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Velocity dependence of eccentric strength in young and old men: the need for speed! Geoffrey A. Power, Demetri P. Makrakos, Daniel E. Stevens, Charles L. Rice, and Anthony A. Vandervoort

Abstract: Older adults better maintain eccentric strength relative to isometric strength, as indicated by a higher ratio of eccentric:isometric torque as compared with younger adults. The effect of increasing angular velocities (>200°/s) on the agerelated maintenance of eccentric strength has not been tested and thus it is unknown whether the eccentric:isometric ratio is velocity dependent in old age. The purpose of this study was to investigate eccentric strength of the ankle dorsiflexors over a large range of lengthening angular velocities in young and older men. Isometric neuromuscular properties were assessed on a HUMAC NORM dynamometer. Nine young (⬃24 years) and 9 older (⬃76 years) healthy men performed maximal voluntary eccentric contractions at angular velocities of 15–360°/s. Despite near full voluntary activation (>95%), the older men were ⬃30% weaker than the young men for isometric strength (P < 0.05). Across all lengthening velocities, older men had a greater eccentric:isometric ratio than young men (P < 0.05). Additionally, there was a velocity dependence of strength in both young and older men: eccentric strength increased as velocity increased up to 120°/s (P < 0.05) and plateaued thereafter. In young and older men, eccentric strength at 15°/s was ⬃20% and ⬃40% greater than isometric strength (P < 0.05), while at 360°/s eccentric strength was ⬃50% and ⬃90% greater, respectively (P < 0.05). These findings indicate that with increasing angular velocity, both young and older men have considerable increases in the eccentric:isometric ratio of torque production. Key words: aging, muscle, lengthening, residual force enhancement, stiffness, weakness, elderly, EMG. Résumé : Les personnes âgées présentent une plus grande force pliométrique relative a` la force isométrique que les jeunes personnes comme le révèle le ratio plus élevé des moments de force pliométrique/isométrique chez les personnes âgées. Il n'y a pas d'études sur le maintien de la force pliométrique avec l'âge a` des vélocités angulaires supérieures a` 200 °/s; on ne sait donc pas si le ratio des moments de force pliométrique/isométrique est lié a` la vélocité chez les personnes âgées. Cette étude se propose d'évaluer la force pliométrique des fléchisseurs dorsaux de la cheville sur une vaste plage de vélocités angulaires d'étirement chez des hommes jeunes et âgées. On évalue les propriétés neuromusculaires en condition isométrique au moyen d'un dynamomètre HUMAC NORM. Neuf jeunes personnes (⬃24 ans) et neuf personnes âgées (⬃76 ans) en santé effectuent des contractions pliométriques maximales volontaires a` des vélocités angulaires variant de 15 a` 360 °/s. Même en présence d'une activation volontaire presque totale (> 95 %), les personnes âgées présentent ⬃30 % moins de force isométrique que les jeunes personnes (P < 0,05). Sur toute la plage des vélocités angulaires d'étirement, les personnes âgées présentent un plus haut ratio des moments de force pliométrique/isométrique que les personnes jeunes (P < 0,05). De plus, on observe une dépendance de la force par rapport a` la vélocité dans les deux groupes d'âge : la force pliométrique augmente avec la vélocité jusqu'a` 120 °/s (P < 0,05) et présente un plateau par la suite. À la vélocité angulaire de 15 °/s, la force pliométrique des jeunes personnes et des plus âgées est de ⬃20 % et ⬃40 % supérieure respectivement a` la force isométrique (P < 0,05); a` la vélocité angulaire de 360 o/s, la force pliométrique est de ⬃50 % et ⬃90 % supérieure respectivement (P < 0,05). D'après ces résultats, le ratio des moments de force pliométrique/isométrique augmente beaucoup avec la vélocité angulaire chez les personnes jeunes et âgées. [Traduit par la Rédaction] Mots-clés : vieillissement, muscle, étirement, amélioration de la force résiduelle, raideur, faiblesse, personnes âgées, EMG.

