first minute of exercise. Data are presented as means ± SEM. Significant time and interaction effects are indicated on the graph. †Significantly different from CTRL.

Figure 2. Rating of perceived exertion at the completion of the all‐out intermittent isometric single‐leg knee‐extensor exercise protocol

Ratings of perceived exertion (RPE) were obtained, using the Borg modified CR10 scale, from the subjects immediately upon completion of the exercise protocol in both control (CTRL) and lumbar intrathecal fentanyl (FENT) conditions. Data are presented as means ± SEM. †Significantly different from CTRL

Figure 3. Intramuscular metabolites during the all‐out intermittent isometric single‐leg knee‐extensor exercise protocol

Intramuscular phosphocreatine (PCr, A and B), inorganic phosphate (P_i, C), diprotonated phosphate (H₂PO₄ˉ, D), pH (E), ATP (F), ADP (G) and AMP (H) were determined with phosphorous magnetic resonance spectroscopy (³¹P‐MRS) in both control (CTRL) and lumbar intrathecal fentanyl (FENT) conditions. Data are presented as means ± SEM. Significant time and interaction effects are indicated on the graphs.

Figure 4. Adenosine triphosphate (ATP) synthesis rates and the ATP cost of contraction during the all‐out intermittent isometric single‐leg knee‐extensor exercise protocol

Rates of ATP synthesis through the creatine kinase reaction (ATP_CK, A), anaerobic glycolysis (ATP_GLY, B), cumulative anaerobic metabolism (ATP_ANA, C), oxidative phosphorylation (ATP_OX, D), total ATPase rate (ATP_TOTAL, E) and the ATP cost of contraction (F) were determined in both control (CTRL) and lumbar intrathecal fentanyl (FENT) conditions. These variables were calculated for each minute of the 60 MVC protocol and were normalized to the first minute of CTRL exercise. Data are presented as means ± SEM for each minute of exercise. Significant time, condition and interaction effects are indicated on the graphs. †Significantly different from CTRL at specific time point.

Figure 5. Graphical illustration of the skeletal muscle bioenergetic influence on exercise performance during the all‐out intermittent isometric single‐leg knee‐extensor exercise protocol

The percentage difference between control (CTRL) and lumbar intrathecal fentanyl (FENT) conditions (ΔCTRL to FENT) for integrated force, total adenosine triphosphate production (ATP_TOTAL) and the ATP cost of contraction are plotted for each minute of the protocol. Integrated force was significantly greater in FENT than CTRL for the first minute of exercise (dark grey shading), when ATP_TOTAL was significantly increased (light grey shading) with no significant change in the ATP cost of contraction. Integrated force was not significantly different between FENT and CTRL for the 2nd–5th min of exercise despite the sustained increase in ATP_TOTAL, due to the significantly increased ATP cost of contraction in FENT compared to CTRL.