INTRODUCTION

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IT HAS BEEN SUGGESTED THAT an inability to maximally activate a muscle, or muscle group, during an isometric maximal voluntary contraction (MVC) may be an important factor in explaining the frequent observation of a greater loss of force with age relative to the loss of muscle mass (25, 33, 40). This is an important concept in understanding the loss of strength that occurs with age. Various versions of the twitch interpolation technique (1, 21, 23, 24, 26, 31, 33) have been used to test the voluntary activation abilities of young and old (34) and of healthy and unhealthy subjects (2, 21, 25, 35) in many different skeletal muscles. Twitch interpolation is a method to measure voluntary muscle activation by delivering one or a brief series of electrical stimuli to the motor axons of a muscle during a voluntary effort contraction (1, 4, 17).

In young healthy adults it seems that maximal voluntary activation can be realized in most muscles (1, 5, 16, 19). However, in old adults results are controversial; some studies indicate that voluntary activation in old adults does not differ from that in young adults (11, 18, 20, 26, 28, 33, 36, 40), whereas others report that old and young adults differ in their activation ability during a MVC (6, 15, 24, 38, 41). The majority of these studies have tested lower limb muscles, and, except for studies (5, 40) in which maximal voluntary activation was assessed in both plantar flexor and dorsiflexor muscles, only single muscle groups have been studied in any subject group.

One potential problem, not addressed systematically, with trying to compare and understand results from studies in old adults is whether and to what extent the task of making a maximal isometric contraction has been practiced. Recently, it has been reported that the variability associated with producing isometric MVCs increases with age (9) and that the rate of learning a task is slower in old adults compared with young adults (10, 39). In addition, daily activities are conducted at submaximal intensities, and with age a more sedentary lifestyle is usually adopted (7), which may lead to fewer moderate-effort contractions. These factors relate to the decline in physical fitness and altered perception of effort found with old age (21, 30). Thus it seems reasonable to suggest that more practice with producing a MVC would be required in advanced age.

Some studies that have evaluated muscle activation in old adults report that an accommodation session was given (3, 23), other studies have given no practice at MVC (38), whereas in others the MVC was recorded as the highest value that was produced over three sessions (28). Not only do the number of sessions given to produce a MVC differ between studies but also the number of attempts within one session ranges between two and five (6, 12, 41), and maximal voluntary activation has been measured from both the contraction that produced the greatest force (12, 41) and an average of the two highest forces (6). To date, no studies have reported whether the number of sessions, or attempts necessary to attain maximal voluntary activation differs between young and old healthy adults. However, studies in the elbow flexors of patient populations (2, 30) and healthy young adults (1, 16) indicate that learning does not occur with each consecutive attempt at MVC and that the degree of variability in producing maximal voluntary activation does not differ between sessions and within a single session (1).

The purpose of this study was to identify whether the number of sessions, or attempts within a session, required to achieve maximal voluntary activation of the elbow flexors and extensors differ between young and old adults. It was hypothesized that old adults would not attain maximal elbow flexor and elbow extensor activation as frequently as would young adults. Far fewer studies have evaluated age-related changes in arm muscles compared with lower limb and specialized hand muscles (34). Furthermore, it is clear that upper limb muscles are not activated habitually in a similar pattern and intensity as lower limb muscles (27), suggesting that the confounding influence of activity patterns on muscle function and sarcopenia might vary between different limb muscle groups. Finally, studying a functional pair of upper limb muscles might provide insight into the differential age-related changes in strength that have been reported between limb muscles (20, 34).

	METHODS

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All subjects signed a written, informed consent according to the guidelines established by the local university review board. Elbow flexion and extension MVCs and voluntary activation were assessed in a supine position, on a modified padded examination table (23, 28). The left arm was supported beside the body on a platform that extended from the side of the table, and the elbow joint was flexed to 90° and the shoulders were secured to prevent flexion of the trunk and shoulder. The legs were elevated for comfort and as a means of preventing extraneous movement in the lower body, which might have influenced upper body positioning or force generation. The wrist was supinated for elbow flexion but placed in a neutral position (semipronated) for elbow extension. Detailed measures were made of each subject's body position to standardize the setup between the two test sessions.

