Changes in single motor unit behaviour contribute to the increase in contraction speed after dynamic training in humans

Abstract

1. The adaptations of the ankle dorsiflexor muscles and the behaviour of single motor units in the tibialis anterior in response to 12 weeks of dynamic training were studied in five human subjects. In each training session ten series of ten fast dorsiflexions were performed 5 days a week, against a load of 30-40% of the maximal muscle strength. 2. Training led to an enhancement of maximal voluntary muscle contraction (MVC) and the speed of voluntary ballistic contraction. This last enhancement was mainly related to neural adaptations since the time course of the muscle twitch induced by electrical stimulation remained unaffected. 3. The motor unit torque, recorded by the spike-triggered averaging method, increased without any change in its time to peak. The orderly motor unit recruitment (size principle) was preserved during slow ramp contraction after training but the units were activated earlier and had a greater maximal firing frequency during voluntary ballistic contractions. In addition, the high frequency firing rate observed at the onset of the contractions was maintained during the subsequent spikes after training. 4. Dynamic training induced brief (2-5 ms) motor unit interspike intervals, or 'doublets'. These doublets appeared to be different from the closely spaced (+/-10 ms) discharges usually observed at the onset of the ballistic contractions. Motor units with different recruitment thresholds showed doublet discharges and the percentage of the sample of units firing doublets was increased by training from 5.2 to 32.7%. The presence of these discharges was observed not only at the onset of the series of spikes but also later in the electromyographic (EMG) burst. 5. It is likely that earlier motor unit activation, extra doublets and enhanced maximal firing rate contribute to the increase in the speed of voluntary muscle contraction after dynamic training.

Figure 1. Rate of tension development as a function of torque and comparison of torque and rectified EMG during ballistic contractions

A, relationship for all subjects between the rate of tension development and torque (expressed as a percentage of MVC) during ballistic contractions. The linear regression lines are, respectively, y = 0.0042x + 0.057 (r = 0.75; P < 0.001) and y = 0.0065x+ 0.063 (r = 0.86; P < 0.001) before and after training. The slopes of the relationships before and after training are significantly different (P < 0.001). B, comparison of the torque and rectified EMG recorded in one subject during a ballistic contraction with a similar MVC percentage (41 vs. 44 %), before and after training.

Figure 2. Distribution of single motor unit recruitment thresholds and contractile properties

Histograms showing the distribution of single motor unit (MU) recruitment thresholds for all subjects expressed either as an absolute value (A) or as a percentage of MVC (B), twitch torques (C) or the time-to-peak torque (D) before and after training. Whereas no significant difference was observed before and after training for the time-to-peak torque distributions (Student's t test), the distributions of the recruitment thresholds and the twitch torques are significantly different (Kolmogorov-Smirnov two-sample test).

Figure 3. Comparison of motor unit twitch torque in one subject before and after training

A, comparison of two motor units recruited in one subject at a similar threshold (58 vs. 56 % of MVC) before (left-hand traces) and after training (right-hand traces). The motor unit action potential and the corresponding mechanical contribution extracted by spike-triggered averaging (200 sweeps) are illustrated. B, the motor unit twitch torque in the same subject before (42 units) and after training (60 units) plotted as a function of the recruitment threshold (expressed as a percentage of MVC) during a ramp contraction. The linear regression lines are, respectively, y = 0.89x + 7.8 (r = 0.89; P < 0.001) and y = 1.07x+ 16.3 (r = 0.83; P < 0.001) before and after training. The ordinate intercepts of the relationships before and after training are significantly different (P < 0.05).

Figure 4. Behaviour of single motor units during ballistic contractions

Behaviour of single motor units during ballistic contractions of similar torque levels (41 vs. 44 % of MVC) before (A) and after (B) dynamic training. The traces correspond to the mechanical force (a) and the intramuscular EMG plotted at slow (b) and fast (c) speeds. In A, a typical example of the firing pattern of a single motor unit in untrained muscle shows a short time lapse between the first two spikes followed by longer interspike periods. The first three interspike intervals are 8, 23 and 36 ms, respectively. B illustrates the usual motor unit behaviour in trained muscle, showing that the high onset of the instantaneous firing rate is maintained during the subsequent spikes. The first three interspike intervals are 11.8, 10 and 11 ms, respectively. The asterisks indicate the discharge of the same motor unit and their traces are superimposed with an extended display (b).

Figure 5. Examples of doublet discharges of single motor units during ballistic contraction after dynamic training

The traces correspond to the mechanical force (a), and the intramuscular EMG plotted at slow (b) and fast (c) speeds. A illustrates two different motor units which started to discharge with a doublet. Motor unit 1 fired two doublets (2.4 and 4.8 ms, respectively) while motor unit 2 discharged with a double spike of 4.2 ms interval. B illustrates a doublet which appeared later during the contraction. The motor unit illustrated showed three single firings at interspike intervals of, respectively, 14, 12.5 and 6 ms, followed by a 3.4 ms doublet. The asterisks indicate double discharges and their traces are superimposed with an extended display (d). Note that in Bd, the double discharge has been superimposed on the first 3 single spikes.

Figure 6. Distribution of the first three interspike intervals during ballistic contractions

Histograms showing the distribution of the first three interspike intervals during ballistic contractions for the whole motor unit (MU) population studied both before and after training. The comparison of the distributions before and after training are significantly different (P < 0.001; Kolmogorov-Smirnov two-sample test) for the three interspike intervals.