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Decreases in motor unit firing rate during sustained maximal-effort contractions in young and older adults
Journal of Electromyography and Kinesiology 15 (2005) 536–543 www.elsevier.com/locate/jelekin
Decreases in motor unit firing rate during sustained maximal-effort contractions in young and older adults Scott Rubinstein, Gary Kamen
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Department of Exercise Science, University of Massachusetts – Amherst, Amherst, MA 01003, United States Received 8 October 2004; received in revised form 22 April 2005; accepted 27 April 2005
Abstract Previous studies have suggested that older adults may be more resistant to muscular fatigue than young adults. We sought to determine whether motor unit firing rate might be a factor that determines the response to fatiguing exercise in young and older subjects. Motor unit recordings and muscular forces were obtained from the tibialis anterior (TA) muscle of 11 young and 8 older individuals. Maximal voluntary force was first measured during maximal-effort dorsiflexion contractions. Each subject then performed a series of 15 maximal isometric contractions, with each contraction lasting 30 s. A 10-s rest period separated the fatiguing contractions. As a result of the fatiguing exercise, both subject groups demonstrated a significant loss in maximal force. The force decline was less in the older adults (20.4%) than in the young adults (33.8%). As expected, prior to muscle fatigue, maximal firing rates in the TA muscle were greater in the young (28.1 ± 5.8 imp/s) than in the older adults (22.3 ± 4.8 imp/s). The decrease in motor unit firing rate with fatigue was also greater in the young adults (34.9%), than in the older adults (22.0%). These results suggest that the greater fatigue-resistance exhibited by older individuals might be explained by the fact that the decline in motor unit firing rate during fatigue is greater in young persons than it is in older adults. 2005 Elsevier Ltd. All rights reserved. Keywords: Aging; Exercise; Muscle; Fatigue; Tibialis anterior
1. Introduction It is well documented that human muscular force production and muscle contractile characteristics exhibit significant decrements with age. Maximal voluntary contractile force (MVC) in persons over 60 years is more than 25% lower than MVC force in young adults in several different muscles, including adductor pollicis [46], knee extensors [41], tibialis anterior [17], and biceps brachii [1]. Such reductions in strength can be due to a decrease in the number of active motor neurons [60] and consequently a loss in the number of active MUs [14], particularly affecting type II motor units [3,39,61]. Sur*
Corresponding author. Tel.: +1 413 545 0784; fax: +1 413 545 2906. E-mail address: [email protected] (G. Kamen). 1050-6411/$ - see front matter 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2005.04.001
viving fast-twitch fibers become reinnervated by slower, type I neuronal axon branches [35] and ultimately exhibit similar physiological characteristics of slow twitch MUs [13], mainly the inability to produce large twitch forces. Consequently, there is a linear increase in the percentage of type I fibers with age [39]. Because there is an overall decline in total muscle fiber numbers, particularly the larger type II fibers, there is an overall loss in muscle cross-sectional area [11], a main contributor to muscle force production. However, the influence of muscular fatigue on older adults is much less clear. While several studies indicate that fatigue resistance is similar in young and older adults [5,41,58], a number of reports (cf. [2]) now suggest that in tasks involving muscular endurance, older adults are actually less susceptible to fatigue than young individuals [15,18,31,38,46]. Thus, in contrast to the known
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decrements in muscular force in older adults, age-related differences in endurance present a more equivocal picture. Though a considerable portion of the decline during muscular exertion is attributed to peripheral changes or impairments in muscle [30,44], there are also central nervous system (CNS) components that impact the fatigue process. There are numerous influences on the motoneuron and potential changes in motoneuron intrinsic properties and these have been studied by assessing motor unit firing rate during fatiguing exercise. In young adults, fatigue is known to produce a decrease in motor unit firing rate in maximal voluntary contractions [6,7,45], though exceptions have been noted in some muscles [42]. Occasionally, it is possible that motor units cease firing altogether [51]. At low levels of force, firing rates are similar among young and older adults [24,29,57]. However, at maximal force levels, firing rates in the elderly have been shown to be significantly slower compared to the young subjects [17,29,49]. Moreover, we have no information on the potential change in motor unit firing rate in older adults following fatiguing exercise. Thus, the question of whether older adults fatigue less than young adults during prolonged exercise is equivocal, and the mechanism for such a phenomenon is unknown. Consequently, we sought to measure and compare changes in motor unit firing rate following a regimen involving fatiguing exercise in young and older individuals.
2. Methods All participants attended one recording session where they were required to sustain 15 maximal dorsiflexion contractions separated by periods of muscle relaxation. Subjects were allowed to monitor their force production on a computer video screen during each contraction and throughout the course of the entire recording session.
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2.2. Motor unit recordings Muscle fiber action potentials were recorded from the tibialis anterior muscle in a manner similar to that reported in previous studies [28,29]. A 25-gauge stainless steel cannula containing four 50 lm platinum–iridium wires was inserted into the tibialis anterior muscle. Three-channel recordings were obtained from the four wires. In our experience, multi-channel recording is essential since single-channel recordings can produce inaccurate identification of muscle fiber action potentials, particularly at greater forces (Fig. 1). The muscle fiber signals were amplified (Dantec Counterpoint Electromyograph; Dantec Electronik Medicinsk, Skovlunde, Denmark; gain 500· typ; bandpass 1–10 kHz), viewed on a digital oscilloscope (Gould 2608, Thermo Electron Corporation, Valley View, OH), and digitized (microcomputer-based WIN-30 data acquisition board, United Electronics, Watertown, MA; Dasylab software; 25.6 kHz sampling rate). Individual action potentials were also viewed on a computer monitor through an oscilloscope module in DASYLab software (Data Acquisition System Laboratory (DASYLab), DasyTec USA, Inc., Amherst, NH). 2.3. Muscular force Isometric dorsiflexion force was measured using a strain gauge force transducer (Interface model MB10, Scottsdale, AZ) mounted to a custom-designed metal apparatus. The force signal was amplified (500·) using a custom-built bridge amplifier, digitized (50 Hz; Data translation DT2801A/D converter, Marlborough, MA), and presented to the subject on a computer monitor for force feedback. Muscular force was concurrently sampled at 25.6 kHz (WIN-30) and later downsampled at 50 Hz for analysis.