Forces of elbow flexion and extension were recorded at the wrist by a strain-gauge device (model SST-700-100A, AS Technology, Haliburton, ON) that was mounted on the wrist plate of the dynamometer that was attached to the platform that extended from the edge of the table. The strain gauge was calibrated with known weights to confirm linearity (r = 0.99) and to convert volts to newtons of force (N). The output from the strain gauge was amplified (Neurolog, Digitimer, Welwyn Garden City, Hertfordshire, UK) and converted from analog to digital format by a 12-bit analog-to-digital converter at a sampling rate of 500 Hz (model 1401 Plus, Cambridge Electronic Design Science Park, Cambridge, UK) for off-line computer analysis. The force signal also was displayed in real time on an oscilloscope in front of the subject.

Electrical stimulation of the elbow flexor and elbow extensor muscle groups was applied percutaneously through carbon rubber stimulation electrodes (4 × 4.5 cm), which were tightly bandaged over the muscle group of interest. To stimulate the elbow flexor muscles, the cathode was placed diagonally across the motor point of the biceps brachii ~12 cm distal to the acromion process, and the anode was located over the distal tendon ~2 cm proximal to the cubital fossa. The elbow extensors were stimulated with the cathode situated diagonally across the proximal posterolateral portion of the long and lateral heads of the triceps brachii, and the anode was placed over the triceps brachii tendon ~4.5 cm proximal to the olecranon process. The modified twitch interpolation technique (14, 29) was utilized to assess voluntary activation ability. This technique consisted of applying a series of paired electrical pulses (2 pulses at 100 Hz) once per second to the muscle during and after each of the attempted 4- to 6-s MVCs (1, 4, 16). By use of a constant-voltage (400 V) stimulator, the intensity of the double pulses was increased by adjusting the current (DS7AH, Digitimer) until a level was attained that activated as much of the muscle as possible without interference from antagonists. Palpation, noticeable contraction of antagonists, or a decrement in force with an increase in current was used to determine involvement of antagonist muscles. Muscle activation was estimated from a ratio of the amplitude of the paired interpolated response, which occurred during the highest MVC force, to the amplitude of a potentiated post-MVC paired-pulse response [(1  superimposed twitch/posttwitch) · 100].

Maximal voluntary activation was defined as the twitch interpolation score that corresponded to the highest MVC, whereas mean voluntary activation was an average of the attempts at MVC. For all attempts at MVC, voluntary activation was measured, and subjects were instructed to either flex or extend their elbow joint as hard and as fast as possible and to sustain this effort for 4-6 s. Visual feedback and strong verbal encouragement were given for all attempts at MVC. Subjects performed five MVCs for each of the two muscle groups (elbow flexor and extensor) in each session. Three to five minutes of rest were given between each contraction, and 5-10 min rest were provided between the elbow flexion and elbow extension MVCs. The testing order of the two muscles was randomized and counterbalanced between the two test sessions.

The highest MVC with the corresponding maximal voluntary activation score were utilized to compare elbow flexion and extension MVCs and maximal voluntary activation between young and old men. Maximal scores were compared with a 2 × 2 (age × muscle group) ANOVA, whereas for the dependent variable of mean voluntary muscle activation and the standard deviation of voluntary activation the effect of session and attempts at MVC were examined with a 2 × 2 × 2 × 5 mixed ANOVA with repeated measures on muscle group, session, and attempts. Significant interactions were examined with Tukey's post hoc tests. Values are expressed as means ± SE. Differences were considered significant at the 5% level.

	RESULTS

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When the voluntary activation scores for all attempts at MVC were compared (4-way ANOVA), there was no statistical interaction between age, muscle, the two test sessions, and the order of MVCs attempted (P = 0.8), and there was no significant interaction between age groups, muscle groups, and the two testing sessions (P = 0.4). Thus the statistical results are presented for the two-way interactions.

The six young (24 ± 1 yr) and six old (83 ± 4 yr) men were similar in body mass (young, 79 ± 1.2 kg; old, 78 ± 0.8 kg) and height (young, 174 ± 0.5 cm; old 170 ± 0.6 kg;). Elbow flexion and extension MVC was less (43 and 47%, respectively) in the old men, yet the maximal voluntary muscle activation was similar between the two age groups (Table 1). The young men in this study achieved a 100% voluntary elbow flexion activation score on 28% of the attempts at MVC (Fig. 1), which is similar to the 25% value previously reported for this muscle group in healthy young men (1). For the old men, maximal elbow flexion activation was only realized for 15% of the attempts at MVC. For elbow extension, success in achieving maximal activation was similar between the young (38%) and old men (31%) and better than for the elbow flexors. Similar to a report by Allen et al. (1) of young men, the young man with the most variable voluntary activation scores ranged from 74 to 100%, but for an old subject the greatest range was 48-93%. Elbow extension activation variability was less than elbow flexors as indicated by the greatest range. In a young man, activation ranged from 89 to 100%, whereas in an old man it was 60-100%.

