Journal of Applied Physiology AJP: Endocrinology and Metabolism
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

J Appl Physiol 92: 2292-2302, 2002. First published February 8, 2002; doi:10.1152/japplphysiol.00367.2001
8750-7587/02 $5.00
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow All Versions of this Article:
92/6/2292    most recent
00367.2001v1
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (58)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Scaglioni, G.
Right arrow Articles by Narici, M. V.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Scaglioni, G.
Right arrow Articles by Narici, M. V.
Vol. 92, Issue 6, 2292-2302, June 2002

Plantar flexor activation capacity and H reflex in older adults: adaptations to strength training

G. Scaglioni1,2,3, A. Ferri1,2,3, A. E. Minetti2,3, A. Martin1, J. Van Hoecke1, P. Capodaglio3, A. Sartorio4, and M. V. Narici2,3

1 Groupe Analyse du Mouvement, Unité de Formation et de Recherche en Sciences et Techniques des Activités Physiques et Sportives, Université de Bourgogne, 21078 Dijon Cedex, France; 2 Centre for Biophysical and Clinical Research into Human Movement, Manchester Metropolitan University, Alsager ST7 2HL, United Kingdom; 3 Centro Studi Attività Motorie, Fondazione S. Maugeri, 27100 Pavia, Italy; and 4 Division Metabolic Diseases, Istituto Auxologico Italiano, Instituto di Ricovero e Cura a Carattere Scientifico, 28900 Piancavallo, Italy


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The purpose of this study was to investigate whether the voluntary neural drive and the excitability of the reflex arc could be modulated by training, even in old age. To this aim, the effects of a 16-wk strengthening program on plantar flexor voluntary activation (VA) and on the maximum Hoffman reflex (Hmax)-to-maximum M wave (Mmax) ratio were investigated in 14 elderly men (65-80 yr). After training, isometric maximum voluntary contraction (MVC) increased by 18% (P < 0.05) and weight-lifting ability by 24% (P < 0.001). Twitch contraction time decreased by 8% (P < 0.01), but no changes in half relaxation time and in peak twitch torque were observed. The VA, assessed by twitch interpolation, increased from 95 to 98% (P < 0.05). Pretraining VA, also evaluated from the expected MVC for total twitch occlusion, was 7% higher (P < 0.01) than MVC. This discrepancy persisted after training. The interpolated twitch torque-voluntary torque relationship was fitted by a nonlinear model and was found to deviate from linearity for torque levels >65% MVC. Compared with younger men (24-35 yr), the Hmax- to Mmax ratio and nerve conduction velocity (H index) of the older group were significantly lower (42%, P < 0.05; and 29%, P < 0.001, respectively) and were not modulated by training. In conclusion, older men seem to preserve a high VA of plantar flexors. However, the impaired functionality of the reflex pathway with aging and the lack of modulation with exercise suggest that the decrease in the Hmax- to Mmax ratio and H index may be related to degenerative phenomena.

twitch interpolation; triceps surae; aging; exercise


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

AGING IS COMMONLY CHARACTERIZED by a progressive decline in motor control, often reflecting changes in neuromuscular function. It is generally accepted that the weakness associated with aging is not only due to sarcopenia but may also be related to neural adaptations (17, 38). In fact, generation of strength relies on the ability of the nervous system to activate muscles effectively, after permanent adjustments of central command on the reflex response integrated at spinal level. However, the role of neural adaptations to training has still not been fully elucidated in the elderly, despite reports that a considerable part of the strength gain observed in aging involves changes in neural drive, such as 1) distribution of the motor command to the muscles, 2) modulation of neuromuscular excitability, and 3) timing of motor unit discharge (17, 20).

In the present study, the effectiveness of strength training on voluntary drive to the plantar flexors (PF) was assessed by means of the twitch interpolation technique, as proposed by Allen et al. (2, 3). This technique is commonly used to test the ability to achieve complete activation of the muscles and, therefore, provide information concerning central motor drive. Based on numerous studies that have applied this technique in young adults, the present consensus is that voluntary drive to the lower limb muscles is very high during maximal effort (2, 3, 7, 39). However, whether the same is also true in older subjects remains to be established. Indeed, results reported in the literature are conflicting, possibly depending on the muscle group studied and the use of different techniques (3, 5, 6, 12, 24). Winegard et al. (48) reported an incomplete activation level (83%) of the PF in a group of very old subjects (73-97 yr). A reduced ability to achieve full muscle activation in old age was also observed in the quadriceps (22) and in the biceps brachii muscles (49). Conversely, other authors concluded that most older individuals are able to utilize their descending motor pathways for an optimal activation of several muscles of the lower and upper limbs (8, 12, 28, 36, 47). Therefore, the heterogeneity in the ability to activate specific muscles suggests that this may be related to differences in their general pattern of use (39). Thus it seems plausible that age-related adaptations in maximal neural activation may vary in relation to the specific involvement of different muscles in daily physical activities. Hence, there is the expectation that, even in old age, adaptations of neural drive to prolonged periods of strength training might be achieved.

Given that regulation of motoneuron activity is obtained through supraspinal as well as spinal inputs, it may also be of interest to investigate age-related changes in excitability at the peripheral level, namely in the spinal reflex pathway, and whether these can be modulated by regular physical activity during aging. The quantitative evaluation of the neuromuscular excitability may be appraised by measuring the electromyographic (EMG) responses evoked by an electrical stimulus applied on a peripheral nerve. It is accepted that a submaximal stimulation produces a characteristic reflex response (H wave), which is the result of the motoneuron discharge evoked by the activation of the Ia fibers from the muscle spindles, whereas increasing the stimulus intensity results in the direct depolarization of the alpha -motoneurons' axons. The ratio between the amplitudes of the maximum reflex response (Hmax) and maximum direct motor wave (Mmax) is commonly used as an index for estimating the level of reflex excitability of the motor pool (Hmax-to-Mmax ratio) (31). However, because this, in turn, depends on the facilitation of the transmission between the Ia fibers and the alpha -motoneurons (44), we cannot neglect the role of presynaptic inhibitions and possibly oligosynaptic contributions in modulating the reflex response. It is noteworthy that, as a consequence of the natural changes occurring in the central nervous system with senescence, aging has been associated with a decrease in motoneuron excitability and thus in nerve conduction velocity (13, 18, 40, 46), but it has also been observed that physically active older adults have preserved an efficient neuromuscular performance with a faster reflex response compared with their sedentary counterparts (23). It remains, therefore, to elucidate whether physical deconditioning rather than just degenerative phenomena may be involved in the age-related adaptations of the spinal reflex pathway. The Hmax-to-Mmax ratio has been shown to display a certain degree of plasticity to regular physical exercise in young subjects (10, 35, 43); nevertheless, whether a similar adaptation also occurs in older adults remains presently unknown.