Introduction Natural adult aging is associated with many alterations to the human neuromuscular system that contribute to impaired function in old age (Larsson et al. 1997; Vandervoort 2002; Power et al. 2013a, 2014a; Theou et al. 2013). However, age-related reductions in muscle contractile capacity are disparate among contraction modes — that is, among shortening (concentric), static (isometric), and lengthening (eccentric) contractions (Vandervoort 2002; Roig et al. 2010). This discrepancy was first identified by Vandervoort

et al. (1990), who observed that older women had maintained eccentric knee extensor strength to a greater degree than concentric strength as compared with young adult women. The finding of a relative maintenance of eccentric strength was later confirmed in older men, across a variety of muscle groups (Poulin et al. 1992; Hortobagyi et al. 1995; Porter et al. 1997; Cannon et al. 2006; Power et al. 2012, 2013b), and in reduced muscle preparations (Phillips et al. 1991; Ochala et al. 2006, 2007). The maintenance of eccentric strength in old age is ⬃2%–50% greater than concentric strength, with an

Received 5 December 2014. Accepted 26 February 2015. G.A. Power.* Faculty of Kinesiology, Human Performance Laboratory, University of Calgary, Calgary, AB T2N 1N4, Canada. D.P. Makrakos,* D.E. Stevens, and A.A. Vandervoort. Canadian Centre for Activity and Aging, School of Kinesiology, Faculty of Health Sciences, The University of Western Ontario, London, ON N6G 2M3, Canada. C.L. Rice. Canadian Centre for Activity and Aging, School of Kinesiology, Faculty of Health Sciences, The University of Western Ontario, London, ON N6G 2M3, Canada; Department of Anatomy and Cell Biology, The University of Western Ontario, London, ON N6A 3K7, Canada. Corresponding author: Geoffrey A. Power (e-mail: [email protected]). *Shared first authorship. Appl. Physiol. Nutr. Metab. 40: 703–710 (2015) dx.doi.org/10.1139/apnm-2014-0543

Published at www.nrcresearchpress.com/apnm on 3 March 2015.

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average difference of ⬃20% (Roig et al. 2010), although in some cases there is no difference in eccentric strength across age (Power et al. 2012). Furthermore, based on observations in humans, animals, and skinned muscle fiber preparations (Phillips et al. 1991; Ochala et al. 2006, 2007), this age-related maintenance of eccentric strength appears to be an intrinsic property of aged muscle. Mechanisms contributing to the relative maintenance of eccentric strength in old age are not entirely clear, but existing evidence places more of an emphasis on age-related changes to the muscle and connective tissue than on neuromuscular control (see Discussion) (Power et al. 2012, 2013b, 2014b). During active stretch, muscle is characterized by its viscoelastic properties (Hill 1938), and the velocity at which muscle is stretched therefore has implications for the peak force reached during a human voluntary eccentric contraction. Moreover, if age-related changes to the muscle alter these intrinsic mechanical properties, it is reasonable to expect increasing age-related differences in the eccentric: isometric ratio with increasing lengthening velocities. The maintenance of eccentric strength in old age is consistent across a range of angular velocities of lengthening, but to our knowledge the angular velocities tested have not exceeded ⬃200°/s (Poulin et al. 1992; Porter et al. 1997; Klass et al. 2005; Roig et al. 2010). Although some might consider 200°/s to be a fast angular velocity during voluntary shortening, the use of isokinetic dynamometers can allow for much faster angular velocities to stress the mechanical properties during lengthening muscle actions. Pushing the limits of human performance in older adults to characterize the full lengthening force-velocity relationship will add to our understanding of the velocity dependence of eccentric strength in old age. Therefore, the purpose of this study was to determine whether the maintenance of eccentric strength in old age is velocity dependent during lengthening velocities higher than 200°/s. We hypothesized that owing to age-related muscle weakness, older adults will have lower absolute eccentric torque values than young adults at slow lengthening angular velocities but similar torque values at faster angular velocities. When eccentric torque is expressed as a percentage of isometric torque, we expect a greater ratio (eccentric:isometric) for older than young adults across all lengthening angular velocities. Further, owing to increased muscle stiffness in older adults (Ochala et al. 2006, 2007), we expect a greater divergence in the eccentric: isometric ratio at fast angular velocities, supporting a velocity dependence of eccentric strength in old age.

