Age-related reductions in the number of serial sarcomeres contribute to shorter fascicle lengths but not elevated passive tension

Power, Geoffrey A.; Crooks, Sean; Fletcher, Jared R.; MacIntosh, Brian R.; Herzog, Walter

doi:10.1101/2020.12.21.423814

Cited by 6 publications

(4 citation statements)

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“…This disconnect between ultrasound-derived FL and actual SSN explains why some studies in humans have observed age-related differences in ultrasound-derived FL (6,16,(53)(54)(55)(56)(57)(58)(59)(60)(61)(62) while others observed no differences (63)(64)(65)(66)(67)(68)(69). Our results are consistent with previous studies that observed 7-37% lesser SSN in old than young rats and mice (9,11,70).…”

Section: Age-related Differences In Baseline Muscle Morphologysupporting

confidence: 90%

Age-related differences in the loss and recovery of serial sarcomere number following disuse atrophy in rats

Hinks,

Power

2024

Preprint

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BackgroundOlder adults exhibit a slower recovery of muscle mass following disuse atrophy than young adults. At a smaller scale, muscle fibre cross-sectional area (i.e., sarcomeres in parallel) exhibits this same pattern. Less is known, however, about age-related differences in the recovery of muscle fibre length, driven by increases in serial sarcomere number (SSN), following disuse. The purpose of this study was to investigate age-related differences in SSN adaptations and muscle mechanical function during and following muscle immobilization. We hypothesized that old rats would experience a similar magnitude of SSN loss during immobilization, however, take longer to recover SSN than young following cast removal, which would limit the recovery of muscle mechanical function.MethodsWe casted the plantar flexors of young (8 months) and old (32 months) male rats in a shortened position for 2 weeks, and assessed recovery during 4 weeks of voluntary ambulation. Following sacrifice, legs were fixed in formalin for measurement of soleus wet weight and SSN with the un-casted soleus acting as a control. Ultrasonographic measurements of pennation angle (PA) and muscle thickness (MT) were also conducted weekly.In-vivoactive and passive torque-angle relationships were constructed pre-cast, post-cast, and following 4 weeks of recovery.ResultsFrom pre- to post-cast, young and old rats experienced similar decreases in SSN (–20%,P<0.001), muscle wet weight (–25%,P<0.001), MT (–30%), PA (–15%,P<0.001), and maximum isometric torque (–40%,P<0.001), but there was a greater increase in passive torque in old (+180%,P<0.001) compared to young rats (+68%,P=0.006). Following cast removal, young exhibited quicker recovery of SSN, PA, and MT than old, but SSN recovered sooner than PA and MT in both young and old. Muscle wet weight recovered 90% and active torque fully recovered in young rats, whereas in old these remained unrecovered at 75% and 72%, respectively.ConclusionsThis study showed that old rats retain a better ability to recover longitudinal compared to parallel muscle morphology following cast removal, making SSN a highly adaptable, appealing mechanism for restoration of functional capacity following disuse in elderly populations.

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Section: Age-related Differences In Baseline Muscle Morphologysupporting

confidence: 90%

Age-related differences in the loss and recovery of serial sarcomere number following disuse atrophy in rats

Hinks,

Power

2024

Preprint

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“…Such interaction effects could include, for example, an increase of passive stiffness in relative rather than absolute terms, which has been suggested based on the observation that active contractions become weaker with age while passive muscle properties remain unchanged [56]. Moreover, the increase in passive force could occur with, and be partially caused by, age-related reduction in optimal muscle lengths [29]. Tendons, which affect force transmission and a muscle’s length and velocity trajectory during movements, may also undergo age-related structural changes [57], although the changes in tendon stiffness can be insignificant in the upper limbs [58].…”

Section: Discussionmentioning

confidence: 99%

“…Roughly fitting an exponential function to the passive tension data for muscle fibre bundles from mice [14] and humans [15] suggests an increase in the range of 0–30% in r p . Changes in the optimal muscle length also affect r p , so that, for example, the 14% reduction observed in older mice [29] translates to a reduction of approximately 12% in r p . We chose r p = 5 based on Winters [26] as the lower parameter value and a relatively high 60% increase to r p = 8 to balance out the overall low values compared to those used by Thelen [20] to simulate the effects of ageing on ankle function ( r p ≈ 8 for young and r p = 10 for old muscles).…”