In light of these considerations, the present study was designed to investigate whether the voluntary neural drive to the muscle and the excitability of the reflex arc could be modulated by training, even in old age. To this aim, the effects of a 16-wk strengthening program on PF activation capacity and on the Hmax-to-Mmax ratio were investigated in a population of 14 elderly men.


    METHODS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The experiments here described are part of a comprehensive training study designed to provide an overall conditioning stimulus, involving both the upper and lower limbs. However, this particular paper shall deal with the neural adaptations of the PF muscles to strength training in aging.

Subjects

Fourteen men (aged 68 yr, range 65-80 yr; mass 80 kg, range 65-98 kg; height 172 cm, range 163-194 cm) agreed to participate in the study after being fully informed about the investigation and the possible related risks and discomfort. All subjects underwent a series of medical examinations, including a complete blood test, urine analysis, chest-X ray, rest and stress electrocardiogram, blood pressure, and detailed anamnesis focusing on the individual physical and leisure activities. For each subject, a profile, based on the past and present physical activities, was defined, taking into account the type and number of hours of exercise per week. Only healthy (free from neurological, cardiovascular, metabolic, inflammatory diseases) and moderately active subjects were admitted to the study. People were considered moderately active who were taking part in recreational, noncompetitive, physical activities with a frequency of no more than twice a week, not including regular strength training or high-intensity muscular efforts. During the 16-wk program, the subjects maintained their habitual leisure activities.

The H-reflex and M-wave measurements at baseline were compared with those obtained in young, moderately active adults (10 men, aged 29 yr, range 24-35 yr; mass 81 kg, range 72-100 kg; height 178 cm, range 165-184 cm), previously tested in our laboratory with the same technique. All of them signed a declaration of informed consent. The study was approved by the Ethics Committee of the S. Maugeri Foundation (Institute of Occupational Medicine and Rehabilitation, Pavia, Italy), where the investigation was carried out.

Strength Training Protocol

The subjects participated in a 16-wk strength-training program. Each training session, carried out on commercially available strengthening machines (Technogym), consisted of six different exercises involving the main muscle groups of the upper and lower limbs. The training frequency was three times per week, every other day, except the weekend. During the first five sessions, before the beginning of the study, subjects were familiarized with the equipment and with the exercise technique. The training of the lower limb muscles involved bilateral, closed kinetic chain movements, performed on a leg-press machine for the knee extensors and PF and on a sitting calf-rise machine specifically for the PF. In the leg press, leg extension was performed from a knee angle of 95 to ~5° from full extension, to prevent knee-joint damage. For the calf-rise exercise, subjects plantar flexed from a position of ~20° of dorsiflexion to maximum plantar flexion (~30°). The subjects were instructed to perform the lifting of the weight (concentric action) in ~2 s and, immediately after, the lowering of the weight (eccentric action) in ~3 s. This timing was achieved through the use of a visual display of the load excursion featured in the Technogym training machines used in this study. The training protocol consisted, for the first 3 mo, of one set of 10 repetitions with an initial load of 50% of one repetition maximum (1 RM: the maximum load that can be lifted once only) and was increased within 4 wk of training to 80% 1 RM. In the last month, an extra set of 10 repetitions was added, and the two sets were interspaced by a 2-min rest. For safety reasons, the 1 RM in each subject was estimated by measuring the three repetitions maximum (3 RM: maximum load that can be lifted 3 times only) with the use of the load-repetitions curve obtained by Sale and MacDougall (42). According to this relationship, a 3 RM corresponds to ~93% of 1 RM. The training load was updated every 2 wk to match it, as close as possible, to 80% of 1 RM. Each training session was preceded by 10-min warm-up exercise on a cycle ergometer at a heart rate corresponding to 50% peak O2 uptake (previously measured) and by one set of 15 repetitions at 20% of 1 RM on each training machine, followed by 10 min of stretching exercises. Subjects were individually supervised during training sessions at all times.

Measurements

All measurements were carried out on the dominant leg. The assessment of H- and M-wave amplitudes was conducted at baseline and after 10 and 16 wk. Voluntary activation (VA) capacity and muscle contractile properties were evaluated before and at the end of the training program.

Maximal voluntary contraction, VA, and contractile properties. The PF isometric maximal voluntary contraction (MVC) and the evoked twitch torque were determined in the supine position with the foot dorsiflexed at 20° (with 0° being the perpendicularity of the dynamometer footplate to the tibia). Such position was maintained throughout the experimental session. The pelvis was firmly fixed to the examination table to prevent movements during efforts. A strap was placed around the foot to secure it sturdily to the strain gauge of the dynamometer (Cybex Norm, Cybex Ronkonkoma) used to measure the force produced during evoked and voluntary contractions. Torque measurements were sampled at 200 Hz, amplified by five, band-pass filtered (10 Hz-1 kHz) by using an analog-to-digital board (Biopac, MP100), and hence stored on the hard disk of a desktop computer (Power Macintosh 8600/200).

A percutaneous constant-voltage electrical stimulator, developed by the European Space Agency, was used to deliver square-wave stimuli of 50 µs in duration to the triceps surae via two large surface electrodes (VersaStim, ConMed). The anode (12.5 × 7.5 cm) was placed over the belly of the gastrocnemius muscle, and the cathode (9 × 3.5 cm) over the soleus muscle, after cleaning of the skin with alcohol pads. The stimulus intensity was progressively increased until a further increase in current resulted in no further increment in twitch amplitude; this current was then regarded as supramaximal and the corresponding twitch as maximum.

During the first part of the experimental session, the subjects were asked to perform three, 5-s-long MVCs of the PF. During each contraction, subjects were verbally encouraged to deliver maximal performance, and the highest torque generated was considered as the MVC. At least a 10-min rest period was introduced after the MVCs to minimize twitch potentiation in the successive test. Three supramaximal single stimuli, separated by a 1-min pause, were then delivered to the relaxed muscle to obtain a mean control twitch. The control twitch recordings enabled the determination of the peak twitch torque (Pt), twitch contraction time (CT), half relaxation time (HRT), and, as a consequence, the Pt-to-MVC ratio (Pt/MVC), as well as Pt-to-CT ratio (Pt/CT), which may be considered as an index of the mean velocity of contraction. Subsequently, the subjects performed, in randomized order, voluntary contractions at five target levels: 20, 40, 60, 80, and 100% of the previously determined MVC. The target efforts and the exerted torque were displayed, in real time, on the computer monitor as visual feedback to the subject. When the torque performed was considered to match the reference, two supramaximal single twitches, at 1 Hz, were interpolated. Especially for the higher contraction levels, the torque developed by the subjects did not always match precisely the target line, but the mechanical recordings allowed accurate determination of the value of voluntary torque at which the stimulus was triggered. To avoid interference due to fatigue, 2 min of rest were given between trials.

