Age-dependent Muscle Adaptation after Chronic Stretch-shortening Contractions in Rats

Abstract

Age-related differences in contraction-induced adaptation have been well characterized especially for young and old rodent models but much less so at intermediate ages. Therefore, additional research is warranted to determine to what extent alterations in adaptation are due to maturation versus aging per se. The purpose of our study was to evaluate muscles of Fisher 344XBrown Norway rats of various ages following one month of exposure to stretch-shortening contractions (SSCs). With exposure, muscles mass increased by ~10% for 27 and 30 month old rats vs. ~20% for 3 and 6 month old rats (P < 0.05). For 3 month old rats, maximum isometric force and dynamic peak force increased by 22 ± 8% and 27 ± 10%, respectively (P < 0.05). For 6 month old rats, these forces were unaltered by exposure and positive work capacity diminished by 27 ± 2% (P = 0.006). By 30 months of age, age-related deficits in maximum isometric force, peak force, negative work, and positive work were apparent and SSC exposure was ineffective at counteracting such deficits. Recovery from fatigue was also tested and exposure-induced improvements in fatigue recovery were indicated for 6 month old rats and to a lesser extent for 3 month old rats whereas no such effect was observed for older rats. Alterations in fatigue recovery were accompanied by evidence of substantial type IIb to IIx fiber type shifting. These results highlight the exceptional adaptive capacity for strength at a young age, the inclination for adaptation in fatigue recovery at early adulthood, and diminished adaptation for muscle performance in general beginning at late adulthood. Such findings motivate careful investigation to determine appropriate SSC exposures at all stages of life.

Keywords: Fisher 344XBrown Norway rats; dorsiflexor muscles; dynamometer; repetitive exposure.

Figure 1.

Muscle mass and isometric performance measures following chronic SSC exposure were age-dependent. For both the exposed and contralateral control TA muscles, muscle mass was normalized by tibia length. Maximum isometric forces were assessed for the initial and final weeks of SSC exposure. Final muscle quality was calculated for exposed muscles by dividing the final maximum isometric force value by normalized muscle mass. Sample sizes were N = 5 per group. Values are means ± S.E.M. *Different from non-exposed value (i.e. contralateral muscle in context of muscle mass or initial data in context of maximum isometric force and muscle quality); †Different from value for 3 month old rats; ‡Different from value for 6 month old rats; §Different from value for 27 month old rats, P< 0.05.

Fig. 2.

Chronic SSC-induced alterations in dynamic muscle performance were sensitive to aging. Measures of peak force, negative work, and positive work were evaluated for the single SSC test prior to the 80 contraction protocol in the initial and final weeks of exposure. For 3 month old rats, chronic SSC exposure increased peak force and a trend for an increase in the magnitude of work required to stretch muscle (i.e. negative work) was observed. For 6 month old rats, SSC exposure decreased the capacity for work done by the muscle during shortening (i.e. positive work). Sample sizes were N = 5 per group. Values are means ± S.E.M. *Different from initial value; †Different from value for 3 month old rats; ‡Different from value for 6 month old rats; §Different from value for 27 month old rats, P< 0.05.

Figure 3.

Age differential effects of chronic SSC exposure on SSC-induced fatigue were present. Values for peak force, negative work, and positive work were evaluated for the first set of 10 contractions for the SSC sessions of the initial and final weeks. (A) Analysis of the absolute values demonstrated that muscles of 3 month old rats either improved or maintained absolute performance while muscles of the older groups generated reduced values. (B) To evaluate fatigue in isolation, peak force, negative work, and positive work values were normalized to the value of the first contraction. Chronic SSC exposure decreased fatigue resistance for all of the outcomes for 3 month old rats and depending on the performance outcome, had either no effect or diminished fatigue resistance for the older groups. Sample sizes were N = 5 per group. Values are means ± S.E.M. *Different from initial value, P< 0.05.

Figure 4.

Indication of SSC-induced improvements in recovery from fatigue for the younger age groups. For the initial and final weeks of SSC exposure, isometric forces were evaluated 2 minutes after each 80 contraction session and expressed relative to the pre-session maximum isometric force. A single SSC test was also performed 4 minutes after each 80 contraction session to assess peak force, negative work, and positive work and expressed relative to these values prior to each session. Sample sizes were N = 5 per group. Values are means ± S.E.M. *Different from initial value; †Different from value for 3 month old rats; ‡Different from value for 6 month old rats, P< 0.05.

Figure 5.

MHC immunofluorescence labeling was apparent in transverse sections of contralateral and exposed TA muscles following chronic SSC exposure. MHC immunofluorescence labeling was apparent for laminin (green) and multiple MHC isoforms - I (blue), IIa (red), IIb (green), and IIx (negative for staining) - in transverse sections of contralateral and exposed TA muscles following chronic SSC exposure. Scale bar = 50 µm.

Figure 6.

Pronounced alterations in type IIb and IIx fiber type distribution were apparent for 3 and 6 month old rats but not at older ages after chronic SSC exposure. (A) Analysis of muscle fiber cross-sectional area for exposed and contralateral non-exposed muscles indicated that increased area occurred predominantly for type IIa and IIx fibers for all the age groups with the exception of 30 month old rats. (B) With exposure, the coupling of a decreased percentage of type IIb fibers with increased percentage of type IIx fibers occurred exclusively for 3 and 6 month old rats. (C) When fiber type percentage is expressed relative to the tissue, 6 month old rats were the only age group to exhibit SSC-induced changes in all type II fibers - IIa, IIx, and IIb fibers. Sample sizes were N = 5 per group. Values are means ± S.E.M. *Different from initial value; †Different from value for 3 month old rats; ‡Different from value for 6 month old rats, P< 0.05.