Materials and methods Participants All young and older men (Table 1) were asked to refrain from any unaccustomed or strenuous exercise for 24 h and caffeine consumption for 2 h prior to testing. All participants were recreationally active and free from any known neuromuscular or musculoskeletal disorders. The young adults were recruited from the university population and the older adults from a local seniors' group that includes walking and light calisthenics twice weekly. Participants had been involved in previous experiments in our laboratory and were well familiarized with the procedures and neuromuscular techniques used. This study was approved by The University of Western Ontario Health Science Research Ethics Board and conformed to the principles of the Declaration of Helsinki. Informed written consent was obtained from all participants prior to testing. Experimental arrangement All testing was conducted on a HUMAC NORM dynamometer (CSMi Medical Solutions, Stoughton, Mass., USA). The nondominant foot was fastened tightly to the ankle attachment footplate with nonelastic straps, aligning the lateral malleolus of the ankle with the rotational axis of the dynamometer. Extraneous move-

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Table 1. Participant characteristics and baseline measurements.

Age (y) Mass (kg) Height (cm) MVC (N·m) VA (%) Optimal angle (°)

Young (n = 9)

Older (n = 9)

24.8±3.2 82.7±10.0 180.0±6.9 42.1±8.5 99.2±1.0 27.0±8.3

76.0±5.5* 83.0±9.4 175.3±5.8 29.1±6.7* 99.6±1.3 25.2±9.9

Note: MVC, isometric maximum voluntary contraction; VA, voluntary activation; optimal angle, optimal joint angle of torque production during the lengthening contractions. Values are means and SD. *Significant difference between age groups.

ments were minimized using nonelastic shoulder, waist, and thigh straps. Participants sat in a slightly reclined position with the hip and knee angles of the experimental leg set at 110° and 140° (180° is straight), respectively. All voluntary and evoked isometric dorsiflexion contractions were performed at an ankle angle of 40° of plantar flexion (PF). Lengthening contractions to determine peak torque began at 5° of dorsiflexion (DF) and continued until 45° PF, thus moving through a 50° range of motion. The range of motion was chosen to ensure the participant could reach maximal torque during lengthening, which was particularly important for the fast angular velocities to allow the dynamometer to reach the programmed angular velocity. Electromyography (EMG) Electromyography signals were collected using self-adhering Ag-AgCl surface electrodes (1.5 × 1 cm; Kendall, Mansfield, Mass., USA) in a monopolar configuration to optimize electrically evoked potential recordings. The active electrode was positioned over the proximal portion of the tibialis anterior, and the reference electrode was placed over the distal tendenous portion of the tibialis anterior at the level of the malleoli. The active electrode for antagonist muscles (plantar flexors) was positioned over the soleus 2 cm distal to the lower border of the medial head of the gastrocnemius, and the corresponding reference electrode was placed over the calcaneal tendon. The ground was placed over the patella. Experimental procedures A timeline of the experimental procedures is presented in Fig. 1. Twitch contractions of the dorsiflexors were evoked electrically with a standard clinical bar electrode (Empi, St. Paul, Minn., USA) coated in conductive gel, which was positioned to maximize the compound muscle action potential (M-wave; Mmax) for the purpose of normalizing voluntary EMG and to assess voluntary activations (see below). The anode was positioned anterior and the cathode posterior to the fibular head over the deep branch of the common fibular nerve. A computer-triggered stimulator (model DS7AH, Digitimer, Welwyn Garden City, Hertfordshire, UK) set at 400 V provided the electrical stimulation using a pulse width of 100 ␮s. Peak twitch torque (Pt: 1 Hz) was determined by increasing the current until a plateau amplitude was reached, and then the current was further increased by 15% to ensure activation of all motor axons via supramaximal stimulation. Additionally, Mmax elicited by supramaximal stimulation of the tibial nerve using procedures described above was evoked from the soleus muscle to normalize antagonist EMG. A commercially available clinical stimulating bar electrode was held firmly in the distal portion of the popliteal fossa between the origins of the heads of the gastrocnemii to electrically activate the tibial nerve where it is readily accessible. Following maximal twitch determination, participants performed at least 2 maximum voluntary contractions (MVCs), each for ⬃3 s, separated by 3 min of rest. Voluntary activation was Published by NRC Research Press

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Fig. 1. Experimental timeline.