Because superimposed stimulation is presumed to activate motor units not recruited by the voluntary effort, the ratio of the extra torque (Pta) generated by each supramaximal superimposed stimulus during MVCs, over the amplitude of the evoked torque at rest (Pt), was used to calculate the VA, where 100% represents full motor unit recruitment [%VA = (1 - Pta/Pt) · 100]. For each subject, the highest over four VA scores was considered as the VA.

Analysis of the Pta-voluntary torque relationship. Because the Pta appeared to decline in a nonlinear fashion as contraction intensity (%MVC) increased (Fig. 1), the analysis of this relationship posed some problems in terms of regression equation, which had to satisfy the following requirements: 1) both the linear and curvilinear portions of the relationship have to be described and 2) curve and axes must intersect at relevant points, namely at MVC = 0% [representing the extrapolated "control twitch" (Pt exp)] and at Pta = 0 [representing the extrapolated maximum intensity contraction (MVCexp), Fig. 1]. To fulfill these constraints, the following equation was obtained
%MVC<IT>=a</IT><FENCE>(1<IT>−b</IT>)<IT>e</IT><SUP><IT>c</IT>P<SUB>ta</SUB></SUP><IT>+b</IT><FENCE>1<IT>−</IT><FR><NU>P<SUB>ta</SUB></NU><DE><IT>d</IT></DE></FR></FENCE></FENCE> (1)
This equation contains curvilinear (exponential) and linear components, weighted by the coefficient b. The curvature of the nonlinear portion of the function is described by c. The coefficient d represents a prediction of Pt exp, whereas a is an estimate of MVCexp (Table 1). The four coefficients have been estimated for each subject by feeding a nonlinear regression software package (SYSTAT 5.2.1 for Macintosh) with individual (Pta, %MVC) data.


View larger version (15K):
[in this window]
[in a new window]
  		Fig. 1.   Relationship between the extra force produced by the interpolated twitch (Pta) and voluntary isometric torque. Data are from 1 representative subject. Contraction intensities are included between 0 and 100% of maximal voluntary contraction (MVC). The Pta declined in a nonlinear fashion for contraction intensities >65% MVC. An exponential plus linear equation is the result of the best fitting regression line to the experimental points (r2 = 0.99, P < 0.001). Pt, peak twitch torque. The composite regression function provides an estimation of the extrapolated MVC (MVCexp) for Pta = 0, of the expected peak twitch torque (Pt exp) for MVC = 0%, and of the point of deviation from linearity.


                              
View this table:
[in this window]
[in a new window]
  		Table 1.   Coefficient values of Eq. 1

To evaluate the contraction intensity at which the relationship with Pta changed from linear to curvilinear, a threshold in the curve slope was introduced as parameter k. (The k was set to 1.5 because it corresponds to the value that minimizes the %MVC variance at which the procedure found the slope flexion. Thus, being k = 1.5, the change in curvature will be detected if the equation slope exceeds 150% of the slope of the linear part.) This process can be formalized as
<FR><NU>1</NU><DE>a</DE></FR> <FR><NU><IT>d</IT>%MVC</NU><DE><IT>d</IT>P<SUB>ta</SUB></DE></FR><IT>=c</IT>(1<IT>−b</IT>)<IT>e</IT><SUP><IT>c</IT>P<SUB>ta</SUB></SUP><IT>−</IT><FR><NU><IT>b</IT></NU><DE><IT>d</IT></DE></FR> <−<IT>k</IT><FR><NU><IT>b</IT></NU><DE><IT>d</IT></DE></FR> (2)
where the first component, namely the first derivative of Eq. 1, representing the overall slope, is compared with a given proportion (k) of the slope for the linear part (-b/d). The solution to Eq. 2
P<SUB>ta</SUB><IT><</IT><FR><NU>1</NU><DE><IT>c</IT></DE></FR> ln <FENCE><FR><NU><IT>b</IT>(1<IT>−k</IT>)</NU><DE><IT>cd</IT>(1<IT>−b</IT>)</DE></FR></FENCE> (3)
represents the Pta at which the slope of the curvilinear portion deviates more than k times from the slope of the linear part. By substituting Pta obtained from Eq. 3 into Eq. 1, the corresponding contraction intensity (%MVC) is thus obtained.

H reflex and M wave. The test was performed with the subject lying prone with his feet freely hanging over the edge of the examining couch. Particular care was taken that the same position was maintained throughout testing and that no head rotation occurred to maintain constant the corticovestibular influences on the excitability of the motor pool (44). The EMG was recorded from the soleus muscle by using bipolar surface electrodes (Neuroline, Medicotest) positioned over the muscle belly with an interelectrode distance of 2 cm. The recording electrodes were placed on the lateral internal part of the muscle, and the reference electrode above the lateral malleolus. To ensure that the same recording site was used on successive sessions, individual maps on acetate paper of the lower leg were prepared, marking the position of individual references, such as moles and small angiomas. Interelectrode resistance was kept <5 kOmega by rubbing the skin with ether and with fine emery paper. The EMG signals were sampled at a frequency of 2 kHz, amplified, band-pass filtered as previously mentioned, and stored for off-line analysis on a computer system. The soleus H reflex was elicited by a constant-current stimulator (DS7, Digitimer, Welwyn Garden City, UK). A 1-ms square-wave stimulus was applied to the posterior tibial nerve via a bipolar stimulating electrode (Meditec, Parma, Italy) with the cathode proximal to the anode, as used by Falco et al. (18). The intensity of the stimulus was gradually intensified from the low level required to elicit the H reflex up to the level for evoking a maximal M response. For each subject, we evaluated the peak-to-peak amplitude of the H and M waves of the soleus muscle, the Hmax-to-Mmax ratio (to normalize the reflex response, minimizing the influence of external factors), and the latency of the H and M potentials. The latency was considered as the time interval between the onset of the stimulus artifact up to the first deflection of the H (Delta tH) or of the M wave (Delta tM). The maximum peak-to-peak amplitude of the H and M responses and the relative Hmax-to-Mmax were expressed as an average of eight measurements.

Furthermore, the H index (19), based on the linear relationship between subjects' height and the H-M interval (Delta tH-Delta tM), was also calculated to provide an estimate of the nervous conduction velocity in the reflex arc, as it is known to supply a useful means for the investigation of peripheral neuropathy {Hindex = [height (cm)/Delta tH - Delta tM]2 · 2}.

Statistics

A one-way factor ANOVA with repeated measures was used to determine the effects of the training program. Subsequently, the Newman-Keuls (post hoc) test was performed to locate differences between means, if present. The pre- and posttraining comparisons were conducted by applying Student's t-test, unless the data did not meet the criteria of normality (P < 0.05), in which case a nonparametric Wilcoxon matched pairs test was applied. Linear regression analysis (Pearson product-moment correlation) was used to compare the degree of association between variables, whereas the individual relationship between Pta and voluntary isometric torque was analyzed by applying a nonlinear correlation test. The one-sample Student's t-test was employed to evaluate the difference between the VA and 100%. Reproducibility of the measurements of VA and of Hmax and Mmax amplitudes was quantified, in consecutive days, during the familiarization period before training, with the intraclass correlation coefficient (ICC), by using a two-way random effect model. The latter measurements were repeated over 4 separate days for the VA and over 3 separate days for the Hmax and Mmax. The accepted level of significance of all statistical tests was set at 5%. The data are presented as means ± SD.


