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J Appl Physiol 95: 1361–1369, 2003. First published March 7, 2003; 10.1152/japplphysiol.00070.2003.

Age effects on force produced by intrinsic and extrinsic hand muscles and finger interaction during MVC tasks Minoru Shinohara, Mark L. Latash, and Vladimir M. Zatsiorsky Department of Kinesiology, The Pennsylvania State University, University Park, Pennsylvania 16802 Submitted 24 January 2003; accepted in final form 3 March 2003

Shinohara, Minoru, Mark L. Latash, and Vladimir M. Zatsiorsky. Age effects on force produced by intrinsic and extrinsic hand muscles and finger interaction during MVC tasks. J Appl Physiol 95: 1361–1369, 2003. First published March 7, 2003; 10.1152/japplphysiol.00070.2003.—Fingerpressing forces are produced by activation of the intrinsic hand muscles, which are finger specific, and the extrinsic muscles that connect to multiple fingers. We tested a hypothesis of greater weakening of intrinsic hand muscles with age and quantified associated indexes of finger interaction such as enslaving (force production by unintended fingers) and force deficit (loss of finger force in multifinger tasks compared with single-finger tasks). Twelve young (23–35 yr old) and 12 elderly (70–95 yr old) men and women performed singlefinger and four-finger maximal pressing tasks, in which force was applied at the proximal phalanges (PP, the intrinsic muscles are major focal force generators) and at the distal phalanges (DP, the extrinsic muscles are focal force generators). The decline in the peak force with age was greater at PP (30%) than at DP (19%). Larger indexes of finger interaction were observed at PP (enslaving ⫽ 17.2 ⫾ 9.4%, force deficit ⫽ 36.1 ⫾ 11.1%) than at DP (enslaving ⫽ 14.9 ⫾ 8.8%, force deficit ⫽ 27.7 ⫾ 10.8%) across ages and genders. We conclude that intrinsic hand muscles show disproportionate weakening with age. The greater indexes of finger interaction in PP tests with greater involvement of intrinsic hand muscles suggest that the finger interactions are predominantly of a central origin across ages and genders. aging; synergy; gender; maximal voluntary contraction

OVERALL PERFORMANCE of the hand within a broad range of functions required for the activities of daily living declines with age (17). A recent study of finger interaction in tasks involving production of maximal voluntary contraction (MVC) forces by pressing on force sensors with the fingertips has shown that aging leads not only to a drop in MVC force but also to changes in indexes of finger interaction, such as force deficit and enslaving (39). Force deficit reflects the fact that peak force of a finger is smaller in multifinger than in single-finger MVC tasks (22, 29). Enslaving quantifies forces produced by fingers not explicitly involved in a finger-pressing MVC task (21, 37, 45, 46). In our previous study (39), elderly subjects showed lower peak forces, greater force deficit, and lower enslaving than

Original submission in response to a call for papers on “Physiology of Aging.” Address for reprint requests and other correspondence: M. L. Latash, Rec. Hall, 267L, Dept. of Kinesiology, The Pennsylvania State University, University Park, PA 16802 (E-mail: [email protected]). http://www.jap.org

young subjects. Further analysis revealed that the group differences in force deficit and enslaving were related to the peak force that could be produced by individual subjects across ages and genders. Finger flexion forces are produced by activation of the intrinsic hand muscles, which are finger specific, and the extrinsic hand muscles, with tendons that attach to multiple fingers. The intrinsic finger-specific muscles (dorsal and palmar interossei and lumbricals) exert focal flexor action at the metacarpophalangeal (MCP) joints, in addition to extensor action at more distal joints, whereas the extrinsic multifinger flexors (flexor digitorum profundus and flexor digitorum superficialis) are the focal generators of flexion force at the distal and proximal interphalangeal joints, respectively (24, 31), in addition to the moments they produce at the MCP joint. This allows for varying the degree of relative involvement of intrinsic and extrinsic muscles by varying the point along the finger that presses against an external object. For example, when a person presses with the fingertips [distal phalanges (DP)], extrinsic flexors are focal force generators, whereas intrinsic muscles participate in balancing moments at the MCP joints. When force is applied at the proximal phalanges (PP), intrinsic finger-specific muscles are major focal force generators, whereas extrinsic flexors balance the action of the extensor mechanism at the interphalangeal joints (9, 30), in addition to their contribution to the MCP moment (2). Although still controversial, there are reports suggesting that the loss of muscle strength with age is related to anatomic location, with distal muscles affected more than proximal muscles (10, 14, 35, 42). Hence, we suggest a hypothesis that force-producing capabilities of intrinsic hand muscles are more affected by age than are more proximal, extrinsic muscles. The hypothesis predicts a greater drop in peak finger forces during tests with force production at PP than with pressing at DP. To provide more evidence for the differential effects of age on intrinsic and extrinsic hand muscles, we also analyzed MVC force during index finger abduction, because this action is controlled primarily by a single intrinsic muscle. Changes in indexes of finger interaction with age could be due to the changes in the properties of hand 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.

