Age- and Sex-Related Differences in Motor Performance During Sustained Maximal Voluntary Contraction of the First Dorsal Interosseous

Abstract

Age and sex affect the neuromuscular system including performance fatigability. Data on performance fatigability and underlying mechanisms in hand muscles are scarce. Therefore, we determined the effects of age and sex on force decline, and the mechanisms contributing to force decline, during a sustained isometric maximal voluntary contraction (MVC) with the index finger abductor (first dorsal interosseous, FDI). Subjects (n = 51, age range: 19-77 years, 25 females) performed brief and a 2-min sustained MVC with the right FDI. Abduction force and root mean squared electromyographic activity (rms-EMG) were recorded in both hands. Double-pulse stimulation was applied to the ulnar nerve during (superimposed twitch) and after (doublet-force) the brief and sustained MVCs. Compared to females, males were stronger (134%, p < 0.001) and exhibited a greater decline in voluntary (difference: 8%, p = 0.010) and evoked (doublet) force (difference: 12%, p = 0.010) during and after the sustained MVC. Age did not affect MVC, force decline and superimposed twitch. The ratio between the doublet- and MVC-force was greater in females (0.33, p = 0.007) and in older (0.38, p = 0.06) individuals than in males (0.30) and younger (0.30) individuals; after the sustained MVC this ratio increased with age and the increase was larger for females compared to males (p = 0.04). The inadvertent contralateral, left force and rms-EMG activity increased over time (2.7-13.6% MVC and 5.4-17.7% MVC, respectively). Males had higher contralateral forces than females (p = 0.012) and contralateral force was higher at the start of the contralateral contraction in older compared with young subjects (difference: 29%, p = 0.008). In conclusion, our results suggest that the observed sex-differences in performance fatigability were mainly due to differences in peripheral muscle properties. Yet the reduced amount of contralateral activity and the larger difference in evoked versus voluntary force in female subjects indicate that sex-differences in voluntary activation should not be overlooked. These data obtained in neurological healthy adults provides a framework and help the interpretation and referencing of neurophysiological measures in patients suffering from neuromuscular diseases, who often present with symptoms of performance fatigability.

Keywords: FDI; aging; contralateral activity; doublets; performance fatigability; sex differences; twitches; voluntary activation.

FIGURE 1

Illustration of the force transducer and an overview of the motor tasks as illustrated by data of an individual subject (female, 64 years old). (A) Photo of the hands holding the force transducers. EMG electrodes were taped to the muscle belly of the FDI and close to the second metacarpal joint. Stimulation electrodes were placed on the ulnar nerve of the right forearm, one electrode at and a second electrode approximately two centimeters proximal from the wrist. (B) An example of four right and three left maximal voluntary contractions (MVCs) at baseline. Subjects alternated between the right and left hand. Electrical stimulation (stim) was applied to the ulnar nerve during the MVCs with the right hand and at rest (during the first stimulus the subject was not at rest yet). (C) Submaximal contractions with the left and right FDI at four different levels (10, 30, 50, and 70% MVC). During each contraction with the right FDI, electrical stimulation was applied to the ulnar nerve. (D) Brief MVC with electrical stimulation of the ulnar nerve, followed by two to three stimuli at rest. After 60 s rest, subjects performed a sustained MVC for 124 s. During this sustained contraction seven stimuli were applied to the ulnar nerve (18 s interval). Following the sustained contraction three doublet-forces were evoked at rest.

FIGURE 2

Mean and standard deviation of the doublet/voluntary force ratios. (A) Association between age and the ratio between the doublet at baseline and the MVC during brief MVC for male (closed symbols) and female subjects (open symbols). Data showed a significant effect of sex, and an interaction effect of sex ^∗ age. (B,C) The doublet at baseline/MVC, doublet prior to the sustained MVC/mean force during first 6 s of sustained MVC (Presustained MVC), doublet after the sustained MVC/mean force during last 6 s of sustained MVC (Postsustained MVC). Data (B) is illustrated for young males (<50 years old, open symbols) and females (closed symbols) and (C) for older males (≥50 years old, open symbols) and females (closed symbols).

FIGURE 3

Mean and standard deviation of the doublet-force for males and females during different force levels of submaximal contractions. Submaximal contractions were performed at circa 10, 30, 50, and 70% of subjects’ MVC. Doublet-forces were normalized as percentage of maximal doublet-force at rest during baseline measurements. Closed symbols represent male subjects, open symbols represent female subjects. The asterisk identifies a significant difference between males and females.

FIGURE 4

Mean and standard deviation of index finger abduction force and root mean squared EMG (rms-EMG) of the first dorsal interosseous (FDI) averaged over 2 s windows during the sustained MVC for males and females. Abduction force expressed as percentage of maximal force and rms-EMG activity expressed as percentage of maximal rms-EMG during brief MVCs at baseline. Values obtained at the times of peripheral nerve stimulation were excluded (every 18 s). (A) Index finger abduction force obtained in the right hand for male (closed symbols) and female subjects (open symbols). (B) Mean rms-EMG activity of the right FDI for male and female subjects during sustained MVC. (C) Averaged index finger abduction force obtained from the left non-target hand. (D) Mean rms-EMG activity of the left, contralateral non-target FDI for male and female subjects separately. The arrows with asterisks identify significant changes over time. Additionally, the significant interaction effect of time ^∗ sex is identified with a bracket and asterisk.

FIGURE 5

Mean and standard deviation of index finger abduction force and rms-EMG of the FDI averaged over 2 s windows during the sustained MVC for young (<50 years old, n = 27, 15 females; open symbols) and older (≥50 years old, n = 24, 10 female; closed symbols) subjects. Values obtained at the times of peripheral nerve stimulation were excluded (every 18 s). (A) Index finger abduction force obtained in the right hand during sustained MVC. (B) Averaged rms-EMG activity of the right FDI. Older subjects showed a smaller potentiation at the start of the sustained contraction, whereas young subjects show a gradual decline in rms-EMG activity of the right FDI. (C) Averaged index finger abduction force of the left hand. (D) Averaged rms-EMG activity of the left FDI. Older subjects exhibited higher averaged rms-EMG activity compared to young subjects. The arrows with asterisks identify significant changes over time. Additionally, the significant interaction effects of time ^∗ age are identified with a bracket and asterisk.

FIGURE 6

Mean and standard deviation of the superimposed twitches (SITs) as percentage of presustained twitch at rest. The x-axis shows times of stimulation; (0) SIT during brief MVC prior to the sustained MVC and times of SITs during sustained MVC (in seconds). The arrow with asterisk identifies a significant change over time.