INTRODUCTION

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THE DECLINE IN MOTOR PERFORMANCE that accompanies healthy aging is attributable to a variety of physiological mechanisms, including adaptations that occur within the nervous system. The functional consequences of these adaptations include such effects as a decrease in the fine motor skills of the hand, a slowing of rapid arm movements, an alteration in the distribution of joint torques and powers in the leg during stepping down and walking, a reduced ability to detect joint displacement, and a decline in the capacity to accommodate disturbances of posture (7, 18, 24, 31, 42, 45, 49). These changes in performance must involve a reorganization of muscle activation, such as reductions in motor unit activity and alterations in the distribution of activity among the involved muscles. For example, older adults frequently exhibit heightened levels of antagonist muscle coactivation during the performance of goal-directed movements (4, 25, 41). This study examined another pattern of muscle activation that could contribute to differences in motor performance between young and old adults: activation of homologous muscles in the contralateral limb during the performance of a unilateral task.

Contractions at moderate-to-high forces are frequently accompanied by the activation of other ipsilateral and contralateral muscles (1, 2, 8, 52). When the intensity of the contralateral activity is sufficient to produce a movement, which can occur in children and in some pathological conditions, the behavior is referred to as a mirror movement (1, 12, 33). However, electromyographic activity can be observed in contralateral muscles in most healthy adults during unilateral contractions that require a substantial effort (5, 9, 14, 52). Although the unintended activity is sometimes described as contralateral irradiation, which can imply the spreading of excitation within the central nervous system, the neural mechanism underlying the contralateral activity may involve a reduction in transcallosal inhibition (1, 13, 15, 30, 46).

The purpose of the study was to compare the amount of contralateral activity produced by young and old adults when they performed unilateral isometric and anisometric contractions with a hand muscle. The contralateral activity was greater for the old adults, which indicates that they had a reduced ability to prevent unintended activity during the performance of unilateral goal-directed tasks. Furthermore, contralateral activity was less for both groups of subjects during anisometric contractions compared with isometric contractions. Some of these results have been presented previously in abstract form (23).

	METHODS

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Experiments were performed on the left and right hands of 10 young (5 women, 5 men; means ± SD 24.1 ± 5.3 yr; range 18-32 yr) and 10 old (5 women, 5 men; 72.5 ± 4.9 yr; range 66-80 yr) subjects with no known neuromuscular disorders. All subjects were right-hand dominant, as assessed by the Edinburgh Handedness Inventory (35), performed no more than minimal levels of physical activity on a regular basis and did not participate in activities that involved skilled activities with either hand (e.g., play a musical instrument, engage in racket sports, or ride a bicycle). The Institutional Review Board at the University of Colorado approved the experimental procedures, and all subjects gave informed consent before participation in the study.

Experimental Setup

Mechanical Recording

Isometric contractions. The test hand was placed in the manipulandum so that the index finger was in a neutral position. A force transducer (Sensotec model 13, Columbus, OH) attached to the splint detected the abduction force at the proximal interphalangeal joint of the index finger. The sensitivity of the transducer differed for high-force [40% maximal voluntary contraction (MVC) force; 0.045 V/N; linear range 0-220 N] and low-force tasks (10% MVC force; 0.45 V/N; 0-9.81 N).

Anisometric contractions. A low-friction, linear variable differential transducer (LVDT; novotechnik, Stuttgart, Germany) was used to detect the abduction-adduction displacement of the index finger about the first metacarpophalangeal joint during the position-tracking task. The LVDT was mounted on an extended delryn platform, and it was placed perpendicular to the proximal interphalangeal joint when the index finger was placed in the neutral position. The LVDT was attached to a waxed string that was directed over a pulley and connected to the finger splint at the proximal interphalangeal joint. The LVDT was calibrated for each subject and session over the range of motion. The loads lifted by the subject were suspended from the LVDT.

Contralateral activity. The subjects were not aware that the focus of the study was the contralateral activity. For each unilateral task (both isometric and anisometric contractions), the splinted index finger of the contralateral hand was secured to the force transducer with a Velcro strap. The force exerted by the index finger of the contralateral hand in the abduction direction due to an isometric contraction of the first dorsal interosseus muscle was measured with a low-sensitivity transducer (0.06 V/N; 0-220 N).

