Oscillations in neural drive and age-related reductions in force steadiness with a cognitive challenge

Abstract

A cognitive challenge when imposed during a low-force isometric contraction will exacerbate sex- and age-related decreases in force steadiness, but the mechanism is not known. We determined the role of oscillations in the common synaptic input to motor units on force steadiness during a muscle contraction with a concurrent cognitive challenge. Forty-nine young adults (19-30 yr; 25 women, 24 men) and 36 old adults (60-85 yr; 19 women, 17 men) performed a cognitive challenge (counting backward by 13) during an isometric elbow flexion task at 5% of maximal voluntary contraction. Single-motor units were decomposed from high-density surface EMG recordings. For a subgroup of participants, motor units were matched during control and cognitive challenge trials, so the same motor unit was analyzed across conditions. Reduced force steadiness was associated with greater oscillations in the synaptic input to motor units during both control and cognitive challenge trials ( r = 0.45-0.47, P < 0.01). Old adults and young women showed greater oscillations in the common synaptic input to motor units and decreased force steadiness when the cognitive challenge was imposed, but young men showed no change across conditions (session × age × sex, P < 0.05). Oscillations in the common synaptic input to motor units is a potential mechanism for altered force steadiness when a cognitive challenge is imposed during low-force contractions in young women and old adults. NEW & NOTEWORTHY We found that oscillations in the common synaptic input to motor units were associated with a reduction in force steadiness when a cognitive challenge was imposed during low-force contractions of the elbow flexor muscles in young women and old men and women but not young men. Age- and sex-related muscle weakness was associated with these changes.

Keywords: aging; arousal; force fluctuations; sex differences.

Fig. 1.

Experimental protocol. Top: elbow flexor muscle force is represented. Bottom: horizontal arrows indicating when the cognitive challenge (CC; mental math) was performed during the protocol. During the cognitive challenge trials, mental math was performed without muscle contraction for 4 min and also continuously during contraction at 5% of maximal voluntary contraction (MVC). In the control trials, each individual sat quietly for the 4 min and performed the isometric contraction with no cognitive challenge. Horizontal arrows also indicate when visual analog scale (VAS) for anxiety, mean arterial pressure (MAP), electromyography (EMG) collected with high-density multiple array surface electrodes, and force steadiness were recorded. Results of different time points for anxiety (A1 and A2) and MAP (MAP1, MAP2, and MAP3) are further indicated in the text. The schematic is not to scale for time or force.

Fig. 2.

A and B: smoothed instantaneous motor unit discharge rate during the control (A) and cognitive challenge (CC) trials (B). Three motor units were decomposed and matched across the control and CC trials. C and D: the 3 components from the smoothed discharge rates for control (C) and CC (D); the bottom component is the common component. The first common component (FCC) increased from control to the CC motor tasks. E and F: smoothed force records at 5% MVC for control (E) and CC (F) trials. Coefficient of variation of force increased from 1.8 to 5.1% from control to CC trial. PPS, pulse per second.

Fig. 3.

Coefficient of variation (CV) of the first common component (FCC; A) and CV of force (B) quantified during contractions at 5% of maximal voluntary contraction (MVC) for young and old men and women. All groups increased both the CV of discharge rate and CV of force, except for young men (session × age × sex: P < 0.05 for both variables). Values are means ± SE. CC, cognitive challenge.

Fig. 4.

Associations between the coefficient of variation (CV) of force and CV of the first common component for the control trial (r =0.47, P < 0.05; A) and cognitive (CC) challenge trial (r = 0.45, P < 0.05; B). Solid lines, regression lines; dashed lines, 95% predicted interval.

Fig. 5.

Associations between maximal voluntary contraction (MVC) and the increase in the coefficient of variation (CV) of the first common component (A and C) and force signal (B and D) during the cognitive challenge (CC) trial. Regression lines show that stronger young and old men had less increase in the CV of the first common component (r = −0.45, P < 0.05; A) and less increase in the CV of force (r = −0.44, P < 0.05; B) with imposition of the cognitive challenge. MVC was not associated with the increase in the CV of the first common component (C) or CV of force (D) for young and old women. Solid lines, regression lines; dashed lines, 95% predicted interval.