Greater fatigability and motor unit discharge variability in human type 2 diabetes

Jonathon W Senefeld, Kevin G Keenan, Kevin S Ryan, Sarah E D'Astice, Francesco Negro, Sandra K Hunter, Jonathon W Senefeld, Kevin G Keenan, Kevin S Ryan, Sarah E D'Astice, Francesco Negro, Sandra K Hunter

Abstract

This study determined the discharge characteristics of motor units from two lower limb muscles before and after fatiguing exercise in people with type 2 diabetes (T2D) with no symptoms of polyneuropathy and activity-matched controls. Seventeen people with T2D (65.0 ± 5.6 years; 8 women) and 17 controls (63.6 ± 4.5 years; 8 women) performed: (a) intermittent, isometric contractions at 50% maximal voluntary isometric contraction (MVIC) sustained to failure with the ankle dorsiflexors, and (b) a dynamic fatiguing task (30% MVIC load) for 6 min with the knee extensors. Before and after the fatiguing tasks, motor unit characteristics (including coefficient of variation (CV) of interspike intervals (ISI)) were quantified from high-density electromyography and muscle contractile properties were assessed via electrical stimulation. Fatigability was ~50% greater for people with T2D than controls for the dorsiflexors (time-to-failure: 7.3 ± 4.1 vs. 14.3 ± 9.1 min, p = .010) and knee extensors (power reduction: 56.7 ± 11.9 vs. 31.5 ± 25.5%, p < .001). The CV of ISI was greater for the T2D than control group for the tibialis anterior (23.1 ± 11.0 vs. 21.3 ± 10.7%, p < .001) and vastus lateralis (27.8 ± 20.2 vs. 24.5 ± 16.1%, p = .011), but these differences did not change after the fatiguing exercises. People with T2D had greater reductions in the electrically evoked twitch amplitude of the dorsiflexors (8.5 ± 5.1 vs. 4.0 ± 3.4%·min-1 , p = .013) and knee extensors (49.1 ± 10.0 vs. 31.8 ± 15.9%, p = .004) than controls. Although motor unit activity was more variable in people with T2D than controls, the greater fatigability of the T2D group for lower limb muscles was due to mechanisms involving disruption of contractile function of the exercising muscles rather than motor unit behavior.

Keywords: contractile properties; diabetes mellitus; motor unit behavior; muscle fatigue; steadiness.

Conflict of interest statement

No conflicts of interest, financial or otherwise, are declared by the authors.

© 2020 The Authors. Physiological Reports published by Wiley Periodicals LLC on behalf of The Physiological Society and the American Physiological Society.

Figures

FIGURE 1
FIGURE 1
Representative muscle performance data from a 62‐year‐old man with type 2 diabetes. (a) Dorsiflexor torque during an intermittent, isometric fatiguing task. (b) Knee extensor power during the 6‐min dynamic fatiguing task. (c) Isometric knee extension torque (black line) and motor unit discharge times (vertical grey bars) of 20 verified motor units during a submaximal (40% MVIC) tracing task. Abbreviations: MVIC, maximal voluntary isometric contraction; W, Watts
FIGURE 2
FIGURE 2
Fatigability and Reductions in Electrically Evoked Twitch Amplitude for the Dorsiflexor and Knee Extensor Muscles. Fatigability was ~2× greater for people with T2D (blue symbols) compared to controls (grey symbols)—time‐to‐task failure for the static dorsiflexor fatiguing task (a) and the MVCC power at the end of the dynamic knee extensor fatiguing task (c). The reduction in electrically evoked twitch amplitude after the fatiguing task was not different (p = .371) for the dorsiflexor task (b) but was greater for people with T2D compared to controls after the knee extensor task (d). * denotes group difference between people with T2D and controls, p < .05. Men are denoted in circles and women are denoted in triangles
FIGURE 3
FIGURE 3
Associations with fatigability. The rate of reduction in electrically evoked twitch amplitude (%·min‐1) was associated with time‐to‐task failure (minutes) of the dorsiflexor muscles (a; r = −0.851, r2 = 0.724, p < .001) and the reduction in twitch amplitude (%) was associated with the reduction in maximal voluntary concentric contraction (MVCC) power (%) of the knee extensor muscles (b; r = 0.655, r2 = 0.429, p < .001)

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