Chronic exposure to stretch–shortening contractions results in skeletal muscle adaptation in young rats and maladaptation in old rats

Abstract

The objective of this research was to investigate skeletal muscle response to a chronic administration of stretch-shortening cycles (SSCs) in young and old rats. Dorsiflexor muscles of old (30 months, n = 5) and young (12 weeks, n = 6) rats were exposed 3 times/week for 4.5 weeks to a protocol of 80 maximal SSCs per exposure in vivo. Skeletal muscle response was characterized by isometric and dynamic performance, as well as by muscle wet mass and quantitative morphological analyses following the exposure period. The performance of the young and old groups was not statistically different at the start of the exposure. By the end of the exposure, however, a statistical difference was noted, as performance increased significantly in the young animals and decreased significantly in the old animals. Muscle wet mass of the left tibialis anterior (TA) in the treated limb was significantly greater in the youngthan in the old animals (p < 0.001), whereas there was no difference in the contra-lateral TA. No degenerative myofibers or changes in non-cellular interstitium were noted in either age group, but a significant increase was observed in the volume of the cellular interstitium in the exposed limb of the old animals (p = 0.01), which is indicative of an inflammatory response. Thus, a chronic exposure of SSCs results in significant performance increase and muscle hypertrophy in young animals, and a significant performance decrease and an increased cellular interstitial response in old animals. These findings suggest that age may impair the ability of skeletal muscle to adapt to repetitive mechanical loading, even in the absence of degeneration.

Eccentric contraction-induced injury to type I, IIa, and IIa/IIx muscle fibers of elderly adults

“…The heightened susceptibility to damage observed here, coupled with an impaired ability to recover from injury or adapt to repeated exercise reported by others (Dedrick and Clarkson 1990;McBride et al 1995;Brooks and Faulkner 1990;Rader and Faulkner 2006;Lavender and Nosaka 2006b;Cutlip et al 2006) could be a contributor to the reduced lower limb muscle strength of elderly adults. Because contraction-induced damage impairs excitation-contraction coupling and cross-bridge function (Balnave and Allen 1995;Warren et al 1994), a heightened susceptibility to injury could initiate the age-related deterioration in muscle fiber activation and contractility (Delbono et al 1995;Wang et al 2002;Larsson et al 1997;Thompson and Brown 1999;Lowe et al 2001;Frontera et al 2000;Hook et al 2001;Krivickas et al 2001).…”

“…Alternatively, functional deficits may not necessarily correspond with histological markers of fiber disruption or degeneration in aged animals, suggesting involvement of more subtle mechanisms. For instance, muscles of old rats chronically exposed to cycles of stretch-shortening contractions produced much less force than muscles from young animals subjected to the same stretchshortening protocol, yet muscles presented few histological features of fiber degeneration (Cutlip et al 2006).…”

“…In addition to the acute effects of eccentric muscular activity, the ability to recover from injury and to adapt to this mode of contractile activity have been reported to be impaired in old animals and elderly human subjects (Cutlip et al 2006;McBride et al 1995;Dedrick and Clarkson 1990;Clarkson and Dedrick 1988;Lavender and Nosaka 2006b;Brooks and Faulkner 1990;Rader and Faulkner 2006). In fact, it has been proposed that an increased susceptibility to eccentric exercise and/or an impaired ability to recover and adapt may underlie the force deficits that are characteristic of old age (Brooks and Faulkner 1990).…”

VCAM‐1 upregulation accompanies muscle remodeling following resistance‐type exercise in Snell dwarf (Pit1dw/dw) mice

“…For each SSC, the muscles were maximally activated at ankle angle 90° for 100 ms, rotated to 70° at 60°/s, returned to 90° at 60°/s, and deactivated 100 ms later. Chronic exposure to SSCs with a velocity of 60°/s induces adaptation without overt muscle inflammation and degeneration in young wild‐type rodents days to weeks into training (Baker, Hollander, Kashon, & Cutlip, 2010; Baker, Hollander, Mercer, Kashon, & Cutlip, 2008; Cutlip et al, 2006; Rader et al, 2017). At 5 min following the 80 SSCs, a maximal isometric tetanic contraction was measured and compared with pre‐80 SSC exposure values to determine recovery from fatigue (Rader et al, 2017).…”

“…The SSC protocol consisted of 80 maximally activated SSCs (8 sets with 10 repetitions per set) and has been validated repeatedly to increase performance for muscles of rats and mice (Cutlip et al, 2006; Rader et al, 2016; Rader, Naimo, Ensey, & Baker, 2017). Because of the potential for opposing training‐induced results for agonist vs. antagonist muscles, the agonist gastrocnemius and antagonist tibialis anterior (TA) muscles were evaluated (Rader et al, 2017).…”