    RESULTS
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

MVC and 1 RM

The 16-wk strength-training program resulted in significant improvements in maximum voluntary isometric torque and weight-lifting capacity of the PF. At the end of the 16th wk, MVC increased by 17.8%, from 103.3 ± 31.4 to 115.7 ± 25.3 N · m (P = 0.02), and the 1 RM (mean of extrapolated values from the 3 RM) increased by 23.7%, from 47.8 ± 11.6 to 57.0 ± 8.8 kg (P < 0.001).

Contractile Properties

Values of Pt, CT, HRT, and Pt/MVC for the triceps surae are presented in Table 2. As can be observed, CT was significantly reduced by training (-7.7 ± 5.5%; P = 0.002) as was Pt/MVC (-10.3 ± 14.2%, P = 0.014). On the other hand, Pt/CT increased by 10.3 ± 14.2% (P = 0.023), whereas HRT, Pt/HRT, and Pt did not show significant changes at the end of the strengthening program.

                              
View this table:
[in this window]
[in a new window]
  		Table 2.   Effects of strength training on contractile properties of the triceps surae muscle at rest.

VA

Individual data for the measurements pre- and posttraining are illustrated in Fig. 2. The mean VA value was 94.8 ± 6.7% at baseline and 97.7 ± 2.1% at the end of the 16 wk, thus showing a slight (+3.7 ± 9.5%, P = 0.03) but significant relative increase [(%VA posttraining - %VA pretraining)/%VA pretraining · 100], with a concomitant tendency for a decline in variability as training progressed. Even excluding the two different outliers pre- and posttraining (indicated in Fig. 2 with asterisks), the increase in VA still remained significant (P = 0.02). The one-sample t-test revealed that VA at pretraining was significantly different from 100% (P = 0.015) and remained significantly lower (P = 0.002) posttraining. This would indicate, in both cases, a relatively high, but still incomplete, activation level. A negative correlation (r2 = 0.812, P < 0.001) was also observed between the baseline activation and the training effect (%VA increase), excepting for the subject who presented a slight decrease in VA after the 16 wk and obviously the outlier with the larger gain (Fig. 3). This suggests that the greatest deficit of activation before the conditioning period corresponds to the greatest increase after training. The ICC of the measurements of VA repeated over 4 consecutive days was 0.88, indicating good reproducibility of these measurements.


View larger version (12K):
[in this window]
[in a new window]
  		Fig. 2.   Voluntary activation (%) calculated from MVCs of plantar flexor muscles before and after 16 wk of training. open circle , Individual data points (n = 14); , means ± SD for each measurement. dagger  Pre- vs. posttraining is statistically different, P < 0.05. *, the two outliers, pre- and posttraining.



View larger version (12K):
[in this window]
[in a new window]
  		Fig. 3.   Relationship between %increase in voluntary activation (VA) after training and VA at baseline for all subjects (). A negative correlation was found between these 2 variables (r2 = 0.81, P < 0.001), excluding the subject who presented a slight decrease of VA after training and the outlier with the larger gain. open circle , Excluded values.

Pta-Voluntary Torque Relationship

The relationship between extra force produced by the interpolated twitch and levels of voluntary isometric torque appears with inverted variables in Eq. 1, because the function fulfilling the imposed constraints (see METHODS) could not be reversed due to the lack of a unique solution. As a consequence, the regression analysis estimates the coefficients by minimizing the horizontal distances between the experimental data and the equation (in the graph shown in Fig. 1, for example), rather than the vertical ones. However, the very high correlation coefficient of individual regressions (0.99 < r2 < 0.94; P < 0.001) suggests that such an approximation should be considered as negligible.

The studied Pta-torque relationship appears to be nonlinear. More specifically, amplitude of the Pta decreases almost linearly with torque in the submaximal torque range, but this effect is progressively lower, with a trend to even out, when the voluntary isometric contraction approaches 100%. The regression, which was found to fit the whole range of torque values, was a composite equation, with a curvilinear (exponential) and a linear component. The individual fitting by Eq. 1 enabled estimation of the expected value of MVC (MVCexp) for zero Pta (Fig. 1 and Table 1), i.e., the maximal voluntary isometric torque that the subject would be able to produce when attaining whole muscle activation. This parameter (MVCexp expressed as a percentage of the MVC observed) did not show any significant difference between the pre- (107.1 ± 10.9%) and posttraining (105.1 ± 4.8%) condition, but in both cases it was significantly higher than the MVC performed (P = 0.008 pre, and P = 0.002 post, Fig. 4). Furthermore, a significant increase in the absolute values of MVCexp was observed subsequent to the strengthening program (109.6 ± 33.6 vs. 122.3 ± 30.4 N · m, P = 0.04), which is quite in line with the improvement in MVC observed (15.8 vs. 17.8%).


View larger version (15K):
[in this window]
[in a new window]
  		Fig. 4.   Comparison of the MVC (open bars) and MVCexp (solid bars) presented as absolute values before and after the training program. Values are means ± SD. * Pre- vs. posttraining is statistically different, P < 0.05. ** MVC vs. MVCexp is statistically different, P < 0.01.

It was also possible to estimate the expected Pt (Pt exp) for MVC = 0%. The comparison with the observed mean Pt (Pt obs) value highlighted a significant gap. It has been observed that the Pt exp was higher than the Pt obs for either pre- (+6.0 ± 9.1%, P = 0.008) or posttraining (+13.9 ± 15.0%, P = 0.001) evaluations (Tables 1 and 2).

Pt exp/MVCexp, consequently derived, did not show any statistically significant modifications with training (Table 1), as opposed to Pt obs/MVC (Table 2).

The %MVC, at which the relationship with Pta changes from linear to curvilinear, was presented as a mean value in 9 subjects for the evaluation before training and in 11 subjects for the evaluation after training, because the other subjects showed a linear Pta-voluntary isometric torque relationship. This suggests that the descriptive ability of the chosen function incorporates both curvilinear and linear relationships; in the latter case, coefficients b and c are equal to 1 and 0, respectively. Finally, it appears that the departure from linearity for k = 1.5 (see METHODS) occurred at a similar %MVC, when pre- and posttraining conditions are compared (64.0 ± 15.2 and 65.2 ± 3.2% MVC, respectively), as illustrated in Fig. 5.