assessed during the MVCs using the interpolated twitch technique. Participants were exhorted verbally and provided with visual feedback in the form of the torque tracing on a computer monitor. The amplitude of the interpolated twitch torque evoked during the peak plateau of the MVC was compared with the resting Pt evoked 1 s after the MVC, when the muscles were relaxed. Percent voluntary activation was calculated as follows: voluntary activation (%) = [1 – (interpolated Pt/resting Pt)] × 100. In all cases, participants were required and able to reach near full voluntary activation (>95%) before continuing the experiment. Values from the baseline MVC with the highest peak torque are reported and used in the eccentric to isometric comparisons. Prior to MVCs, passive tension was assessed in 10° steps from 0° PF to 40° DF. Lengthening muscle actions Participants performed lengthening contractions at 10 different randomized angular velocities: 15, 30, 45, 60, 120, 210, 270, 300, 330, and 360°/s (i.e., 0.26, 0.52, 0.79, 1.05, 2.09, 3.67, 4.71, 5.24, 5.76, and 6.28 rad/s). Each trial consisted of a maximal isometric pre-activation contraction of ⬃1 s at 5° DF followed directly by a lengthening contraction as the dynamometer moved at the programmed angular velocity through the range of motion, ending at 45° PF. Participants were strongly encouraged verbally for both the isometric and eccentric portions of the contraction and were provided with visual feedback in the form of the torque tracing on a computer monitor. One minute of rest was given between contractions, and participants were allowed to retry a velocity if they did not consider the contraction to be a maximal effort. Residual force enhancement To investigate the influence of angular velocity on the previously observed elevated residual force enhancement (RFE) in older adults (Power et al. 2012), a subset of participants (5 young and 5 old) performed additional experiments. The protocol used to determine RFE, described previously in detail (Power et al. 2012), involved a 10-s isometric reference MVC at 40° PF followed by 3 min of rest. The dorsiflexors were then voluntarily activated maximally for 10 s, beginning with a 1-s isometric contraction at the starting muscle length (0° PF), followed by a lengthening contraction at either a slow (15°/s) or fast (120°/s) angular velocity, performed randomly, and ending with an isometric contraction at the same angle as the 10-s reference MVC (40° PF) (Fig. 1). After 5 min of rest, this procedure was repeated. To calculate RFE, we determined the mean torque value over 1 s during the isometric

steady state at 6–8 s after initial activation (0 s) of the muscle, which corresponded to the period of minimal torque fluctuations. The value for the steady-state MVC following the end of lengthening was then divided by the mean torque value for the reference MVC at the same time point. Residual force enhancement was defined as the percent increase in isometric torque following lengthening during the isometric steady state, relative to the reference MVC. To ensure RFE was not influenced by fatigue or muscle damage, an additional MVC was performed at the end of each experiment, and if peak torque was reduced by more than 10% compared with the MVC performed at the beginning of the experiment, that trial was removed from analysis. Three minutes of rest were given after the end of the RFE protocol and at the beginning of the lengthening muscle actions. Data analyses Torque, velocity, and position channel information was sampled at a rate of 2500 Hz and converted to digital format using a 12-bit analog-to-digital converter (model 1401 Power, Cambridge Electronic Design, Cambridge, UK). Peak torque during the lengthening contraction trials was required to occur while the dynamometer arm was moving at the programmed velocity. At higher velocities, acceleration and deceleration of the dynamometer occupied a larger portion of the contraction range; if peak torque occurred during either of those phases, it was disregarded, and peak torque at the programmed velocity was used instead. Relative peak torque was calculated as follows: [(eccentric torque/ MVC torque) – 1] × 100. Once the peak torque was determined, the position channel was used to determine the ankle angle at which peak torque had been achieved (Fig. 2). Surface EMG signals were pre-amplified (×100), amplified (×2), band-pass filtered (10–1000 Hz), and sampled at 2500 Hz using Spike 2 software (version 7.07, Cambridge Electronic Design). The EMG was measured as root mean square amplitude (EMGRMS) for both the tibialis anterior and soleus. For analysis of EMG during lengthening, 0 s represented the start of lengthening, such that negative time was during the MVC prior to lengthening and positive time was during the lengthening phase. The time intervals (in seconds) chosen for analysis were as follows: –0.5 to 0.0, 0.0 to 0.18, and 0.0 to the time peak torque was achieved. For some of the faster velocities, 0.18 s represented a greater portion of the lengthening contraction, whereas for the slower velocities this time interval represented a smaller portion (Fig. 2). Published by NRC Research Press

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Fig. 2. Raw data of typical torque, velocity, and position traces indicating the windows in which torque and electromyography (EMG) signals were analyzed. (A) 30°/s, (B) 120°/s, and (C) 330°/s. Cursors 1, 0, 2, and 3 represent 0.5 s before onset of lengthening, onset of lengthening, 0.18 s after onset of lengthening, and peak torque, respectively.