Electrical Recording

Experimental Procedures

MVC. The MVC task involved a gradual increase in the abduction force exerted by the index finger from baseline to maximum in 3-4 s and then sustained at maximum for 1-2 s. The index finger force was displayed on the monitor. The timing of the task was based on a verbal count given at 1-s intervals, with vigorous encouragement from the investigators when the force began to plateau. Each subject performed three MVC trials, with subsequent trials performed if the difference in peak force between two MVCs was >5%. The trial with the highest peak force was chosen for analysis.

Isometric contractions. The target forces, which were presented to the subject randomly, were set at 2.5, 10, 40, 60, and 80% MVC force. On the basis of feedback provided on the monitor, the subject gradually increased the abduction force to the target force and sustained it at this value for either 20 s (target forces < 50% MVC force) or 10 s (target forces > 50% MVC force). The sensitivity of the force display was set relative to the target force so that the distance from the baseline to the target force was kept constant across trials. The subject performed either two (target forces < 50% MVC force) or one (target forces > 50% MVC force) trial at each target force.

Anisometric contractions. The maximum load that each subject could lift once using the first dorsal interosseus muscle [one-repetition maximum (1-RM load)] was estimated from the MVC force of the subject. On the basis of a previously determined relation between 1-RM load and MVC force (4, 29), 1-RM load was set at 51% MVC force for young subjects and at 36% MVC for old subjects. Loads corresponding to 2.5, 10, 40, 60, 80, and 100% of the 1-RM load were attached in random order to the line and connected to the splint at the level of the proximal interphalangeal joint. Each load was first lifted (6 s) and then lowered (6 s) by moving the index finger through a 0.35-rad range of motion.

Fatiguing contractions. The last hand to perform the preceding set of three contractions then completed a sequence of 10 anisometric contractions with an 80% 1-RM load. Because of the random order in which the hands were tested, the fatiguing contractions were performed by 10 left and 10 right hands in these right-hand dominant subjects. The time between each contraction was 8 s. The subjects were not informed that the task involved 10 contractions until completion of the ninth contraction. To assess the level of fatigue caused by the 10 contractions, an MVC was performed immediately after the tenth anisometric contraction was completed.

Data Analysis

Dependent variables. The dependent variables for the isometric and anisometric tasks performed by each hand were the peak force and the average of the full-wave rectified EMG (AEMG) for a 0.5-s window centered at the peak force during the trial. The dependent variable for the fatiguing contractions was the AEMG during a 0.5-s window centered in the middle of the concentric and eccentric contractions (lifting and lowering the load). When each hand was being tested, the force and AEMG in the contralateral hand were also recorded. The dependent variables for the contralateral hand were the peak force and the associated AEMG for a 0.5-s window. The force and AEMG were expressed both in absolute values and normalized to the respective maximum values. For the conditions that involved two trials (<50% MVC force and 1-RM load), the trial with the largest value was used in the analysis.

Statistical analysis. The dependent variables for the MVC and 1-RM tasks were compared with a two-factor ANOVA (2 age groups × 2 hands) with repeated measures on hand. The dependent variables for the isometric contractions were compared with a three-factor ANOVA (2 age groups × 2 hands × 6 target forces) with repeated measures on hand and target force. The dependent variables for the anisometric contractions were compared with a four-factor ANOVA (2 age groups × 2 hands × 6 loads × 2 contraction types) with repeated measures on hand, load, and contraction type. The dependent variables for the fatiguing contractions were compared with a three-factor ANOVA (2 age groups × 2 hands × 10 repetitions) with repeated measures on hand and repetition. MVC force before and after the fatiguing contractions was compared with a two-factor ANOVA (2 age groups × 2 testing times) with repeated measures on testing time. An  level of 0.05 was chosen for all initial statistical comparisons, with post hoc comparisons (Newman-Keuls) performed when necessary. Unless stated otherwise, the data are presented as means ± SD in the text and table and as means ± SE in the figures.

	RESULTS

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The results report the amount of activity in the contralateral homologous muscle when young and old subjects performed various isometric and anisometric contractions with the first dorsal interosseus muscle of each hand separately. The data are expressed relative to the maximum values achieved during an MVC by each hand.

The two groups of subjects preferred to use the right hand for most activities of daily living, as indicated by similar values for the laterality quotient (35) for the young (0.69 ± 0.15) and old subjects (0.78 ± 0.23). Similarly, the MVC forces were not different for either the two groups of subjects (P = 0.24) or the two hands (P = 0.35; Table 1), and the associated AEMG was not different (P = 0.08 for the two groups and P = 0.11 for the two hands). The 1-RM load, however, was greater for the young subjects (P < 0.01).