View larger version (18K): [in this window] [in a new window]   Fig. 1.   Individual voluntary activation scores for 6 subjects for the elbow flexors (A) and the elbow extensors (B) of young (left) and old (right) men. Open symbols, 5 attempts at maximal voluntary contraction for the first session; filled symbols, 5 attempts at maximal voluntary contraction in the second session. Each column of data corresponds to 1 subject.

When the standard deviation of voluntary activation for all attempts at MVC was assessed, there was a significant difference between age groups (P = 0.001; Fig. 2A), and muscle groups (P = 0.02; Fig. 2B), but not between sessions (P = 0.14). Thus both individual subject data and group standard deviation results indicate that muscle activation was more variable in the old men compared with the young men and that the elbow flexors were less consistent compared with the elbow extensors.

View larger version (12K): [in this window] [in a new window]   Fig. 2.   Differences in the standard deviation of voluntary activation between age groups (A) and muscle groups (B). The standard deviation of activation is the variability score averaged for the 2 sessions. The average for each session is the mean of 5 attempts at maximal voluntary contraction within a session. *Significant difference, P < 0.05.

When the voluntary activation scores for all 10 attempts at MVC were compared, there was a significant interaction between age and muscle groups (P = 0.0001; Fig. 3A). Tukey's post hoc multiple comparisons indicated that in both muscle groups the mean muscle activation was greater in the young men, compared with the old men, and that elbow extensor activation was greater than elbow flexor activation in the old men. In addition, there was a significant interaction between age and test session (P = 0.05; Fig. 3B). This interaction resulted from lower mean muscle activation in the old men, compared with the young men, during session 1, whereas during session 2, voluntary activation did not differ between age groups. Moreover, this interaction occurred because of the significant increase in elbow flexor mean voluntary activation between sessions 1 and 2 in the old men (~13%), whereas elbow extension activation was similar between sessions 1 and 2. The mean voluntary activation of both muscles in young men was similar to the elbow extensors of old men, and no difference was observed between sessions.

View larger version (10K): [in this window] [in a new window]   Fig. 3.   Comparison of voluntary activation scores for all 10 attempts at maximal voluntary contraction. There was a significant interaction (*P < 0.05) for muscle activation between age and muscle group (A) that resulted from a lower mean voluntary activation score in the old men compared with the young men in both muscle groups and from a difference between elbow flexion and extension activation in the old men. The significant interaction (*P < 0.05) between age and test session (B), collapsed across muscle groups, occurred as a result of a significant lower mean voluntary activation in the old men, compared with the young men, during session 1 but not session 2. Furthermore, voluntary activation differed between sessions 1 and 2 in the old men but not in the young men.

	DISCUSSION

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The primary purpose of this study was to determine whether young and old adults differ in the number of attempts required to maximally activate the elbow flexors and extensors as assessed with the twitch interpolation technique. The novel finding of this study was that the variability associated with producing MVCs results in a difference in the ability of young and old men to voluntary activate the elbow flexors. When the maximal elbow flexion and extension activation scores were utilized in the age comparison, there was no difference in activation ability between young and old men. However, in both muscles mean voluntary activation in old men was less during the first session compared with the second session, whereas in young men both mean and maximal voluntary activation did not differ between sessions and muscle groups. In the old men, the difference in voluntary activation between sessions occurred because mean elbow flexion activation was higher during the second session, and thus old men required a session to become familiar with producing elbow flexion MVCs but not elbow extension MVCs. Nevertheless, if sufficient attempts at MVC are provided, maximal voluntary activation can be attained in most subjects, at least once.