2.1. Subjects Subjects consisted of 34 young women (18–30 years; mean age: 19.2 years) and 12 older women (>69 years, mean age: 73.1 years). Each participant completed a Physical Activity Readiness Questionnaire (PARQ [55]) and were screened for any neuromuscular, sensorimotor, and cardiopulmonary disorders and/or injuries. All participants were engaged in moderate levels of daily physical activity (3–5 days/week) and each person refrained from any physically abnormal and/or strenuous activity 24 h prior to her participation. All procedures were approved for human subject participation by the institutional review board. Participants provided written informed consent.
Fig. 1. Multi-channel recordings are critical to ensure correct identification of muscle fiber action potentials, particularly at higher forces. Signals for three channels and two motor units are illustrated. On channel 1, the signals from two motor units are virtually identical. However, the addition of two other recording channels reveals that these comprise distinct signals from two different motor units.
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2.4. Procedures Subjects were seated in a custom-built apparatus designed to measure ankle dorsiflexion in the dominant leg (Fig. 2). Limb dominance was assessed by asking each subject which leg they would use to kick a ball. Hip and knee angles of 90 were maintained and the ankle was set at 20 of plantarflexion as this angle allows maximum dorsiflexion force to be produced [63]. A Velcro strap was secured over the mid-portion of the subjectsÕ dominant thigh while belts were fastened around the subjectÕs waist and chest to isolate the dorsiflexion contraction. Anteroposterior and mediolateral movements of the ankle and knee joints were restricted using foam braces. The subjects were required to sit with their arms folded across the waist to ensure consistent posture across subjects. Subjects performed four maximal voluntary contractions (MVCs; 3–4 s duration) of the dominant dorsiflexors. Individuals were asked to reach their maximal force within about 1–2 s so as not to produce any fast, jerking movements. A two-minute rest was provided between contractions and the highest value was used as their MVC for force-feedback displays during the remainder of the experiment. The needle electrode was inserted into the TA muscle approximately half-way between the tibial tuberosity and the lateral malleolus and at an approximate 30 angle. The proper position of the needle was determined by the presence of high frequency motor unit activity at 20– 30% MVC as assessed by action potentials on the digital oscilloscope and by high frequency audible cues from the differential amplifier and speaker. The needle depth
varied in different subjects; the most important consideration was a location from which stable recordings could be obtained. 2.5. Fatiguing protocol The fatiguing protocol consisted of 15 intermittent MVC isometric contractions, each requiring a 30-s dorsiflexion contraction followed by a 10-s rest period. Instructions to contract and relax were provided by voice cues from a tape recording. Subjects viewed a computer monitor which provided feedback regarding the requisite force level. The researcher provided verbal encouragement throughout the entire 30-s contraction. 2.6. Data analysis During each contraction, muscular force was obtained as the average force produced during the 3 s interval following the maximum force produced within the first 10 s of each contraction. Due to changes in the position of the needle electrode, the task of recording muscle fiber action potentials during each of the 15 contractions proved to be technically difficult. Consequently, we analyzed the firing rates of motor units that were identified during the first and last contractions by computing the mean interfiring interval (IFI) for all accurately identified MU trains in the 3 s block following maximum force. A customized algorithm was used to identify individual motor unit action potentials. This algorithm included both an automatic routine as well as software that displayed the signals and relevant firing statistics
Fig. 2. Apparatus used to measure ankle dorsiflexion.
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on computer monitors. The process included detection using signal threshold measures, and classification using least squares identification based upon template matching. The routine is modified from the algorithm reported by LeFever and colleagues [40]. Though distinct motor unit trains could be classified with over 90% accuracy by the custom software automatically, trained operators reviewed the motor unit signals to correct any misidentifications. Motor unit action potential trains in which identification was uncertain due to difficulties in template matching were not included for analysis. A separate algorithm was used to algebraically resolve superpositions into constituent action potentials. The superposition algorithm requires alignment with the highest peak in the signal waveform, and subtraction of known motor unit templates. A least squares criterion is used to identify two or more motor unit templates with minimal signal residual error. The accuracy of this motor unit identification technique has been demonstrated in earlier studies [27,29,48,49]. Motor units occasionally fire in doublets – two firings with a short interpulse interval less than 10 ms [22]. Among the motor units used in this study, six such doublets were observed and these were included in the analysis. The interfiring interval between two discharges may also be abnormally long (>150 ms) and these are generally due to technical difficulties in identifying motor unit activity, though it is also possible that there are brief pauses in motor unit activity [51]. These elongated IFIs were not included in the calculation of the mean motor unit discharge rate.
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Fig. 3. (Top) Mean (±SD) dorsiflexion force (N) for each of the 15 contractions. The mean force was computed for a 3 s period following the peak force occurring within the first 10 s of each MVC. Older adults had smaller absolute MVC values than the young adults. Both age groups demonstrate significant losses in muscular force (bottom). Percentage of mean force during the 3 s block in Contraction 1 for all 15 contractions.