View larger version (12K):
[in this window]
[in a new window]
  		Fig. 5.   Point at which the relationship between extra force and maximal isometric torque change from linear to exponential. The fraction of Pta at which the curvature deviates >1.5 times from the linear slope was calculated from the first derivative of Eq. 1. The corresponding contraction intensity is obtained from Eq. 1 by substituting the Pta value (see METHODS). Small circles, individual data points (pretraining n = 9, posttraining n = 11); large circles, means ± SD; open circle , pretraining; , posttraining.

H Reflex and M Wave

In the investigated senior group, it was found that the Hoffmann reflex could be elicited only in 11 out of 14 subjects. The results were compared with those obtained in young adults formerly tested in our laboratory. It was found that the Hmax-to-Mmax was 42% lower (P = 0.02) in the elderly compared with the younger group. This difference is due to a larger depression of the Hmax (-64%, P = 0.005) compared with Mmax peak-to-peak amplitude (-44%, P = 0.007, Table 3) with aging.

                              
View this table:
[in this window]
[in a new window]
  		Table 3.   Motoneuron excitability and conduction velocity

Furthermore, regular resistance training in old age did not induce adaptive changes in the excitability of the H-reflex loop. As a matter of fact, no statistically significant differences were found in Hmax and Mmax amplitudes or in the Hmax-to-Mmax during the course of the 16-wk strength training. Anyway, it has to be taken into account that the absence of significant modifications might also be related to the great intersubject variability of the reflex response, as observed in our elderly population (see Table 3). The ICC of measurements repeated over 3 consecutive days before training was 0.74 for Hmax and 0.79 for Mmax, indicating quite a high reliability of both evaluations.

The mean latency time of the two responses was measured to detect possible changes in the signal conduction velocity through the reflex and the direct motor pathway. At baseline, older participants presented a longer mean H conduction time than the younger counterparts (+11%, P = 0.004), whereas no difference of M latency was observed. Even in this case, measurements were not significantly modified by the exercise. The linear relationship between the body height and the H-M interval, observed by Guiheneuc and Bathien (19) in adults, was maintained in our older population (r = 0.7; P = 0.01). Such correlation enabled the estimation of the H index for each subject. The mean value showed at pretraining was 75.2 ± 10.4, considering that the equation to assess the H index has been drawn so as to obtain a value close to 100 in healthy young subject (19), as confirmed by the value obtained from our younger population (105.8 ± 13.1). The significant difference between the two groups (29%, P < 0.001) confirms the reduction in nerve conduction velocity with aging, which, furthermore, does not appear to be modified by exercise, because no significant variation was observed over the course of the training period (Table 3).


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

MVC and Weight-lifting Capacity

The present study confirms that older adults, aged between 65 and 80 yr, positively respond to a high-resistance training program in terms of increments in maximal isometric torque and weight-lifting capacity of the PF. One noteworthy observation is the lack of a significant difference between the increase in extrapolated 1 RM (24%) and MVC (18%). This finding contrasts with the majority of studies in young adults (41), as emphasized by the results of Jones and Rutherford (25), of a 250% improvement in weight-lift capacity but just a 15% increase in MVC after a 12-wk strengthening program. A general explanation for the larger increase in 1 RM, compared with the static measurement, is that increments in strength after training may be limited to specific movement patterns. Therefore, it is not the first time that a lower degree of specificity in the training response has been observed in the aged (compare Ref. 37). It seems that, at least for the PF, dynamic strength training in older adults may lead to smaller improvements in the ability to coordinate synergist muscle and fixator muscle function (39). Nevertheless, this explanation will need to be borne out by further investigations, given the present lack of consensus, with several studies upholding the validity of the principle of specificity of training even in the elderly (8).

Contractile Properties

The contractile characteristics of our older group, before training, present the typical traits of elderly muscle, with slower contraction kinetics compared with literature values for young adults (21, 47). One noteworthy finding, after strength training, was the significant decrease in CT with a concomitant increase in Pt/CT, despite the fact that there were no changes in HRT and Pt. These reports are in agreement with results obtained by Duchateau and Hainaut (15) after 16 wk of dynamic strength training in young adults but differ from some of the results obtained from senile muscle. In fact, Rice et al. (37) reported an increase in CT of the triceps brachii, whereas Brown et al. (8) observed a significant increment in HRT on the elbow flexors, after dynamic strength training in older subjects.

Key factors that may be held responsible for faster CT and greater Pt/CT could be related to changes in the excitation-contraction coupling process, to an increased shortening velocity of muscle fibers, and, possibly, to modifications in myotendinous stiffness (37). Several studies have provided experimental evidence that changes in CT may be associated with quantitative as well as qualitative modifications of the sarcoplasmic reticulum (volume, density, and calcium release and recapture kinetics) and correlated with myosin ATPase activity (4). Because similar adaptations have been observed after strength training in aged lower mammals (29), it could be speculated that a prolonged period of increased loading might induce an enhancement in ATPase activity and calcium kinetics (15). Yet the reduction of CT after training may also be related to changes in the spread of excitation through the transverse tubular system. Even if EMG were not recorded during the percutaneous muscle stimulation, an additional analysis of the maximal M wave recorded from the soleus muscle, before and after training, showed no differences in terms of amplitude (see Table 3) but also in terms of conduction time (M wave peak-to-peak duration: 3.2 ± 1.0 ms pretraining vs. 3.1 ± 0.9 ms posttraining). Thus these observations suggest that the acceleration of the twitch time course is not associated, in this case, with a faster electrical propagation due to an enhancement in muscle membrane excitability. It has to be added that the shorter CT might account for the lack of increase in Pt, despite the improvement in maximal voluntary torque. Indeed, the reduced CT would decrease the time available to the contractile elements to stretch the series elastic component (SEC) and, consequently, result in a smaller Pt.

VA and Expected MVC

In the present study, the capacity of older adults to employ all available motor units was evaluated by using the twitch interpolation technique (2, 3). This technique has for long been regarded has the "gold standard" for the assessment of activation capacity (2, 7, 8, 22, 36, 46, 48), and several authors reported no difference when comparing single twitches, doublets, quadruplets, and quintuplets (3, 6, 24). On the other hand, more recent studies indicate that the use of pulse-train stimulation may be more reliable than single pulses, because this technique may enable assessment of both recruitment and activation (5, 12, 28, 32, 45, 49). However, tetanic stimulation is undoubtedly painful. Therefore, in view of these unsettled opinions regarding the choice of single or multiple pulses and to minimize discomfort in older individuals, we opted for the more frequently used method to detect muscle activation deficit in older individuals, based on single pulses (2, 7, 8, 22, 36, 46, 48).

