Evolving concepts on the age-related changes in "muscle quality"

Abstract

The deterioration of skeletal muscle with advancing age has long been anecdotally recognized and has been of scientific interest for more than 150 years. Over the past several decades, the scientific and medical communities have recognized that skeletal muscle dysfunction (e.g., muscle weakness, poor muscle coordination, etc.) is a debilitating and life-threatening condition in the elderly. For example, the age-associated loss of muscle strength is highly associated with both mortality and physical disability. It is well-accepted that voluntary muscle force production is not solely dependent upon muscle size, but rather results from a combination of neurologic and skeletal muscle factors, and that biologic properties of both of these systems are altered with aging. Accordingly, numerous scientists and clinicians have used the term "muscle quality" to describe the relationship between voluntary muscle strength and muscle size. In this review article, we discuss the age-associated changes in the neuromuscular system-starting at the level of the brain and proceeding down to the subcellular level of individual muscle fibers-that are potentially influential in the etiology of dynapenia (age-related loss of muscle strength and power).

Fig. 1

Age-related changes in voluntary activation (a measure of how much of a muscle’s possible force is produced by a voluntary contraction) is muscle group specific. Studies quantifying age-related differences in voluntary activation of the knee extensors (a), elbow flexors (b), and ankle dorsiflexors (c) during isometric contractions. Selected studies have been highlighted with an arrow pointing to them (see main text for further discussion on these specific papers). Data points in a correspond to the following articles: filled circles: [50], filled squares: [48], filled diamonds: [35], filled triangle: [40], open circles: [51], open squares: [36], open diamonds: [46]. Data points in b correspond to the following articles: filled circles: [38], filled squares: [34], filled diamonds: [45], filled triangle: [42], open circles: [52], open squares: [41], open diamonds: [53]. Data points in c correspond to the following articles: filled circles: [43], filled squares: [38], filled diamonds: [47], filled triangle: [44], open circles: [49], open squares: [37]. Reprinted with permission from [233]

Fig. 2

Age-related decline in the human soleus muscles H-max to M-max ratio suggesting that advancing age results in a decrease in global spinal excitability. Data were obtained during standing while the muscle was activated at an intensity equal to 15% of its maximum voluntary contraction. Reprinted with permission from [234]

Fig. 3

Percentage of motor unit trains in which doublets were observed in young (black) and older (white) individuals at three rates of force production. There were no significant differences among rates of force production, but significant differences between groups were found, indicating that the young subjects tended to display more doublet discharges. Reprinted with permission from [105]

Fig. 4

Lack of difference in myosin/actin ratio between adult (6–8 months) and old (24 months) muscles. a Representative Coomassie-stained gel. Lane 1, molecular weight markers; lane 2, myofibrillar fraction from a previous experiment for positive control; lanes 11 and 14, actin standards of 2.0 and 1.0 μg, respectively; lanes 12 and 13, BSA standards of 2.5 and 5 μg, respectively; lanes 3 and 4, adult and old soleus; lanes 5 and 6, adult and old plantaris; lanes 7 and 8, adult and old medial gastrocnemius; lanes 9 and 10, adult and old lateral gastrocnemius. b Mean (±SE) myosin/actin ratio for adult and old muscles (n = 8/group). Unpublished data from Russ Laboratory

Fig. 5

Graphical illustration of the excitation–contraction coupling process. VICR voltage-induced calcium release, CICR calcium-induced calcium release, SOCE store-operated calcium entry, RYR ryanodine receptor, DHPR dihydropyridine receptor, SERCA sarcoplasmic/endoplasmic reticulum calcium ATPase, JP juntophilin