2.7. Statistical analysis The mean isometric dorsiflexion force was compared between age groups and across all 15 MVCs using a two-factor (2 groups by 15 contractions) repeated measures analysis of variance (ANOVA), with the 15 contractions as a repeated measure. Orthogonal polynomial comparisons were used to further test for significant trends in force reduction [66]. A repeated measures ANOVA compared mean firing rate (impulses/s) between age groups and pre- and post-fatigue (contractions 1 and 15). TukeyÕs honestly significant difference (HSD) test determined any significant paired contrasts.
3. Results 3.1. Muscular force Fig. 3 shows the decrease in maximal force capability in both young and older adults during the fatiguing exercise protocol. Trial 1 scores revealed that baseline muscular force was significantly greater in young adults
than in older adults (p < 0.05). Both age groups demonstrated a significant loss in maximal dorsiflexion force throughout the 15 contractions (p < 0.001). Though older adults had significantly lower absolute MVC values as compared to the younger adults (Fig. 3(a); p < 0.05), older adults displayed a significantly smaller loss in their normalized MVC across the 15 contractions (20.4% decrease) compared to the younger adults (33.8% decrease; p < 0.001). Orthogonal polynomial comparisons showed that the significant age by contraction interaction was due to differences in the linear component (p < 0.01). No significant higher-order polynomial comparisons were obtained. Thus, a straight-line fit best described the loss in force over the 15 contractions for both subject groups. Fig. 3 (bottom) displays force loss as a percentage of the mean force value produced in the first contraction. 3.2. Motor unit firing rates Under non-fatiguing conditions, it can be technically difficult to record individual motor unit action
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Fig. 4. Motor unit firing rates (mean ± SD) in the tibialis anterior muscle in young and older adults. During the first contraction, older adults had slower firing rates than the young adults. Both age groups experienced significantly slower MU firing rates as a result of the fatiguing exercise. However, a greater decline in MU firing rates was observed in the young adults than in the older adults (statistical symbols – *, p < 0.05; , p < 0.01).
potentials at maximal force levels. During fatiguing conditions, this difficulty was compounded by changes in the intramuscular milieu which produced a low-pass filtering effect on the signals, exacerbating the difficulty of identifying single motor unit potentials. Consequently, the final data set consisted of 11 young and 8 older adults. Both force and firing rate statistics were obtained from these subjects. The motor unit sample included a total of 70 motor units, 39 MUs from the young adults, and 31 MUs from the older adults. Under non-fatiguing conditions, older adults exhibited significantly slower MU firing rate (22.3 ± 4.8 imp/s; mean ± SD) than did the young adults (28.1 ± 5.8 imp/s; Fig. 4; p < 0.05). Both age groups experienced significant reductions in MU firing rate between contractions 1 and 15 (p < 0.001). Following the fatiguing exercise, the decrease in MU firing rate was more pronounced for the young adults (34.9%) than for the older adults (22.0%). Although there was no significant two-way interaction (p = 0.12), TukeyÕs HSD test revealed that MU firing rates between the two subject groups were not significantly different at the fifteenth contraction (p > 0.05). Thus, there was a substantial difference in the MU firing rate response of the two groups, with the young subjects demonstrating a somewhat greater decline in firing rates during the fatiguing exercise than the older adults.
4. Discussion The purpose of the current study was to provide the first experimental assessment of changes in motor unit behavior after a maximal-effort fatiguing exercise of the tibialis anterior muscle in women younger than 30 and older than 69 years of age. Such an observation
may help explain the central nervous systemÕs role in fatigue, specifically addressing why older adults have been shown to be less fatigable during maximal-effort contractions [18,8,31] . Indeed, these data confirm earlier reports suggesting that older adults have more fatigue resistance than do younger individuals. During the fatiguing exercise task, force output in the older adults declined by 20%, while young subjects lost 34% of their maximum contractile force. These changes in force were matched by similar declines in motor unit firing rate in both groups. At the end of the exercise, firing rates in the young subjects declined by 35%, while firing rates in older adults declined 22%. As mentioned in Section 1, there are some studies that have failed to note any differences in fatigability due to age [5,41,58]. It is possible that one of the differences among the earlier fatigue studies is activity level. In the present study, we recruited active older adults, whose activity level was similar to that of the young adults. It is possible that those studies that have found no difference due to age may not have accounted for activity level. At least one report suggests that active individuals demonstrate greater resistance to fatigue than sedentary individuals [37]. The magnitude of force change due to the fatiguing exercise is similar to that observed in previous investigations. When subjects were asked to hold a fatiguing submaximal contraction as long as possible, post-fatigue force values decreased by approximately 25% in biceps brachii [16,21], 30% in triceps brachii [23], and 35% in first dorsal interosseus [67]. During sustained maximal efforts, force declined by approximately 40% during a one-minute dorsiflexion contraction [4]. Lanza et al. [38] reported almost identical fatigue-related reductions in maximal force for both young and older men for the TA muscle. In similar studies using intermittent muscle contractions, researchers have frequently reported that most of the force decline occurs in a linear fashion. However, high-strength individuals frequently exhibit an initial steep decline in force resulting in a quadratic polynomial component in the fatigue curve [26,34]. On a relative basis, high-strength subjects (both men and women) demonstrate greater declines in force than do low-strength subjects [32,33]. Similarly, fast-twitch motor units fatigue faster than slow-twitch motor units [59], and the greater proportion of slow-twitch motor units in the older adults would provide more fatigue-resistance. Thus, it is not altogether surprising that the high-strength young adults would exhibit greater endurance than the lower-strength older adults. The firing rates observed in the tibialis anterior muscle (young – 28 imp/s; older – 22 imp/s) are comparable to those reported previously. Bigland-Ritchie et al. [10] reported a maximal firing rate of 28 imp/s, and Van Cutsem et al. [62] reported maximal discharge rates of
