Effects of aging and sex on voluntary activation and peak relaxation rate of human elbow flexors studied with motor cortical stimulation

Abstract

Data are equivocal on whether voluntary activation is preserved or decreased in old compared to young adults. Further, data are scant on the effect of age on the rate of muscle relaxation when the muscle is contracting voluntarily. Assessment of both measures with transcranial magnetic stimulation (TMS) yields information which cannot be obtained with traditional peripheral nerve stimulation. Hence, voluntary activation and peak relaxation rate of the elbow flexors were assessed with TMS during repeated maximal efforts in 30 men and 28 women between the ages of 22-84 years. Voluntary activation was similar for the two sexes (P = 0.154) and was not affected by age in men (96.2 ± 2.7 %; P = 0.887) or women (95.1 ± 3.0 %; P = 0.546). Men had a significantly faster peak rate of relaxation than women in absolute units (-880.0 ± 223.2 vs. -360.2 ± 78.5 Nm/ s, respectively; P < 0.001) and when normalized to subject strength (-12.5 ± 2.1 vs. -8.7 ± 1.0 s(-1), respectively; P < 0.001). Absolute and normalized relaxation rates slowed with age in men (P = 0.002 and P = 0.006, respectively), but not women (P = 0.142 and P = 0.950, respectively). Across the age range studied, all subjects, regardless of age or sex, were able to achieve high voluntary activation scores for the elbow flexors (~95 %). In contrast, peak relaxation rate was markedly faster in men than women and slowed with age in men but not women. Normalization of relaxation rates to strength did not affect the influence of age or sex.

Fig. 1

Influence of stimulus intensity on amplitudes of the superimposed twitch and motor evoked potentials of the biceps and triceps. Data were recorded from a single subject (48-year old man) during multiple efforts at 50 % MVC to determine the optimal TMS intensity for the part of the protocol concerned with calculating voluntary activation. The optimal intensity (denoted by the shaded bar) was that which generated the greatest superimposed twitch amplitude whilst keeping the triceps MEP < 15 % the amplitude of the triceps compound muscle action potential (M_max) during a contraction at 100 % MVC (dotted horizontal line)

Fig. 2

Raw traces of elbow flexor torque and EMG responses to stimulation of the motor cortex during voluntary contractions at 50, 75 and 100 % maximal torque. Arrows indicate timing of the motor cortical stimulus. A, torque traces from a single subject (56-year-old man) showing the superimposed twitch (shaded area) and subsequent loss of torque caused by muscle relaxation. Dotted vertical lines indicate the time at which the peak relaxation rate occurred. B, corresponding biceps EMG traces showing motor-evoked potentials and silent periods. Solid vertical lines indicate the end of the silent period

Fig. 3

Calculation of the estimated resting twitch (ERT) in a single subject. A, data were recorded from a single subject (56-year-old man) during five sets of three contractions (one each at 50, 75 and 100 % MVC). Amplitude of the estimated resting twitch (ERT) is the y-intercept (18.4 Nm) of the extrapolated linear regression (r² = 0.98)

Fig. 4

Effect of age and sex on maximal torque, estimated resting twitch amplitude and voluntary activation. Data points represent peak values from individual men (n = 30 in A but 29 in B and C; filled circle) and women (n = 28 in A but 26 in B and C; empty circle) plotted against subject age. Linear regressions are displayed for men (solid line) and women (dashed line) separately. A, maximal torque was greater in men than women (P < 0.001). Maximal torque decreased with advancing age in men (P = 0.029) but only approached statistical significance in women (P = 0.060). B, expressed as a percentage of MVC torque, estimated resting twitch amplitude was similar in men and women (P = 0.234) and was unaffected by age in men (P = 0.496) and women (P = 0.066). C, voluntary activation was similar in men and women (P = 0.154) and unaffected by age in both men (P = 0.887) and women (P = 0.546)

Fig. 5

Effect of age and sex on absolute and normalized peak relaxation rates. Data points represent peak values from individual men (n = 30; filled circle) and women (n = 28; empty circle) plotted against subject age. Linear regressions are displayed for men (solid line) and women (dashed line) separately. Note that the y-axes are inverted and that larger negative numbers indicate a faster muscle relaxation. A, The absolute peak relaxation rate was faster in men than women (P < 0.001). Peak relaxation rate slowed with advancing age in men (P = 0.002) but not women (P = 0.142). B, Normalized rates represent absolute rates from A divided by the peak torque prior to the relaxation. Similar to absolute data, the normalized peak relaxation rate was faster in men than women (P < 0.001) and slowed with age in men (P = 0.006) but not women (P = 0.950)