When the highest MVC and corresponding voluntary activation score were compared between young and old adults, maximal voluntary activation scores did not differ between age or muscle groups. Findings from this study of the elbow flexors and extensors, and prior studies from many different muscles (5, 11, 12, 28, 36, 40), report that the decrease in voluntary strength with age does not seem to be due to a decline in maximal voluntary activation. Yet, in contrast, Yue et al. (41) and Bilodeau et al. (6) suggested that in the elbow flexors the age-related decrease in strength could be partially attributed to a reduced ability to maximally activate the muscle. It is possible that these studies (6, 41) reported a difference in voluntary activation between young and old men because practice was not given to achieve MVC. When an accommodation session has been given (3, 23), or MVC was recorded as the highest value that was produced over three sessions (28), voluntary activation of the elbow flexors was similar between young and old men. In the present study, a difference was observed between sessions 1 and 2 for the elbow flexors of old men, and these data indicate that at least one session is required for old adults to become familiar with producing elbow flexion MVCs. For young men, the finding in the present study that voluntary activation does not differ between sessions for the elbow flexors and extensors is similar to results from prior studies of the elbow flexors in young men (1, 2).

A difference between young and old adults was observed in this study when the mean voluntary activation of all attempts at MVC was compared between age groups, and this is similar to results from prior studies when maximal voluntary activation was calculated as an average of the two highest forces from two or three attempts at elbow flexion MVC (6, 41). It is unlikely that differences observed between studies can be attributed to differences in stimulation methods employed because the maximal voluntary activation scores reported for young men in the present study are nearly identical to those in earlier studies (6, 41). Furthermore, in the present study the proportion of times old adults achieved maximal voluntary elbow flexion activation was considerably fewer than the young adults. Thus it is possible that differences exist between studies because of the manner in which maximal voluntary activation is defined and calculated. When maximal ability between age groups is compared, an average score is not appropriate. However, evaluation of MVCs over a number of trials provides an indication of MVC variability when comparing between age groups.

Muscle activation in old men was more variable than in the young men. Furthermore, elbow flexor activation was more variable than elbow extensor activation, irrespective of age. However, results from this study indicate that most subjects were able to attain maximal elbow flexion and extension voluntary activation, although they did not do so for all attempts at MVC. Because there was no improvement with each consecutive attempt at the five MVCs (P = 0.128), "learning" does not seem to occur.

To date, the ability to maximally activate a functional muscle pair in the arm of young and old men has not been studied. However, in the leg of old men, plantar flexor and dorsiflexor voluntary activation did not differ (40), whereas in young men activation was dissimilar between these muscle groups (5). It was speculated that the discrepancy in voluntary activation observed between the pair of leg muscles occurred in the young adults because of habitual activity or because differences that exist in excitatory monosynaptic connections between the plantar flexors and dorsiflexors (5). Little is understood about habitual activity patterns in the elbow flexors (27) and elbow extensors of young and old adults and how this relationship might change with age. However, the pattern of projections of corticospinal neurons (32) and group I afferents (8) differ between these muscle groups, and these differences might contribute to the variability in achieving voluntary activation between this functional pair with age. Moreover, in old men the difference between elbow flexion and extension activation might be accounted for by a greater age-related decrease in motor unit discharge rates in the biceps brachii, compared with the triceps brachii (22), because suboptimal discharge rates have been ascribed as a possible factor that might cause a decrease in voluntary activation (17, 29).

The utility of the twitch interpolation technique to be able to detect a true MVC has been questioned (1, 13, 17, 37). It has been reported that in some instances it may not be possible to distinguish between contractions of 60 and 100% of MVC (17) and that some studies only resolve force increments of 4-10% (1). The issue of the ability that this technique has to detect a true MVC is founded on the sigmoid shape of the relationship between the amplitude of the interpolated twitch and the voluntary force produced (4, 5, 17). However, the sigmoid curve was similar (data not shown, r = ~0.87) for the elbow flexors and extensors for a subset of young and old men in this study, and thus the assumptions that are inherent in this technique for measuring voluntary activation from a nonlinear relationship are similarly applied between these two age and muscle groups. Because a similar curvilinear relationship was observed, this technique can be utilized to make relative comparisons between the elbow flexors and extensors of young and old men.

Results from this study indicate that old men are not as consistent as young men in performing MVCs and that there is greater variability associated with attaining maximal voluntary elbow flexion activation, compared with elbow extension. In the old men, elbow flexion voluntary activation was greater during the second session compared with the first. When the highest maximal voluntary activation score was compared between age and muscle groups, there were no differences; however, for the 10 attempts at MVC, the mean voluntary activation score was significantly less in the old men compared with the young men. Thus evaluation of voluntary activation over a number of trials provides insight into performance differences between young and old adults. However, to determine whether maximal voluntary activation differs between young and old men, the highest value attained, not the mean of all attempts, should be utilized in the assessment, and a sufficient number of attempts needs to be given to attain the best MVC in old adults.