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33 imp/s in the tibialis anterior. Although we reported somewhat higher values earlier [48], this is likely due to the choice of metric for computing maximal firing rate. Using scores obtained from the shortest five consecutive interpulse intervals, we previously reported firing rates of 60 imp/s for young subjects, 44 imp/s for older adults [48]. In the present investigation, we computed firing rates over the first three seconds following the attainment of maximal force. Several laboratories have now consistently reported lower motor unit discharge rates in older adults than in young adults [17,29], though some exceptions have been noted [54]. There are several possible explanations for age-related decreases in firing rate. It is possible that there are some disruptions in the quality of the descending command that impact maximal motor unit firing rate. Using transcranial magnetic stimulation, Peinemann et al. [50] observed an age-related decrease in the excitability of intracortical inhibitory pathways, and these intracortical pathways may be important in organizing the final command to motoneurons. There is also a loss in the numbers of descending corticospinal neurons [19], and this could also account for decreases in maximal firing rate. Synaptic transmission from spindles is altered in aged cats [12], resulting in diminished la drive to the motoneuron pool. The density of synaptic input to the motoneuron pool is also diminished in aged rats [36]. Any or all of these factors could be important in determining maximal firing rate, however, the exact mechanism through which motor unit firing rates decline with age remains to be determined. Motor unit firing rate significantly decreased in both age groups across the current protocol, and this is in agreement with other MVC fatiguing protocols in the adductor pollicis [6] and biceps brachii muscle [9] where age-related differences were not compared. The effect of afferent feedback altering central drive to the muscle is speculated to reduce MU firing rate. While ischaemic conditions reduce the peripheral force-generating capabilities during a sustained MVC [9], MU firing rate also remains depressed during blood occlusion. Bigland-Ritchie et al. [9] posited a reflex mechanism elicited by metabolic byproducts in fatigued muscle that might lead to a reduction in MU firing rate. The tibialis anterior muscle is composed mostly of type I, slow-twitch fibers, particularly in older adults [25,52]. Anaerobic metabolism used by type II fibers can raise the [H+] within a muscle fiber during prolonged activity, especially during maximal-effort isometric conditions where blood flow is occluded. As a result, a muscle with a greater proportion of type II fibers would be more likely to induce an inhibitory afferent reflex. In the event that some motor neurons completely cease firing during fatigue, it would most likely be due to the corresponding muscle fibers that have lost the ability to generate force. Because type I muscle fibers are aerobic, older muscle
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may be less likely to elicit metabolic feedback inhibition during a sustained muscle task. It is also possible that motor unit discharge rates decline with fatigue as a compensatory mechanism to match the fatigue-related changes in muscle fiber contractile properties. Such a mechanism is called muscular wisdom [43]. Muscular wisdom could also explain the decline in maximal firing rates observed in older adults [17,29], since a slowing of contractile properties occurs in older muscle [64]. As fatigue ensues, older adults already have slower contraction duration and halfrelaxation times, and might not benefit very much from a fatigue-induced slowing of firing rate to match the already slow contractile properties. Young adults, however, might be able to delay fatigue by slowing motor unit firing rates to match changes in contractile properties. As indicated above, the decrease in firing rates could also be caused by reflex inhibition produced by group III–IV afferents [20], however, there is little data on the characteristics of slow-conducting afferents in older adults. In general, the responses produced by small afferents are diminished with advancing age [47,53, 56,65], and if the responses of group III–IV afferents decrease with age, this could also account for a greater fatigue-related slowing of firing rates in young adults than in older individuals. In summary, we concur with previous observations made during fatiguing contractions, in demonstrating that fatiguing exercise produces a relatively greater force loss in young subjects than in older subjects. The data regarding motor unit firing rates provide further support for a lowering of maximal motor unit firing rate in older individuals. Finally, we conclude that the loss of force following fatiguing exercise in both young and older subjects is accompanied by a proportional decrease in motor unit firing rate; the decrease in firing rate following fatiguing exercise in older adults is somewhat less than that observed in young individuals.
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Scott Rubinstein is a research specialist in the Spinal Cord Injury Center at the Department of Veterans Affairs Health Care System in Palo Alto, CA. He received his B.S. in Kinesiology from the University of Texas at Austin in 2000, and his M.S. in Exercise Science in 2004 from the University of Massachusetts at Amherst. As a student in the Exercise Neuroscience laboratory, his focus was in motor unit behavior in older adults during neuromuscular fatigue. He presented these results at the biennial conference of the International Society of Electrophysiology and Kinesiology in Boston, MA in 2004. Additional research consisted of intrinsic motor unit properties as well as firing rate behavior during ramping muscle contractions. Gary Kamen received his Ph.D. in Exercise Science from the University of Massachusetts. Following academic appointments at Indiana University and Boston University, he joined the Dept. of Exercise Science at UMass-Amherst in 1995. Dr. KamenÕs area of expertise is Human Motor Control. His research activities have been designed to understand how processes such as longterm exercise and aging produce adaptations in the neuromuscular system. These projects, supported by NIH and other sponsors, have culminated in the publication of over 100 books, book chapters, articles and research abstracts at national and international meetings. He has served as a reviewer for over 20 journals and numerous granting agencies. He is currently a Fellow of the Research Consortium, AAHPERD, a Fellow of the American College of Sports Medicine, and a Fellow of the American Academy of Kinesiology and Physical Education.