Statistical analysis SPSS software (version 20, SPSS Inc., Chicago, Ill., USA) was used for all statistical analyses. A one-way analysis of variance (ANOVA) was performed to assess baseline neuromuscular function of the young and older adults. A repeated-measures ANOVA was performed on “age” and “velocity” to compare eccentric peak torque values between young and older men across the isometric MVC and 10 lengthening velocities. A repeated-measures ANOVA was also performed on “age” and eccentric:isometric torque ratios across “velocity”. When significance was observed for velocity, a post hoc analysis using paired t tests was performed with a Bonferroni correction factor to determine where the significant differences existed. Voluntary activation values were not normally distributed, and thus a Mann–Whitney U test was employed for this particular variable. The level of significance for all tests was set at P < 0.05. Data in tables and text are presented as the mean ± SD, and data in figures are the mean ± SE.

Results Baseline The older adults were ⬃31% weaker than the young adults for MVC (P < 0.05), despite similar high levels of voluntary activation (Table 1) and EMGRMS amplitude (P > 0.05). Although there was a trend for elevated passive tension at 0°, 10°, 20°, and 30° PF, it did not reach statistical significance until 40°, at which point passive tension in the older group was elevated ⬃33% compared with the young group (P < 0.05; Table 2). Age-related maintenance of eccentric strength An Age × Velocity interaction (P < 0.001, ␩p2 = 0.17) was found for absolute peak torque during active lengthening. Peak torque during lengthening was ⬃20% higher for the young men as compared with the older men for 15–45°/s (P < 0.05). As angular velocity was increased to 60°/s, the difference in strength was no longer present and there were no age-related differences in absolute peak Published by NRC Research Press

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Table 2. Dorsiflexor passive tension. Ankle angle (°PF)

Young

Older

0 10 20 30 40

0.0±0.0 8.8±2.1 12.7±3.2 15.3±3.6 18.7±3.9

0.0±0.0 9.8±4.3 14.1±5.8 18.0±5.7 24.8±6.7*

Fig. 3. Absolute peak torque during dorsiflexor lengthening over 10 angular velocities. Values are means ± SE. *, Significant difference across velocity (0–120°/s) as compared with 360°/s (P < 0.05); †, significant difference between age groups (P < 0.05).

Note: Means are normalized to zero and represent the percentage of MVC torque. Values are means and SD. PF, plantar flexion. *Significant difference between age groups.

eccentric torque (P > 0.05; Fig. 3). Peak torque during lengthening continued to increase up to 120°/s and plateaued thereafter. Upon normalizing peak torque during lengthening to the isometric MVC (eccentric:isometric), there was an Age × Velocity interaction (P < 0.001, ␩p2 = 0.29): the older adults showed a greater eccentric: isometric ratio across all angular velocities (P < 0.05) as compared with the young adults. The eccentric:isometric ratio increased for both young and older men up to 210°/s and plateaued thereafter (Fig. 4, Table 3). There was no significant difference between older and young men for the ankle angle at which peak torque during lengthening was achieved (P > 0.05; Table 1). As well, there were no interaction (Velocity × Age; P = 0.47, ␩p2 = 0.07) or significant main effects across age or velocity for EMGRMS of the agonist or antagonist co-activation (P > 0.05; Fig. 5).

Fig. 4. Peak torque during dorsiflexor lengthening as a percent increase from isometric torque (ECC:ISO), over 10 angular velocities. Values are means ± SE. *, Significant difference (15–210°/s) across velocity as compared with 360°/s (P < 0.05); †, significant difference between age groups (P < 0.05).

Steady-state torque following lengthening Torque values were significantly higher in the isometric steadystate phase following lengthening as compared with the isometric reference for both young and older men, and values did not differ between fast (120°/s) and slow (15°/s) lengthening contractions (P > 0.05), suggesting there is no velocity dependence of RFE in old age (i.e., interaction: Age × Velocity; P = 0.32, ␩p2 = 0.09). Thus, data were pooled for the RFE analysis. Residual force enhancement, when expressed as the percent difference in the isometric steady state compared with the purely isometric reference contraction, was elevated in the older men as compared with the young men (P < 0.05; Fig. 6).