Isometric Contractions

View larger version (16K): [in this window] [in a new window]   Fig. 1.   Representative data from an old subject performing an isometric contraction at a target force of 80% maximal voluntary contraction (MVC) force (A) and an anisometric contraction with a load of 80% one-repetition maximum (1-RM) load (B). The test hand for both contractions was the right hand, which meant the contralateral activity was measured in the left hand. The traces for the isometric contractions and the contralateral activity during the anisometric contraction correspond to the force (upper trace) and the rectified electromyogram (EMG) of first dorsal interosseus (lower trace). The force was exerted by the proximal interphalangeal joint of the index finger. The traces for the test hand during the anisometric contraction indicate the angle of the metacarpophalangeal joint (upper trace) and the rectified EMG of first dorsal interosseus (lower trace).

View larger version (16K): [in this window] [in a new window]   Fig. 2.   Maximum contralateral force (A) and average rectified EMG (AEMG; B) for the young and old subjects during isometric contractions performed with the first dorsal interosseus muscle of the other hand to 6 different target forces. Data shown are group means ± SE.

View larger version (11K): [in this window] [in a new window]   Fig. 3.   Maximum contralateral force (A) and AEMG (B) for the young and old subjects during unilateral isometric contractions performed with the first dorsal interosseus muscle of the left and right hands. Solid bars indicate the force and EMG recorded in the right hand when the task was performed by the left hand. Conversely, open bars indicate the contralateral activity in the left hand when the task was performed by the right hand. Data shown are group means ± SE. * P < 0.05 compared with the same hand of the young subjects.

Anisometric Contractions

View larger version (20K): [in this window] [in a new window]   Fig. 4.   Contralateral force and average rectified EMG during unilateral tasks performed by young and old subjects. A: maximum isometric force exerted in the abduction direction by the index finger of the contralateral hand of young and old subjects. Data (means ± SE) were averaged across concentric and eccentric contractions. B: AEMG for the contralateral first dorsal interosseus muscle of the young and old subjects during the unilateral anisometric contractions. C: maximum isometric force exerted in the abduction direction by the index finger of the contralateral hand during unilateral concentric and eccentric contractions. Data (means ± SE) were averaged across the 2 age groups. D: AEMG for the contralateral first dorsal interosseus muscle during the 2 types of unilateral contractions. Data (means ± SE) were averaged across the 2 age groups. * P < 0.05 for contraction type.

Fatiguing Contractions

View larger version (17K): [in this window] [in a new window]   Fig. 5.   Maximum contralateral force (A) and average rectified EMG (B) for the young and old subjects during 10 anisometric contractions performed with the first dorsal interosseus muscle of the other hand. The load during the anisometric contractions was 80% 1-RM load. The data were collapsed across contraction type in this figure. Data shown are group means ± SE. * P < 0.05 and ** P < 0.01 compared with young subjects.

	DISCUSSION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION REFERENCES

The main findings were that the contralateral activity in the homologous hand muscle exhibited by all subjects when performing voluntary contractions with the first dorsal interosseus muscle was greater for old subjects compared with young subjects, for isometric contractions compared with anisometric contractions, and for eccentric contractions compared with concentric contractions. Furthermore, the rate of change in contralateral activity during a set of fatiguing contractions differed for the two age groups.

A previous study on contralateral activity in the first dorsal interosseus muscle of young adults reported similar results to those obtained in the present study (52). They found contralateral forces of 7.6 ± 5.5% in the dominant hand and 8.2 ± 7.9% in the nondominant hand during MVCs performed with the first dorsal interosseus muscle by young adults, which compared with 6.91 ± 11.1% in the present study. Furthermore, they indicated that although all subjects demonstrated contralateral activity, there was substantial variability between subjects, as indicated by the large standard deviations. Neither group of young subjects, those tested by Zijdewind and Kernell (52) and those examined in the present study, exhibited a difference in the amount of contralateral activity between the two hands. In both studies, there was an increase in the contralateral activity with target force, except at the highest forces (80 and 100% MVC force). Similarly, the contralateral activity increased during a fatiguing contraction for the young subjects in both studies: despite differences in the two protocols, Zijdewind and Kernell reported an increase in contralateral force from 9.1 ± 6.5 to 26.0 ± 12.1% compared with an increase from 2.34 ± 3.27 to 20.4 ± 15.2% in the present study. The main new findings of the present study are the augmented contralateral activity exhibited by old adults compared with young adults, isometric contractions compared with anisometric contractions, and eccentric contractions relative to concentric contractions.