Decreases in motor unit firing rate during sustained maximal-effort contractions in young and older adults Scott Rubinstein, Gary Kamen
*
Department of Exercise Science, University of Massachusetts – Amherst, Amherst, MA 01003, United States Received 8 October 2004; received in revised form 22 April 2005; accepted 27 April 2005
Abstract Previous studies have suggested that older adults may be more resistant to muscular fatigue than young adults. We sought to determine whether motor unit firing rate might be a factor that determines the response to fatiguing exercise in young and older subjects. Motor unit recordings and muscular forces were obtained from the tibialis anterior (TA) muscle of 11 young and 8 older individuals. Maximal voluntary force was first measured during maximal-effort dorsiflexion contractions. Each subject then performed a series of 15 maximal isometric contractions, with each contraction lasting 30 s. A 10-s rest period separated the fatiguing contractions. As a result of the fatiguing exercise, both subject groups demonstrated a significant loss in maximal force. The force decline was less in the older adults (20.4%) than in the young adults (33.8%). As expected, prior to muscle fatigue, maximal firing rates in the TA muscle were greater in the young (28.1 ± 5.8 imp/s) than in the older adults (22.3 ± 4.8 imp/s). The decrease in motor unit firing rate with fatigue was also greater in the young adults (34.9%), than in the older adults (22.0%). These results suggest that the greater fatigue-resistance exhibited by older individuals might be explained by the fact that the decline in motor unit firing rate during fatigue is greater in young persons than it is in older adults. 2005 Elsevier Ltd. All rights reserved. Keywords: Aging; Exercise; Muscle; Fatigue; Tibialis anterior
1. Introduction It is well documented that human muscular force production and muscle contractile characteristics exhibit significant decrements with age. Maximal voluntary contractile force (MVC) in persons over 60 years is more than 25% lower than MVC force in young adults in several different muscles, including adductor pollicis [46], knee extensors [41], tibialis anterior [17], and biceps brachii [1]. Such reductions in strength can be due to a decrease in the number of active motor neurons [60] and consequently a loss in the number of active MUs [14], particularly affecting type II motor units [3,39,61]. Sur*
Corresponding author. Tel.: +1 413 545 0784; fax: +1 413 545 2906. E-mail address: [email protected] (G. Kamen). 1050-6411/$ - see front matter 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.jelekin.2005.04.001
viving fast-twitch fibers become reinnervated by slower, type I neuronal axon branches [35] and ultimately exhibit similar physiological characteristics of slow twitch MUs [13], mainly the inability to produce large twitch forces. Consequently, there is a linear increase in the percentage of type I fibers with age [39]. Because there is an overall decline in total muscle fiber numbers, particularly the larger type II fibers, there is an overall loss in muscle cross-sectional area [11], a main contributor to muscle force production. However, the influence of muscular fatigue on older adults is much less clear. While several studies indicate that fatigue resistance is similar in young and older adults [5,41,58], a number of reports (cf. [2]) now suggest that in tasks involving muscular endurance, older adults are actually less susceptible to fatigue than young individuals [15,18,31,38,46]. Thus, in contrast to the known
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decrements in muscular force in older adults, age-related differences in endurance present a more equivocal picture. Though a considerable portion of the decline during muscular exertion is attributed to peripheral changes or impairments in muscle [30,44], there are also central nervous system (CNS) components that impact the fatigue process. There are numerous influences on the motoneuron and potential changes in motoneuron intrinsic properties and these have been studied by assessing motor unit firing rate during fatiguing exercise. In young adults, fatigue is known to produce a decrease in motor unit firing rate in maximal voluntary contractions [6,7,45], though exceptions have been noted in some muscles [42]. Occasionally, it is possible that motor units cease firing altogether [51]. At low levels of force, firing rates are similar among young and older adults [24,29,57]. However, at maximal force levels, firing rates in the elderly have been shown to be significantly slower compared to the young subjects [17,29,49]. Moreover, we have no information on the potential change in motor unit firing rate in older adults following fatiguing exercise. Thus, the question of whether older adults fatigue less than young adults during prolonged exercise is equivocal, and the mechanism for such a phenomenon is unknown. Consequently, we sought to measure and compare changes in motor unit firing rate following a regimen involving fatiguing exercise in young and older individuals.
2. Methods All participants attended one recording session where they were required to sustain 15 maximal dorsiflexion contractions separated by periods of muscle relaxation. Subjects were allowed to monitor their force production on a computer video screen during each contraction and throughout the course of the entire recording session.
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2.2. Motor unit recordings Muscle fiber action potentials were recorded from the tibialis anterior muscle in a manner similar to that reported in previous studies [28,29]. A 25-gauge stainless steel cannula containing four 50 lm platinum–iridium wires was inserted into the tibialis anterior muscle. Three-channel recordings were obtained from the four wires. In our experience, multi-channel recording is essential since single-channel recordings can produce inaccurate identification of muscle fiber action potentials, particularly at greater forces (Fig. 1). The muscle fiber signals were amplified (Dantec Counterpoint Electromyograph; Dantec Electronik Medicinsk, Skovlunde, Denmark; gain 500· typ; bandpass 1–10 kHz), viewed on a digital oscilloscope (Gould 2608, Thermo Electron Corporation, Valley View, OH), and digitized (microcomputer-based WIN-30 data acquisition board, United Electronics, Watertown, MA; Dasylab software; 25.6 kHz sampling rate). Individual action potentials were also viewed on a computer monitor through an oscilloscope module in DASYLab software (Data Acquisition System Laboratory (DASYLab), DasyTec USA, Inc., Amherst, NH). 2.3. Muscular force Isometric dorsiflexion force was measured using a strain gauge force transducer (Interface model MB10, Scottsdale, AZ) mounted to a custom-designed metal apparatus. The force signal was amplified (500·) using a custom-built bridge amplifier, digitized (50 Hz; Data translation DT2801A/D converter, Marlborough, MA), and presented to the subject on a computer monitor for force feedback. Muscular force was concurrently sampled at 25.6 kHz (WIN-30) and later downsampled at 50 Hz for analysis.