Our results provide evidence that VA achieved before training was incomplete (94.8%). This conclusion also appears to be supported by the estimated MVC values. Indeed, both pre- and posttraining, the higher values of the expected vs. the observed MVC (Fig. 1) indicate that there is a discrepancy between what can be voluntarily performed and what might be achieved for total twitch occlusion. Belanger and McComas (7) observed that young adults had similar difficulty in reaching full motor unit activation during MVCs. It has been proposed that this suboptimal activation capacity may be a muscle-specific limitation to force generation, rather than a consequence of age-related disuse. As a matter of fact, Dowling et al. (14) suggested that certain muscles could not be fully activated during voluntary efforts, thereby limiting the expression of maximal force production. In this context, it seems noteworthy that the present group of moderately active older men has preserved an almost maximal VA capacity of the PF. This contrasts with the observations of Harridge et al. (22) and Winegard et al. (48), indicating an ~20% reduction in activation capacity of the quadriceps femoris and PF muscles in octogenarian men. It is plausible that the lower activation level, observed by these authors, may partially depend on the higher mean age of their experimental groups (88 and 81 yr, respectively). This appears to be in line with the observation that the eldest subject in our study (80 yr) showed, pretraining, the greatest deficit in VA and the largest increase after the conditioning period (71.9 vs. 98.5%), whereas the "youngest" volunteer (65 yr) showed no modification (99.3 vs. 99.2%), suggesting a presumable age-related effect on activation capacity. More generally, given the negative correlation (r2 = 0.812, P < 0.001) between the training effect (%VA increase) and the baseline activation, it appears that the greatest deficit of VA at baseline corresponds to the greatest increase after training (Fig. 3). On the other hand, the preserved activation capacity of the dorsiflexors observed in very old subjects by Winegard et al. (48) suggests that the discrepancy in central activation among muscles is probably associated with differences in their patterns of use.

Conversely, it is also plausible that disuse, as well as physical deconditioning, may justify the significant increase in VA (3.7%) after training. However, it should be pointed out that even a 5% increase in activation may not have an effect on MVC (12) and, as such, the functional significance of this increase in VA should be viewed with caution. In fact, De Serres and Enoka (12) argued that, in the interpolation technique, the signal-to-noise ratio is too low to make definitive conclusions about such small changes. Yet the fact that the relative MVCexp (%MVC observed) did not increase significantly with exercise argues against an improvement in motor unit activation. Thus, according to these observations and given the greater reliability of this alternative approach, we may conclude that the increase in VA is probably not a training effect.

Surprisingly, Pt/MVC decreased after training (Table 2), which could indicate the presence of neural adaptations. However, taking into account that the shorter CT might justify the lack of increase in Pt, it follows that the contribution of muscular factors cannot be excluded. Therefore, the widely held view that a major portion of the strength gain, induced by training older adults, is due to changes in neural drive (17, 20) seems partly challenged by the results of this study. Also, measurements of PF cross-sectional area performed in these subjects showed an increase of 9% after training, thus suggesting that hypertrophy, or intrinsic changes of the contractile tissue, exerted a greater contribution to the gain in torque than did neural factors (34).

Pta-Voluntary Torque Relationship

As previously observed in young adults, the relationship between the extra force produced by the interpolated twitch and the levels of voluntary isometric torque is nonlinear, thus indicating a near-maximal activation capacity for a submaximal voluntary torque (3, 7, 9, 12, 14, 36, 39). Moreover, the shape of this relationship seems to be muscle specific, as is also the capacity of attaining complete motor unit activation (7). Using the best curve-fitting procedure, previous authors have fitted the experimental points with an exponential (14) or a third-order polynomial function (12). However, in both cases, the regression line often did not intersect the x-axis, and, as a result, prediction of the MVC corresponding to complete muscle activation was not always possible. This drawback was overcome by Phillips et al. (36) with a procedure involving linearization of the evoked force, preserving a reasonable least squares fit of the data. In the present investigation, care was taken to preserve the method of the best fitted regression to identify a function that satisfied the requirements for intersection of the axis at relevant points, allowing us to estimate a MVCexp and a Pt exp. At the same time, we were able to describe a linear plus curvilinear data set and, consequently, locate the contraction intensity at the transition point. The departing from linearity may be caused by several factors, including an increasing mechanical contribution of synergistic muscles at high-torque levels of voluntary plantar flexion, as well as a modification of motor unit activation pattern (recruitment vs. rate coding). It has, in fact, been shown that, for certain muscles, the majority of the motor units are recruited for submaximal levels of effort (11). The departure from linearity could also be attributed to the progressive stretching of the SEC. Because of the viscoelastic properties of this component, damping of the twitch would be higher at low-force levels (when the SEC is more slack) but would be very low when the SEC is fully stretched, i.e., at high-force levels. It is likely that the higher value of the Pt exp compared with the observed measure could be attributable to the fact that the model proposed in the present study does not take into account the tensile properties of the SEC. It seems, in fact, that, for the weaker levels of efforts, the relationship between extra force and voluntary torque may not be strictly linear (7, 9) because of the slack of the SEC. On the other hand, above ~20% MVC, a considerable part of the slack is taken up by the contractile component, and the SEC are probably stretched enough so that the muscle could reach true isometric conditions earlier in time and thus, presumably, at a length closer to optimum muscle length. Accordingly, with this assumption, we may hypothesize that the extrapolation technique enables determination of a Pt response as if it were evoked in the same conditions of the Pta, thus justifying the relevance in Pt exp/MVCexp. Again, the absence of neural adaptations was suggested by the fact that, differently from Pt/MVC (see previous session), the expected ratio was not modulated by training.

The present study, therefore, confirms the nonlinearity of the relationship between the extra force and voluntary torque for older subjects, as previously observed for young adults. However, it would be interesting if further studies could investigate whether age contributes to the departure from linearity of this curve. For instance, given the marked reduction in motor unit discharge rate in old age (26), a later deviation from linearity in the elderly compared with young adults could be hypothesized.

H Reflex and M Wave

Our results provide further evidence of the progressive age-related impairment of the neuromuscular system at the peripheral and spinal level as reported in the literature (1, 13, 18, 30, 33, 38, 40, 46). The attenuation of the Hmax-to-Mmax ratio in this older group, compared with a population of younger adults, points to a decrease in the proportion of the available motor units reflexively recruited. The mechanisms responsible for the age-related decrease in reflex excitability may be associated with changes affecting interneurons, as well as both the afferent and efferent pathways, inducing an increased temporal dispersion of impulses. This may result in an increased presynaptic inhibition of Ia afferent fibers (33) and in random degenerative changes in both sensory and motor axons (1, 30), leading to progressive loss of spinal motoneurons and of the number of functioning motor units with aging (38, 47). The significantly longer reflex latency exhibited by the older adults, together with the maintained direct motor time, suggest specific alterations at the afferent level. This may be associated with a modified conduction velocity of Ia afferents and/or a decreased synaptic transmission efficacy. On the other hand, the functionality of the neuromuscular junction and efferent conduction speed seems to be maintained.