Discussion In accordance with our hypothesis, the older and young adults had similar levels of eccentric strength at faster lengthening velocities (i.e., above 45°/s). Additionally, when eccentric strength was expressed as a percentage of isometric strength, older adults had a higher eccentric:isometric ratio across all lengthening velocities as compared with young adults. In both young and older adults, the eccentric:isometric ratio increased with increasing velocity before reaching a plateau (>120°/s). Thus, older adults appear to have a velocity dependence of absolute eccentric strength (no age-related differences above 45°/s). Although older adults have a higher eccentric:isometric ratio across all lengthening velocities, both young and older adults show increases in the eccentric:isometric ratio with increasing angular velocity. In the present study, all participants were capable of near full voluntary activation (Table 1) of the ankle dorsiflexors, and tibialis anterior EMGRMS amplitude during active lengthening was not different across age or velocity. Furthermore, soleus antagonist coactivation was not different across either age or velocity (Fig. 5). These findings indicate that neural activation (i.e., as assessed with surface EMG) is not limiting in either age group during isometric or lengthening contractions for this particular muscle group, which is in line with a similar investigation that found no difference in tibialis anterior activation (EMG) between old and young adults or across lengthening velocities (Klass et al. 2005). In the present study, we show that in addition to no change in the agonist EMG, there was no

Table 3. Confidence intervals for eccentric: isometric torque ratio (%) across velocities. Angular velocity (°/s)

Young (%)

Older (%)

15 30 45 60 120 210 270 300 330 360

12.0, 22.9 15.6, 30.1 18.1, 37.0 24.1, 35.7 24.3, 45.6 28.5, 49.0 30.5, 50.8 33.4, 55.7 29.7, 54.2 36.3, 61.5

31.5, 42.4 36.3, 50.8 38.7, 57.5 54.4, 66.0 59.3, 80.7 69.5, 90.0 72.9, 93.2 76.3, 98.7 73.2, 97.7 76.0, 101.1

difference in antagonist co-activation across age or velocity. These findings are important because increased antagonist co-activation will decrease overall net joint torque and bias the isometric reference contraction, thus potentially elevating the eccentric:isometric ratio. Published by NRC Research Press

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Fig. 5. Electromyography (EMG) values for agonist (solid lines) and antagonist activation (dashed lines) during isometric and lengthening contractions. The black and gray lines represent the EMGRMS amplitude during isometric contraction prior to lengthening and during active lengthening, respectively, through the whole range of motion (A; controlling for range of motion) and for the first 0.18 s of lengthening (B; controlling for duration of lengthening).

Fig. 6. Residual force enhancement (RFE) expressed as a percent increase in isometric steady-state torque relative to the purely isometric reference contraction. Torque values were significantly higher in the isometric steady-state phase following lengthening as compared with the isometric reference contraction for both young and older adults and did not differ between fast (120°/s) and slow (15°/s) lengthening contractions, suggesting there is no velocity dependence of RFE in old age. Thus, data were pooled for the RFE analysis. Residual force enhancement was elevated in the older adults as compared with the young. The young adults are represented by the black bar and the older adults by the gray bar. Values are means ± SE. *, Significant difference between age groups (P < 0.05).

The age-related increase in the eccentric:isometric torque ratio across a wide range of lengthening angular velocities that was observed in the present study is consistent with the literature. For ankle dorsiflexors, Klass et al. (2005) showed that the eccentric: isometric torque ratio at 100°/s was ⬃10% higher in older adults than in young adults. In the same muscle group, Hasson et al. (2011b) measured eccentric torque at faster velocities (up to 200°/s) in older adults and found a 40% increase relative to isometric torque. In the present study, the eccentric torque at 200°/s was 75% higher than isometric torque for the older group. Thus it seems that our results for the age-related effect of velocity are more pronounced than those in other studies. The elevated torque during lengthening may be due to the imposed pre-activation in the present study, which is known to increase torque during lengthening (Baudry et al. 2007). Another factor that may account for the higher values in the present study is the range of motion used. The ankle dorsiflexors were actively lengthened to 45° PF. Older adults present significantly higher passive tension than young adults following a 30° range of motion (Table 2). Passive tension of the muscle group increases with age as a result of an increase in connective tissue in either the parallel or series elastic component (Alnaqeeb et al. 1984; Kent-Braun et al. 2000; Hasson et al. 2011a). We can assume the increase in passive tension observed in the older men was due to the increase of noncontractile elements and their contribution to the larger viscoelastic effect during stretch that older adults would experience at long muscle lengths as compared with young adults (Power et al. 2013b). Therefore, the stretch amplitude in the present study may have allowed the older men to benefit from the passive force generating capacity at longer muscle lengths to achieve higher eccentric torque values. However, this on its own would not explain the increasing age-related divergence in the eccentric:isometric ratio at faster velocities. The maintenance of eccentric strength in older adults can be attributed to either neural or mechanically mediated mechanisms, Published by NRC Research Press