2.1. Subjects Subjects consisted of 34 young women (18–30 years; mean age: 19.2 years) and 12 older women (>69 years, mean age: 73.1 years). Each participant completed a Physical Activity Readiness Questionnaire (PARQ [55]) and were screened for any neuromuscular, sensorimotor, and cardiopulmonary disorders and/or injuries. All participants were engaged in moderate levels of daily physical activity (3–5 days/week) and each person refrained from any physically abnormal and/or strenuous activity 24 h prior to her participation. All procedures were approved for human subject participation by the institutional review board. Participants provided written informed consent.
Fig. 1. Multi-channel recordings are critical to ensure correct identification of muscle fiber action potentials, particularly at higher forces. Signals for three channels and two motor units are illustrated. On channel 1, the signals from two motor units are virtually identical. However, the addition of two other recording channels reveals that these comprise distinct signals from two different motor units.
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2.4. Procedures Subjects were seated in a custom-built apparatus designed to measure ankle dorsiflexion in the dominant leg (Fig. 2). Limb dominance was assessed by asking each subject which leg they would use to kick a ball. Hip and knee angles of 90 were maintained and the ankle was set at 20 of plantarflexion as this angle allows maximum dorsiflexion force to be produced [63]. A Velcro strap was secured over the mid-portion of the subjectsÕ dominant thigh while belts were fastened around the subjectÕs waist and chest to isolate the dorsiflexion contraction. Anteroposterior and mediolateral movements of the ankle and knee joints were restricted using foam braces. The subjects were required to sit with their arms folded across the waist to ensure consistent posture across subjects. Subjects performed four maximal voluntary contractions (MVCs; 3–4 s duration) of the dominant dorsiflexors. Individuals were asked to reach their maximal force within about 1–2 s so as not to produce any fast, jerking movements. A two-minute rest was provided between contractions and the highest value was used as their MVC for force-feedback displays during the remainder of the experiment. The needle electrode was inserted into the TA muscle approximately half-way between the tibial tuberosity and the lateral malleolus and at an approximate 30 angle. The proper position of the needle was determined by the presence of high frequency motor unit activity at 20– 30% MVC as assessed by action potentials on the digital oscilloscope and by high frequency audible cues from the differential amplifier and speaker. The needle depth
varied in different subjects; the most important consideration was a location from which stable recordings could be obtained. 2.5. Fatiguing protocol The fatiguing protocol consisted of 15 intermittent MVC isometric contractions, each requiring a 30-s dorsiflexion contraction followed by a 10-s rest period. Instructions to contract and relax were provided by voice cues from a tape recording. Subjects viewed a computer monitor which provided feedback regarding the requisite force level. The researcher provided verbal encouragement throughout the entire 30-s contraction. 2.6. Data analysis During each contraction, muscular force was obtained as the average force produced during the 3 s interval following the maximum force produced within the first 10 s of each contraction. Due to changes in the position of the needle electrode, the task of recording muscle fiber action potentials during each of the 15 contractions proved to be technically difficult. Consequently, we analyzed the firing rates of motor units that were identified during the first and last contractions by computing the mean interfiring interval (IFI) for all accurately identified MU trains in the 3 s block following maximum force. A customized algorithm was used to identify individual motor unit action potentials. This algorithm included both an automatic routine as well as software that displayed the signals and relevant firing statistics
Fig. 2. Apparatus used to measure ankle dorsiflexion.
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on computer monitors. The process included detection using signal threshold measures, and classification using least squares identification based upon template matching. The routine is modified from the algorithm reported by LeFever and colleagues [40]. Though distinct motor unit trains could be classified with over 90% accuracy by the custom software automatically, trained operators reviewed the motor unit signals to correct any misidentifications. Motor unit action potential trains in which identification was uncertain due to difficulties in template matching were not included for analysis. A separate algorithm was used to algebraically resolve superpositions into constituent action potentials. The superposition algorithm requires alignment with the highest peak in the signal waveform, and subtraction of known motor unit templates. A least squares criterion is used to identify two or more motor unit templates with minimal signal residual error. The accuracy of this motor unit identification technique has been demonstrated in earlier studies [27,29,48,49]. Motor units occasionally fire in doublets – two firings with a short interpulse interval less than 10 ms [22]. Among the motor units used in this study, six such doublets were observed and these were included in the analysis. The interfiring interval between two discharges may also be abnormally long (>150 ms) and these are generally due to technical difficulties in identifying motor unit activity, though it is also possible that there are brief pauses in motor unit activity [51]. These elongated IFIs were not included in the calculation of the mean motor unit discharge rate.
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Fig. 3. (Top) Mean (±SD) dorsiflexion force (N) for each of the 15 contractions. The mean force was computed for a 3 s period following the peak force occurring within the first 10 s of each MVC. Older adults had smaller absolute MVC values than the young adults. Both age groups demonstrate significant losses in muscular force (bottom). Percentage of mean force during the 3 s block in Contraction 1 for all 15 contractions.