Several studies in young subjects have addressed the differences in the Hmax- to-Mmax ratio among sedentary and/or differently trained athletes (10, 35), thus suggesting that habitual physical activity may influence the excitability of the spinal reflex pathway. In young adults, strength training and overloading in particular have been shown to influence neural factors such as nerve conduction velocity (27), motoneuron excitability (43), and nerve fiber diameter (16). Thus the hypothesis was put forward that, even in old age, remodeling of neural structures involved in the reflex arc might occur in response to training to mitigate the decline in excitability (13, 40, 46). Had this occurred, a facilitation of the H-reflex recruitment would have been expected, but our results showed that neuromuscular excitability and nerve conduction velocity were not modified by a 16-wk strength-training program. The lack of modifications in the Hmax-to-Mmax ratio and in the H index suggests that regular training in the elderly does not induce adaptations in afferent and efferent fibers, interneuronal structures, or modulation in synaptic transmission efficacy, as well as in neuromuscular junction function. In other words, the whole inhibitory and excitatory effects that may influence the alpha -motoneuron pool efficiency do not seem to be influenced by a prolonged period of resistive loading. The absence of adaptive responses seems to indicate that the decrease in the Hmax-to-Mmax ratio and nerve conduction velocity with age could be mainly due to degenerative phenomena rather than disuse. However, it cannot be excluded that the lack of modulation of the H reflex may be due to the rather short period of physical intervention of the present study, because adaptations of the reflex arc have been observed after very long periods of habitual physical activity (35).

Conclusions

This study has shown that muscle activation capacity of the PF is well preserved in fairly active older men aged 65-80 yr. Conversely, a lower Hmax-to-Mmax ratio and a slower nerve conduction velocity were found compared with a younger group of adults, with no modulation after training. These findings confirm an impaired functionality of the peripheral neuromuscular system in old age. Hence, regular resistive exercise does not seem to influence the peripheral segment reflex loop. The absence of adaptive responses suggests that the depression in reflex amplitude in old age could be mostly due to degenerative phenomena.

In older individuals, as already demonstrated in young subjects, the PF motor unit recruitment proceeds in a nonlinear fashion. This suggests that, at high contraction intensities, a substantial contribution of 1) other neural factors, such as the rate coding, 2) a more efficient force transmission due to stretching of the SEC, and 3) an increased mechanical contribution of synergistic muscles may occur.


    ACKNOWLEDGEMENTS

We are particularly grateful to the senior citizens of Pavia who volunteered to take part in this study.


    FOOTNOTES

The authors thank TECHNOGYM Italia for generous support of this research project.

Address for reprint requests and other correspondence: G. Scaglioni, Groupe Analyse du Mouvement, UFR STAPS, Faculté des Sciences du Sport, PO Box 27877, Université de Bourgogne, 21078 Dijon Cedex, France (E-mail: gscaglioni{at}fsm.it).

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

First published February 8, 2002;10.1152/japplphysiol.00367.2001

Received 19 April 2001; accepted in final form 30 January 2002.


    REFERENCES
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

1.   Adinolfi, AM, Yamuy J, Morales FR, and Chase MH. Segmental demyelination in peripheral nerves of old cats. Neurobiol Aging 12: 175-179, 1991.

2.   Allen, GM, Gandevia SC, and McKenzie DK. Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 18: 593-600, 1995.

3.   Allen, GM, McKenzie DK, and Gandevia SC. Twitch interpolation of the elbow flexor muscles at high force. Muscle Nerve 21: 318-328, 1998.

4.   Alway, SE, MacDougall JD, and Sale DG. Contractile adaptations in the human triceps surae after isometric exercise. J Appl Physiol 66: 2725-2732, 1989.

5.   Behm, D, Power K, and Drinkwater E. Comparison of interpolation and central activation ratios as measures of muscle inactivation. Muscle Nerve 24: 925-934, 2001.

6.   Behm, DG, St-Pierre DM, and Perez D. Muscle inactivation: assessment of interpolated twitch technique. J Appl Physiol 81: 2267-2273, 1996.

7.   Belanger, AY, and McComas AJ. Extent of motor unit activation during effort. J Appl Physiol 51: 1131-1135, 1981.

8.   Brown, AB, McCartney N, and Sale DG. Positive adaptations to weight-lifting training in the elderly. J Appl Physiol 69: 1725-1733, 1990.

9.   Bulow, PM, Norregaard J, Danneskiold-Samsoe B, and Mehlsen J. Twitch interpolation technique in testing of maximal muscle strength: influence of potentiation, force level, stimulus intensity and preload. Eur J Appl Physiol 67: 462-466, 1993.

10.   Casabona, A, Polizzi MC, and Perciavalle V. Differences in H-reflex between athletes trained for explosive contractions and non-trained subjects. Eur J Appl Physiol 61: 26-32, 1990.

11.   De Luca, CJ, LeFever RS, McCue MP, and Xenakis AP. Behaviour of human motor units in different muscles during linearly varying contractions. J Physiol 329: 113-128, 1982.

12.   De Serres, SJ, and Enoka RM. Older adults can maximally activate the biceps brachii muscle by voluntary command. J Appl Physiol 84: 284-291, 1998.

13.   DeVries, HA, Wiswell RA, Romero GT, and Heckathorne E. Changes with age in monosynaptic reflexes elicited by mechanical and electrical stimulation. Am J Phys Med Rehabil 64: 71-81, 1985.

14.   Dowling, JJ, Konert E, Ljucovic P, and Andrews DM. Are humans able to voluntarily elicit maximum muscle force? Neurosci Lett 179: 25-28, 1994.

15.   Duchateau, J, and Hainaut K. Isometric or dynamic training: differential effects on mechanical properties of a human muscle. J Appl Physiol 56: 296-301, 1984.

16.   Edds, MV. Hypertrophy of nerve fibers to functionally over-loaded muscles. J Comp Neurol 93: 259-275, 1950.

17.   Enoka, RM. Neural adaptations with chronic physical activity. J Biomech 30: 447-455, 1997.

18.   Falco, FJ, Hennessey WJ, Goldberg G, and Braddom RL. H reflex latency in the healthy elderly. Muscle Nerve 17: 161-167, 1994.

19.   Guiheneuc, P, and Bathien N. Two patterns of the results in polyneuropathies investigated with the H reflex. Correlation between proximal and distal conduction velocities. J Neurol Sci 30: 83-94, 1976.

20.   Häkkinen, K, Alen M, Kallinen M, Newton RU, and Kraemer WJ. Neuromuscular adaptation during prolonged strength training, detraining and re-strength-training in middle-aged and elderly people. Eur J Appl Physiol 83: 51-62, 2000.

21.   Harridge, SD, Bottinelli R, Canepari M, Pellegrino MA, Reggiani C, Esbjornsson M, and Saltin B. Whole-muscle and single-fibre contractile properties and myosin heavy chain isoforms in humans. Pflügers Arch 432: 913-920, 1996.