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or both (Roig et al. 2010). The neural factors discussed above are not altered with aging (Phillips et al. 1992; Roos et al. 1999; Jakobi and Rice 2002; Klass et al. 2005), and therefore it is most likely that noncontractile and structural properties intrinsic to the muscle tissue are contributing to the maintenance and velocity dependence of eccentric strength observed in the ankle dorsiflexors in the present study. Support for an intrinsic muscle property leading to maintained eccentric strength is the elevated force following a quick active stretch in single muscle fibers of older adults. The elevated force following stretch is suggested to be related to an increased number of weakly bound cross-bridges, which would contribute to passive tension during stretch but not during active force production (Ochala et al. 2006). As well, instantaneous stiffness (Ochala et al. 2007) measured from maximally activated single skinned muscle fibers taken from older adults was greater than that measured from fibers taken from younger adults. Furthermore, the age-related slowing of cross-bridge kinetics, specifically the slowed detachment rate of myosin (Miller et al. 2013), may provide greater resistance to stretch, which would allow older adults to develop higher forces during eccentric muscle actions as compared with isometric actions. Moreover, in intact humans, it was observed that reduced contraction duration of an electrically evoked twitch was associated with an age-related maintenance of eccentric strength (Cannon et al. 2006). Together, these findings provide evidence of altered elastic, structural, and cross-bridge properties of the muscle being partly responsible for the maintenance of eccentric strength, although the precise contributions of the various potential mechanisms are unknown. To investigate additional potential steady-state mechanisms that might explain the velocity dependence of the age-related maintenance of eccentric strength, RFE experiments were performed in a subset of participants (for additional information on RFE please see Seiberl et al. 2015). Despite the clear velocity dependence of eccentric strength, RFE values were similar for the fast and slow conditions. In agreement with previously reported findings for this muscle group (Power et al. 2012), older adults experienced higher RFE values as compared with young adults. However, the novel finding here is that RFE is indeed independent of velocity in old age, which agrees with the basic proposed mechanisms of RFE (Abbott and Aubert 1952). Therefore, some of the mechanisms associated with elevated RFE in old age may also contribute to the greater eccentric:isometric ratio. However, there are velocity-dependent mechanisms contributing to the maintenance of eccentric strength in old age that cannot account for elevated RFE. Therefore, there are likely different mechanisms contributing to the elevated steady-state RFE and the dynamic (transient) maintenance of eccentric strength observed in older adults as compared with young adults. Eccentric torque values were measured up to lengthening angular velocities of 360°/s in both young and older adults. It was observed that older men showed a contraction-dependent maintenance of strength (e.g., eccentric) and that eccentric strength, when expressed as a percentage of isometric strength, was indeed higher in older men than in young men. Eccentric strength increased in a velocity-dependent manner, plateauing at fast velocities (>120°/s) in both young and older men. The age-related difference in the eccentric:isometric ratio cannot be explained by peripheral measures of neural activation, as the EMGRMS amplitude of the agonist and antagonist muscles did not change in either young or older men as the velocity increased. Thus, the elevated eccentric:isometric ratio in older men is most likely due to age-related structural changes to the musculotendinous unit. These findings shed new light on the plasticity of the aged neuromuscular system and indicate that fitness interventions could take advantage of the considerable preserved performance seniors have during lengthening (eccentric) contractions.

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Conflict of interest statement The authors have no conflicts of interest to disclose.

Acknowledgements The authors would like to thank all those who participated in the study. This research was supported by funding from The Natural Sciences and Engineering Research Council of Canada (NSERC). G.A. Power was supported by a Banting postdoctoral fellowship (Canadian Institutes for Health Research; CIHR) and Alberta Innovates Health Solutions (AIHS).

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Velocity dependence of eccentric strength in young and old men: the need for speed!

Older adults better maintain eccentric strength relative to isometric strength, as indicated by a higher ratio of eccentric:isometric torque as compar...
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