The aging neuromuscular system and motor performance

Abstract

Age-related changes in the basic functional unit of the neuromuscular system, the motor unit, and its neural inputs have a profound effect on motor function, especially among the expanding number of old (older than ∼60 yr) and very old (older than ∼80 yr) adults. This review presents evidence that age-related changes in motor unit morphology and properties lead to impaired motor performance that includes 1) reduced maximal strength and power, slower contractile velocity, and increased fatigability; and 2) increased variability during and between motor tasks, including decreased force steadiness and increased variability of contraction velocity and torque over repeat contractions. The age-related increase in variability of motor performance with aging appears to involve reduced and more variable synaptic inputs that drive motor neuron activation, fewer and larger motor units, less stable neuromuscular junctions, lower and more variable motor unit action potential discharge rates, and smaller and slower skeletal muscle fibers that coexpress different myosin heavy chain isoforms in the muscle of older adults. Physical activity may modify motor unit properties and function in old men and women, although the effects on variability of motor performance are largely unknown. Many studies are of cross-sectional design, so there is a tremendous opportunity to perform high-impact and longitudinal studies along the continuum of aging that determine 1) the influence and cause of the increased variability with aging on functional performance tasks, and 2) whether lifestyle factors such as physical exercise can minimize this age-related variability in motor performance in the rapidly expanding numbers of very old adults.

Keywords: aging; contractile velocity; motor unit; muscle fatigue; power; steadiness; strength; voluntary activation.

Copyright © 2016 the American Physiological Society.

Figures

Fig. 1.

Structural and physiological changes to the aging motor unit (MU) and motor performance outcomes. Shown is a working model of some of the known age-related changes in structures (top) and physiology and function (middle) that are thought to occur at each level of the MU identified as the motor neuron, neuromuscular junction, and muscle fibers (top row). Arrows (left) indicate the direction of change that occurs with advanced age. The supporting evidence varies for those variables identified, so a question mark (?) denotes when there is conflicting or small amounts of evidence. Furthermore, other factors (not shown) such as physical activity, nutrition, genetics, and inflammation among other possible modifiers, can interact with biological aging to alter motor performance in old and very old adults. Supraspinal and spinal inputs are not highlighted here but are influential. Motor performance outcomes (bottom) are each influenced to varying degrees by the variables in the model. The panels are interconnected so that the changes in physiology and function in one column (e.g., the motor neuron) are profoundly affected by age-related changes in the structures and physiology from the other levels (columns) of the motor unit (e.g., the neuromuscular junction and the muscle fibers). Ach, acetylcholine; Ca2+, calcium; Endog, endogenous; MHC, myosin heavy chain; NMJ, neuromuscular junction; SR, sarcoplasmic reticulum.

Fig. 2.

Age-related change in neural activation during voluntary maximal effort contractions. Torque (1) and behavior of single motor units (2) from the tibialis anterior of a young (A) and an old (B) adult during a brief isometric contraction performed during rapid force development. Intramuscular electromyographic (EMG) recordings are shown over the same time interval as the torque (2) and also with a greater time resolution inset of the EMG data (3). *Discharge of the same motor unit (2 and 3) and their traces are superimposed (4). Both the recruitment threshold [2–3% maximum voluntary contraction (MVC)] and the peak torque (∼50% of MVC) were similar for the two motor units identified with intramuscular EMG recordings. The maximal rate of torque development was lower in the old subject (480% MVC/s) compared with the young subject (784% MVC/s). The instantaneous discharge rate during the first three interspike intervals were 78, 71, and 61 Hz, respectively, for the young adult; and 63, 40, and 34 Hz, respectively, for the old adult. [A and B are borrowed from Fig. 6 in Klass et al. (80)]. C and D: voluntary activation (estimated from interpolating cortical stimulation during MVC) for each individual during five brief MVCs with the elbow flexor muscles in young (n = 17; age, 25.5 ± 3.6 yr) and old (n = 7; age, 73.0 ± 3.3 yr) adults. C: old adults had lower voluntary activation compared with young adults during trials 1–3, but similar values were obtained between groups during trials 4 and 5 (age × trial interaction, P < 0.01). D: larger variability in voluntary activation between the old adults compared with young adults for each of the trials. [C and D are borrowed from Fig. 2 in Hunter et al. (63)].

Fig. 3.

Age-related variability during fatiguing contractions. Top: time to task failure during fatiguing contractions with the ankle dorsiflexor muscles for young (A) and old (B) adults during control (circle), low-cognitive demand (subtracting by 1) (Low-CD, triangles), and high-cognitive demand (subtracting by 13) (High-CD, squares) sessions. Data for each individual are displayed for each session (men and women are separated by the middle vertical line). The mean for each session is on the ri ght. The range and variability of time to task failure among the old adults and women were greater than for the young adults and men, respectively, for each session. [A and B are Fig. 4 from Vanden Noven et al. (150), CC BY 3.0, http://journal.frontiersin.org/article/10.3389/fnagi.2014.00097/full.] C: representative data of maximal velocity of knee extensor muscles during the first (–5) and last (–90) contractions performed during a fatiguing contraction with a load equivalent to 20% of MVC for a young man (black line) and old man (gray dashed line). Contractions were performed once every 3 s. Overall, the old adults (n = 32, 71.3 ± 6.3 yr; 14 women) had greater reductions in velocity at the last five contractions compared with young adults (n = 35; age, 21.0 ± 2.6 yr; 19 women). On average, there was ∼35% age-related difference in the reduction of velocity. D: coefficient of variation (CV) of velocity during the same contractions depicted in C. Old adults had greater CV of power compared with young adults during the first five contractions. At the last five contractions old adults had a greater increase in CV of power than young adults. [C and D are from data extracted from Senefeld et al. (134)].

Fig. 4.

Force steadiness with and without imposition of a cognitive challenge in young and (A, C, and E) old (B, D, and F) adults. A and B: representative force signals of the elbow flexor muscles in a young and an old woman performed at 5% of MVC for a control and high-cognitive demand trial (subtracting by 13). C and D: CV of force for the elbow flexor muscles during contractions at 5, 7, 10, and 20% of MVC. Values are means ± SE for men (filled symbols) and women (open symbols) during the control session (circles) and high-cognitive demand session (subtracting by 13) (High-CD, squares). [Data for A and B are from Pereira et al. (116), and for the 7–20% MVC from Pereira HM and Hunter SK, unpublished.] E and F: CV of force for the ankle dorsiflexor muscles during contractions at 5% MVC performed by men and women for a control (filled circles), low-cognitive demand (Low-CD, subtracting by 1; open triangles) and high-cognitive demand (High-CD, subtracting by 13; filled squares) trials. The mean is shown for each session for young (E) and old (F) adults. E and F show that old adults, especially women, exhibited greater between trial variability in CV of force with imposition of the cognitive demand. [E and F were created using data presented in Vanden Noven et al. (150).]