2.7. Statistical analysis The mean isometric dorsiflexion force was compared between age groups and across all 15 MVCs using a two-factor (2 groups by 15 contractions) repeated measures analysis of variance (ANOVA), with the 15 contractions as a repeated measure. Orthogonal polynomial comparisons were used to further test for significant trends in force reduction [66]. A repeated measures ANOVA compared mean firing rate (impulses/s) between age groups and pre- and post-fatigue (contractions 1 and 15). TukeyÕs honestly significant difference (HSD) test determined any significant paired contrasts.
3. Results 3.1. Muscular force Fig. 3 shows the decrease in maximal force capability in both young and older adults during the fatiguing exercise protocol. Trial 1 scores revealed that baseline muscular force was significantly greater in young adults
than in older adults (p < 0.05). Both age groups demonstrated a significant loss in maximal dorsiflexion force throughout the 15 contractions (p < 0.001). Though older adults had significantly lower absolute MVC values as compared to the younger adults (Fig. 3(a); p < 0.05), older adults displayed a significantly smaller loss in their normalized MVC across the 15 contractions (20.4% decrease) compared to the younger adults (33.8% decrease; p < 0.001). Orthogonal polynomial comparisons showed that the significant age by contraction interaction was due to differences in the linear component (p < 0.01). No significant higher-order polynomial comparisons were obtained. Thus, a straight-line fit best described the loss in force over the 15 contractions for both subject groups. Fig. 3 (bottom) displays force loss as a percentage of the mean force value produced in the first contraction. 3.2. Motor unit firing rates Under non-fatiguing conditions, it can be technically difficult to record individual motor unit action
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Fig. 4. Motor unit firing rates (mean ± SD) in the tibialis anterior muscle in young and older adults. During the first contraction, older adults had slower firing rates than the young adults. Both age groups experienced significantly slower MU firing rates as a result of the fatiguing exercise. However, a greater decline in MU firing rates was observed in the young adults than in the older adults (statistical symbols – *, p < 0.05; , p < 0.01).
potentials at maximal force levels. During fatiguing conditions, this difficulty was compounded by changes in the intramuscular milieu which produced a low-pass filtering effect on the signals, exacerbating the difficulty of identifying single motor unit potentials. Consequently, the final data set consisted of 11 young and 8 older adults. Both force and firing rate statistics were obtained from these subjects. The motor unit sample included a total of 70 motor units, 39 MUs from the young adults, and 31 MUs from the older adults. Under non-fatiguing conditions, older adults exhibited significantly slower MU firing rate (22.3 ± 4.8 imp/s; mean ± SD) than did the young adults (28.1 ± 5.8 imp/s; Fig. 4; p < 0.05). Both age groups experienced significant reductions in MU firing rate between contractions 1 and 15 (p < 0.001). Following the fatiguing exercise, the decrease in MU firing rate was more pronounced for the young adults (34.9%) than for the older adults (22.0%). Although there was no significant two-way interaction (p = 0.12), TukeyÕs HSD test revealed that MU firing rates between the two subject groups were not significantly different at the fifteenth contraction (p > 0.05). Thus, there was a substantial difference in the MU firing rate response of the two groups, with the young subjects demonstrating a somewhat greater decline in firing rates during the fatiguing exercise than the older adults.
4. Discussion The purpose of the current study was to provide the first experimental assessment of changes in motor unit behavior after a maximal-effort fatiguing exercise of the tibialis anterior muscle in women younger than 30 and older than 69 years of age. Such an observation
may help explain the central nervous systemÕs role in fatigue, specifically addressing why older adults have been shown to be less fatigable during maximal-effort contractions [18,8,31] . Indeed, these data confirm earlier reports suggesting that older adults have more fatigue resistance than do younger individuals. During the fatiguing exercise task, force output in the older adults declined by 20%, while young subjects lost 34% of their maximum contractile force. These changes in force were matched by similar declines in motor unit firing rate in both groups. At the end of the exercise, firing rates in the young subjects declined by 35%, while firing rates in older adults declined 22%. As mentioned in Section 1, there are some studies that have failed to note any differences in fatigability due to age [5,41,58]. It is possible that one of the differences among the earlier fatigue studies is activity level. In the present study, we recruited active older adults, whose activity level was similar to that of the young adults. It is possible that those studies that have found no difference due to age may not have accounted for activity level. At least one report suggests that active individuals demonstrate greater resistance to fatigue than sedentary individuals [37]. The magnitude of force change due to the fatiguing exercise is similar to that observed in previous investigations. When subjects were asked to hold a fatiguing submaximal contraction as long as possible, post-fatigue force values decreased by approximately 25% in biceps brachii [16,21], 30% in triceps brachii [23], and 35% in first dorsal interosseus [67]. During sustained maximal efforts, force declined by approximately 40% during a one-minute dorsiflexion contraction [4]. Lanza et al. [38] reported almost identical fatigue-related reductions in maximal force for both young and older men for the TA muscle. In similar studies using intermittent muscle contractions, researchers have frequently reported that most of the force decline occurs in a linear fashion. However, high-strength individuals frequently exhibit an initial steep decline in force resulting in a quadratic polynomial component in the fatigue curve [26,34]. On a relative basis, high-strength subjects (both men and women) demonstrate greater declines in force than do low-strength subjects [32,33]. Similarly, fast-twitch motor units fatigue faster than slow-twitch motor units [59], and the greater proportion of slow-twitch motor units in the older adults would provide more fatigue-resistance. Thus, it is not altogether surprising that the high-strength young adults would exhibit greater endurance than the lower-strength older adults. The firing rates observed in the tibialis anterior muscle (young – 28 imp/s; older – 22 imp/s) are comparable to those reported previously. Bigland-Ritchie et al. [10] reported a maximal firing rate of 28 imp/s, and Van Cutsem et al. [62] reported maximal discharge rates of