Difference Due to Age

In contrast, electrophysiological measurements suggest a cortical origin for the unintended contralateral activity. For example, when the cutaneomuscular reflex was evoked in the hand of individuals who exhibited contralateral activity in first dorsal interosseus, the transcortical component of the reflex was enhanced when a unilateral task was being performed (33). This result suggests a heightened level of excitation among the corticospinal neurons contralateral to the unintended activity, which indicates that the unintended activity arose from the contralateral cortex and not the ipsilateral cortex. Although unilateral hand movements are associated with bilateral activation of the premotor cortex and supplementary motor area (16, 34, 44, 51) with significant differences due to age (32), the absence of unintended contralateral activity appears to be the result of transcallosal inhibition (1, 13, 15, 30, 33, 40). Furthermore, a flat cross-correlation histogram derived from the interference EMGs of the first dorsal interossei in both hands during a unilateral task indicated that the contralateral activity was not due to common input to the two motor neuron pools (33). Rather, the potential evoked in a muscle in response to transcranial magnetic stimulation of one motor cortex was reduced in amplitude when the stimulus was preceded (7-15 ms) by a conditioning stimulus delivered to the other motor cortex (33). The reduction in the evoked response is consistent with an inhibitory effect mediated by the transcallosal pathway (1, 13). Children did not exhibit a decrease in the conditioned response, because of an immature transcallosal pathway, but did display more frequent episodes of unintended contralateral activity (33).

Imaging studies indicate that the structure of the corpus callosum changes across the life span. The midsagittal cross-sectional area of the anterior half of the corpus callosum, for example, was larger in magnetic resonance images of professional musicians who began training in music before 7 yr of age (39). The anterior fibers contribute significantly to bimanual coordination (11). Conversely, there is a small but consistent decrease in the size of the corpus callosum after middle age, which is presumed to underlie the decline in sensorimotor function that involves the transfer of information between the two hemispheres (3, 37). Although these findings suggest that the greater contralateral activity exhibited by the old subjects during unilateral tasks may be a functional consequence of such changes in the corpus callosum, there are other marked changes that influence connectivity in the cerebral cortex of older adults. For example, there is evidence of reduced cortical excitability (10) and depressed intracortical inhibition (36) during unilateral tasks performed by older adults. As a consequence, the greater unintended contralateral activity observed in older adults may reflect a change in the balance between interhemispheric excitation and inhibition within the cerebral cortex (16).

Isometric and Anisometric Contractions

In contrast to the qualitative similarity in the relative amplitudes of the contralateral activity for the two types of contractions performed by both groups of subjects, there was a marked difference for the set of fatiguing contractions. Consistent with the results of Zijdewind and Kernell (52), the young subjects increased the contralateral activity progressively during the task beginning with a value that was comparable to a single repetition with the 80% 1-RM load. The old subjects, however, sustained a constant level of contralateral activity during the 10 repetitions and began with a value that was greater than observed during a single repetition of the task. Although unintended contralateral activity is typically considered to depend on the intensity of the unilateral contraction (5, 9, 14, 52), the behavior exhibited by the old adults indicates contralateral activity that was not graded with the effort of the unilateral task.

Functional Implications

One example of contralateral activity consistent with these conditions that has dire consequences is the unintentional discharge of a handgun. For example, if a person performs a high-intensity isometric contraction with the left hand while holding a handgun in the right hand, the unintended contralateral activity can cause the gun to discharge. Such incidents are experienced occasionally by law-enforcement officers when they attempt to apprehend a struggling individual with one hand while holding a gun in the other hand. As a consequence, many firearms instructors propose weapon-handling strategies that minimize the unintended placement of the index finger on the trigger of the gun (22). This example introduces another factor not considered in the present study, however: that the amount of contralateral activity probably depends on the level of physiological arousal experienced by the individual. Although the functional significance of unintended contralateral activity presumably varies along a continuum from a null effect to a substantial effect, it seems premature to assign a level of significance to the present findings. Nonetheless, the results indicate that activation of a hand muscle by the nervous system during the performance of unilateral tasks differs for young and old adults and for isometric and anisometric contractions.