22.   Harridge, S, Kryger A, and Stensgaard A. Knee extensor strength, activation, and size in very elderly people following strength training. Muscle Nerve 22: 831-839, 1999.

23.   Hart, BA. Fractionated myotatic reflex times in women by activity level and age. J Gerontol 41: 361-367, 1986.

24.   Herbert, RD, and Gandevia SC. Twitch interpolation in human muscles: mechanisms and implications for measurement of voluntary activation. J Neurophysiol 82: 2271-2283, 1999.

25.   Jones, DA, and Rutherford OM. Human muscle strength training: the effects of three different regimes and the nature of the resultant changes. J Physiol 391: 1-11, 1987.

26.   Kamen, G, Sison SV, Du CC, and Patten C. Motor unit discharge behavior in older adults during maximal-effort contractions. J Appl Physiol 79: 1908-1913, 1995.

27.   Kamen, G, Taylor P, and Beehler PJ. Ulnar and posterior tibial nerve conduction velocity in athletes. Int J Sports Med 5: 26-30, 1984.

28.   Kent-Braun, JA, and Ng AV. Specific strength and voluntary muscle activation in young and elderly women and men. J Appl Physiol 87: 22-29, 1999.

29.   Klitgaard, H, Marc R, Brunet A, Vandewalle H, and Monod H. Contractile properties of old rat muscles: effect of increased use. J Appl Physiol 67: 1401-1408, 1989.

30.   Lascelles, RG, and Thomas PK. Changes due to age in internodal length in the sural nerve in man. J Neurol Neurosurg Psychiatry 29: 40-44, 1966.

31.   Maffiuletti, AN, Martin A, Babault N, Pensini M, Lucas B, and Schieppati M. Elctrical and mechanical Hmax-to-Mmax ratio in power- and endurance-trained athletes. J Appl Physiol 90: 3-9, 2001.

32.   Miller, M, Downham D, and Lexell J. Superimposed single impulse and pulse train electrical stimulation: a quantitative assessment during submaximal isometric knee extension in young, healthy men. Muscle Nerve 22: 1038-1046, 1999.

33.   Morita, H, Shindo M, Yanagawa S, Yoshida T, Momoi H, and Yanagisawa N. Progressive decrease in heteronymous monosynaptic Ia facilitation with human ageing. Exp Brain Res 104: 167-170, 1995.

34.   Narici, MV. Structural and Functional Adaptations to Strength Training in the Elderly. The Ageing Motor System and Its Adaptations to Training. Pavia, Italy: Maugeri Foundation Books, 2000, p. 55-59.

35.   Nielsen, J, Crone C, and Hultborn H. H-reflexes are smaller in dancers from The Royal Danish Ballet than in well-trained athletes. Eur J Appl Physiol 66: 116-121, 1993.

36.   Phillips, SK, Bruce SA, Newton D, and Woledge RC. The weakness of old age is not due to failure of muscle activation. J Gerontol 47: M45-M49, 1992.

37.   Rice, CL, Cunningham DA, Paterson DH, and Dickinson JR. Strength training alters contractile properties of the triceps brachii in men aged 65-78 years. Eur J Appl Physiol 66: 275-280, 1993.

38.   Roos, MR, Rice CL, and Vandervoort AA. Age-related changes in motor unit function. Muscle Nerve 20: 679-690, 1997.

39.   Rutherford, OM, Jones DA, and Newham DJ. Clinical and experimental application of the percutaneous twitch superimposition technique for the study of human muscle activation. J Neurol Neurosurg Psychiatry 49: 1288-1291, 1986.

40.   Sabbahi, MA, and Sedgwick EM. Age-related changes in monosynaptic reflex excitability. J Gerontol 37: 24-32, 1982.

41.   Sale, DG. Neural adaptation to resistance training. Med Sci Sports Exerc 20, Suppl 5: S135-S145, 1988.

42.   Sale, DG, and MacDougall JD. Specificity in strength training: a review for the coach and athlete. Can J Appl Sport Sci 6: 87-92, 1981.

43.   Sale, DG, MacDougall JD, Upton AR, and McComas AJ. Effect of strength training upon motoneuron excitability in man. Med Sci Sports Exerc 15: 57-62, 1983.

44.   Schieppati, M. The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man. Prog Neurobiol 28: 345-376, 1987.

45.   Stackhouse, SK, Dean JC, Lee SC, and Binder-MacLeod SA. Measurement of central activation failure of the quadriceps femoris in healthy adults. Muscle Nerve 23: 1706-1712, 2000.

46.   Vandervoort, AA, and Hayes KC. Plantarflexor muscle function in young and elderly women. Eur J Appl Physiol 58: 389-394, 1989.

47.   Vandervoort, AA, and Mc Comas AJ. Contractile changes in opposing muscles of human ankle joint with aging. J Appl Physiol 61: 361-367, 1986.

48.   Winegard, KJ, Hicks AL, Sale DG, and Vandervoort AA. A 12-year follow-up study of ankle muscle function in older adults. J Gerontol A Biol Sci Med Sci 51: B202-B207, 1996.

49.   Yue, GH, Ranganathan VK, Siemionow V, Liu JZ, and Sahgal V. Older adults exhibit a reduced ability to fully activate their biceps brachii muscle. J Gerontol A Biol Sci Med Sci 54: M249-M253, 1999.

J APPL PHYSIOL 92(6):2292-2302
8750-7587/02 $5.00 Copyright © 2002 the American Physiological Society


This article has been cited by other articles:


Home page
 J. Appl. Physiol.Home page
S. K. Hunter, G. Todd, J. E. Butler, S. C. Gandevia, and J. L. Taylor
Recovery from supraspinal fatigue is slowed in old adults after fatiguing maximal isometric contractions
J Appl Physiol, October 1, 2008; 105(4): 1199 - 1209.
[Abstract] [Full Text] [PDF]

Home page
 J. Gerontol. A Biol. Sci. Med. Sci.Home page
B. C. Clark and T. M. Manini
Sarcopenia != Dynapenia
J. Gerontol. A Biol. Sci. Med. Sci., August 1, 2008; 63(8): 829 - 834.
[Abstract] [Full Text] [PDF]

Home page
 J. Gerontol. A Biol. Sci. Med. Sci.Home page
K. Kubo, Y. Ishida, T. Komuro, N. Tsunoda, H. Kanehisa, and T. Fukunaga
Age-Related Differences in the Force Generation Capabilities and Tendon Extensibilities of Knee Extensors and Plantar Flexors in Men
J. Gerontol. A Biol. Sci. Med. Sci., November 1, 2007; 62(11): 1252 - 1258.
[Abstract] [Full Text] [PDF]

Home page
 J. Gerontol. A Biol. Sci. Med. Sci.Home page
M. D. de Boer, C. I. Morse, J. M. Thom, A. de Haan, and M. V. Narici
Changes in Antagonist Muscles' Coactivation in Response to Strength Training in Older Women