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33 imp/s in the tibialis anterior. Although we reported somewhat higher values earlier [48], this is likely due to the choice of metric for computing maximal firing rate. Using scores obtained from the shortest five consecutive interpulse intervals, we previously reported firing rates of 60 imp/s for young subjects, 44 imp/s for older adults [48]. In the present investigation, we computed firing rates over the first three seconds following the attainment of maximal force. Several laboratories have now consistently reported lower motor unit discharge rates in older adults than in young adults [17,29], though some exceptions have been noted [54]. There are several possible explanations for age-related decreases in firing rate. It is possible that there are some disruptions in the quality of the descending command that impact maximal motor unit firing rate. Using transcranial magnetic stimulation, Peinemann et al. [50] observed an age-related decrease in the excitability of intracortical inhibitory pathways, and these intracortical pathways may be important in organizing the final command to motoneurons. There is also a loss in the numbers of descending corticospinal neurons [19], and this could also account for decreases in maximal firing rate. Synaptic transmission from spindles is altered in aged cats [12], resulting in diminished la drive to the motoneuron pool. The density of synaptic input to the motoneuron pool is also diminished in aged rats [36]. Any or all of these factors could be important in determining maximal firing rate, however, the exact mechanism through which motor unit firing rates decline with age remains to be determined. Motor unit firing rate significantly decreased in both age groups across the current protocol, and this is in agreement with other MVC fatiguing protocols in the adductor pollicis [6] and biceps brachii muscle [9] where age-related differences were not compared. The effect of afferent feedback altering central drive to the muscle is speculated to reduce MU firing rate. While ischaemic conditions reduce the peripheral force-generating capabilities during a sustained MVC [9], MU firing rate also remains depressed during blood occlusion. Bigland-Ritchie et al. [9] posited a reflex mechanism elicited by metabolic byproducts in fatigued muscle that might lead to a reduction in MU firing rate. The tibialis anterior muscle is composed mostly of type I, slow-twitch fibers, particularly in older adults [25,52]. Anaerobic metabolism used by type II fibers can raise the [H+] within a muscle fiber during prolonged activity, especially during maximal-effort isometric conditions where blood flow is occluded. As a result, a muscle with a greater proportion of type II fibers would be more likely to induce an inhibitory afferent reflex. In the event that some motor neurons completely cease firing during fatigue, it would most likely be due to the corresponding muscle fibers that have lost the ability to generate force. Because type I muscle fibers are aerobic, older muscle
541
may be less likely to elicit metabolic feedback inhibition during a sustained muscle task. It is also possible that motor unit discharge rates decline with fatigue as a compensatory mechanism to match the fatigue-related changes in muscle fiber contractile properties. Such a mechanism is called muscular wisdom [43]. Muscular wisdom could also explain the decline in maximal firing rates observed in older adults [17,29], since a slowing of contractile properties occurs in older muscle [64]. As fatigue ensues, older adults already have slower contraction duration and halfrelaxation times, and might not benefit very much from a fatigue-induced slowing of firing rate to match the already slow contractile properties. Young adults, however, might be able to delay fatigue by slowing motor unit firing rates to match changes in contractile properties. As indicated above, the decrease in firing rates could also be caused by reflex inhibition produced by group III–IV afferents [20], however, there is little data on the characteristics of slow-conducting afferents in older adults. In general, the responses produced by small afferents are diminished with advancing age [47,53, 56,65], and if the responses of group III–IV afferents decrease with age, this could also account for a greater fatigue-related slowing of firing rates in young adults than in older individuals. In summary, we concur with previous observations made during fatiguing contractions, in demonstrating that fatiguing exercise produces a relatively greater force loss in young subjects than in older subjects. The data regarding motor unit firing rates provide further support for a lowering of maximal motor unit firing rate in older individuals. Finally, we conclude that the loss of force following fatiguing exercise in both young and older subjects is accompanied by a proportional decrease in motor unit firing rate; the decrease in firing rate following fatiguing exercise in older adults is somewhat less than that observed in young individuals.
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Scott Rubinstein is a research specialist in the Spinal Cord Injury Center at the Department of Veterans Affairs Health Care System in Palo Alto, CA. He received his B.S. in Kinesiology from the University of Texas at Austin in 2000, and his M.S. in Exercise Science in 2004 from the University of Massachusetts at Amherst. As a student in the Exercise Neuroscience laboratory, his focus was in motor unit behavior in older adults during neuromuscular fatigue. He presented these results at the biennial conference of the International Society of Electrophysiology and Kinesiology in Boston, MA in 2004. Additional research consisted of intrinsic motor unit properties as well as firing rate behavior during ramping muscle contractions. Gary Kamen received his Ph.D. in Exercise Science from the University of Massachusetts. Following academic appointments at Indiana University and Boston University, he joined the Dept. of Exercise Science at UMass-Amherst in 1995. Dr. KamenÕs area of expertise is Human Motor Control. His research activities have been designed to understand how processes such as longterm exercise and aging produce adaptations in the neuromuscular system. These projects, supported by NIH and other sponsors, have culminated in the publication of over 100 books, book chapters, articles and research abstracts at national and international meetings. He has served as a reviewer for over 20 journals and numerous granting agencies. He is currently a Fellow of the Research Consortium, AAHPERD, a Fellow of the American College of Sports Medicine, and a Fellow of the American Academy of Kinesiology and Physical Education.