Section: Methodsmentioning

confidence: 99%

The impact of age-related increase in passive muscle stiffness on simulated upper limb reaching

Murtola

Richards

2023

R. Soc. open sci.

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Ageing changes the musculoskeletal and neural systems, potentially affecting a person’s ability to perform daily living activities. One of these changes is increased passive stiffness of muscles, but its contribution to performance is difficult to separate experimentally from other ageing effects such as loss of muscle strength or cognitive function. A computational upper limb model was used to study the effects of increasing passive muscle stiffness on reaching performance across the model’s workspace (all points reachable with a given model geometry). The simulations indicated that increased muscle stiffness alone caused deterioration of reaching accuracy, starting from the edges of the workspace. Re-tuning the model’s control parameters to match the ageing muscle properties does not fully reverse ageing effects but can improve accuracy in selected regions of the workspace. The results suggest that age-related muscle stiffening, isolated from other ageing effects, impairs reaching performance. The model also exhibited oscillatory instability in a few simulations when the controller was tuned to the presence of passive muscle stiffness. This instability is not observed in humans, implying the presence of natural stabilizing strategies, thus pointing to the adaptive capacity of neural control systems as a potential area of future investigation in age-related muscle stiffening.

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“…Muscle fascicle length (FL) becomes shorter with age driven by a loss of in-series aligned sarcomeres (1)(2)(3)(4). This loss of serial sarcomere number (SSN) contributes to muscle atrophy and impaired mechanical function in old age (3,5).…”

Section: Introductionmentioning

confidence: 99%

Submaximal eccentric resistance training increases serial sarcomere number and improves dynamic muscle performance in old rats

Hinks,

Vlemmix,

Power

2024

Preprint

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The age-related loss of muscle mass is partly accounted for by the loss of sarcomeres in series. Serial sarcomere number (SSN) influences muscle mechanical function including the force-length and force-velocity-power relationships, and the age-related loss of SSN contributes to declining performance. Resistance training biased to active lengthening (eccentric) contractions increases SSN in young muscle, however, we showed maximal eccentric training in old rats did not alter SSN and further worsened performance. A submaximal eccentric training stimulus may be more conducive to adaptation for aged muscle. Therefore, the purpose of this study was to assess whether submaximal eccentric training can increase SSN and improve mechanical function in old rats. Twelve 32-month-old male F344/BN rats completed 4 weeks of submaximal (60% maximum) isokinetic eccentric plantar-flexion training 3 days/week. Pre- and post-training, we assessedin-vivomaximum isometric torque at a stretched and neutral ankle angle, the passive torque-angle relationship, and the isotonic torque-angular velocity-power relationship. The soleus and MG were harvested for SSN measurements via laser diffraction, with the untrained leg as a control. SSN increased 11% and 8%, and muscle wet weight increased 14% and 13% in the soleus and MG, respectively. Maximum isometric torque and shortening velocity were unaltered, but there was a shift towards longer muscle lengths for the optimal angle of torque production, a 42% reduction of passive torque, and 23% increase in peak isotonic power. Eccentric training at 60% maximum was beneficial for aged muscle, increasing SSN and muscle mass, reducing muscle passive tension, and improving dynamic performance.New & NoteworthyFour weeks of submaximal (60% of maximum) eccentric resistance training increased serial sarcomere number and muscle mass in old ratsIncreased serial sarcomere number corresponded to broadening of the torque-angle relationship following training, which contributed to increased peak isotonic powerSubmaximal eccentric training also led to a large reduction in passive torque throughout the range of motion

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Age-related reductions in the number of serial sarcomeres contribute to shorter fascicle lengths but not elevated passive tension

Cited by 6 publications

References 36 publications

Age-related differences in the loss and recovery of serial sarcomere number following disuse atrophy in rats

Age-related differences in the loss and recovery of serial sarcomere number following disuse atrophy in rats

The impact of age-related increase in passive muscle stiffness on simulated upper limb reaching

Submaximal eccentric resistance training increases serial sarcomere number and improves dynamic muscle performance in old rats

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