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AGE EFFECTS ON INTRINSIC AND EXTRINSIC HAND MUSCLES

Table 1. Physical characteristics of subjects Length, cm

Young Elderly Male Female

Age, yr

Height, cm

Body Mass, kg

Middle finger

PP

29.6 ⫾ 3.9 81.8 ⫾ 7.0† 58.3 ⫾ 30.4 53.1 ⫾ 24.6†

170.8 ⫾ 7.9 167.0 ⫾ 9.5 174.1 ⫾ 6.1 163.6 ⫾ 7.9†

66.5 ⫾ 14.0 71.4 ⫾ 14.8 74.6 ⫾ 11.2 63.3 ⫾ 15.2*

10.2 ⫾ 0.7 10.6 ⫾ 1.1 10.9 ⫾ 0.9 9.8 ⫾ 0.5†

5.4 ⫾ 0.4 5.2 ⫾ 0.4 5.5 ⫾ 0.4 5.2 ⫾ 0.3

Values are means ⫾ SD. PP, proximal phalange. * P ⬍ 0.05; † P ⬍ 0.01 for subject group (young vs. elderly or male vs. female).

muscles (16, 25, 35) and adaptive changes in neural commands to the muscles and muscle compartments involved in finger force production (39). Recent studies have shown that, in young subjects, indexes of finger interactions are larger when the force is applied at PP than at DP (13, 26). Whether this is true in elderly subjects is unknown. Because of the dependence of the indexes of finger interactions on peak finger force and the drop in peak force with age (13, 39), relations between indexes of finger interaction at DP and at PP in elderly subjects could differ from those in young controls. Differences in finger forces and indexes of finger interaction between male and female subjects are similar to those between young and elderly subjects when pressing at the fingertips (39); female and elderly subjects show smaller MVC force, greater force deficit, and smaller enslaving than male and young subjects, respectively. However, in contrast to the hypothesized greater weakening of intrinsic muscles with age, we do not expect male and female subjects to be different in the relative strength of intrinsic and extrinsic muscles. Hence, we predict that the differences in MVC force between men and women should not depend on the site of force application, i.e., DP or PP, in contrast to the earlier prediction for comparisons between young and elderly subjects.

joint) between the subject groups. All the subjects gave informed consent according to the procedures approved by the Office for Regulatory Compliance of The Pennsylvania State University. Apparatus. Four unidirectional piezoelectric sensors (model 208C02, PCB Piezotronics, Depew, NY) were used to measure the force production of individual fingers. The sensors were each connected in series with wire cables that were suspended by swivel attachments from slots in the top plate of the inverted U-shaped frame of the experimental device (Fig. 1). The slots were placed 30 mm apart in the mediolateral direction and allowed fore-aft adjustment of the wires to accommodate an individual subject’s anatomic differences in finger length. The fingers applied force to rubber-coated loops located at the bottom of each wire. These loops could be placed against the middle of the DP or against the middle of the PP. Changes in the position of the loops changed the relative contributions of intrinsic and extrinsic hand muscles to force production (30). Analog output signals from the sensors were connected to separate alternating current-direct current conditioners (model M482M66, PCB Piezotronics). The signal conditioners operated in a direct-currentcoupled mode, utilizing the sensor’s discharge time constant as established by the built-in microelectronic circuits within the sensors. The time constant of the sensor was ⱖ500 s. The system involved ⬃1% error over the typical epoch of record-

METHODS

Subjects. Twelve (6 men and 6 women) young and 12 (6 men and 6 women) elderly subjects took part in the experiment. All the subjects were healthy and right-handed according to their preferential use of the hand during daily activities such as writing, drawing, and eating. None of the subjects had a history of long-term involvement in activities such as typing and playing musical instruments. Elderly subjects passed the screening process that involved a cognition test (Mini-mental status exam, ⱖ24 points), a depression test (Beck depression inventory ⱕ20 points), a quantitative sensory test (monofilament ⱕ3.22), and a general neurological examination. Physical characteristics of the subjects are shown in Table 1. Elderly subjects were recruited from a local retirement community. Elderly female subjects (76.3 ⫾ 4.0 yr) were younger than elderly male subjects (87.2 ⫾ 4.5 yr, P ⬍ 0.01) because of the availability of subjects in the retirement community. This resulted in a significant difference in age between male and female subjects, but there was no difference in age between young male subjects (29.3 ⫾ 3.6 yr) and young female subjects (29.8 ⫾ 4.6 yr). The length of the middle finger (from the MCP joint to the fingertip) was significantly shorter in female than in male subjects, but there was no difference in the length of the PP of the middle finger (from the MCP joint to the proximal interphalangeal J Appl Physiol • VOL

Fig. 1. Setup for measuring finger flexion force. The forearm was placed on the supporting surface, the hand was clamped by the fixation device, and the loops were positioned at the distal or proximal phalanges.

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ing of a constant signal. A 16-bit analog-to-digital converter board (DAQCard-AI-16XE-50, National Instruments, Austin, TX) was used to digitize the signals at 1,000 Hz. A Dell laptop computer controlled the experiment and was used for data acquisition and processing. The possible force range of the sensor was ⫾444.8 N, and the resolution of the system was 2.715 mN/bit. The high resolution was made possible by allotting only the force range of ⫾88.96 N to the 16-bit analog-to-digital converter. The subject was seated in a chair facing the testing table and a monitor, with his/her right upper arm at ⬃45° of abduction in the frontal plane and ⬃45° of flexion in the sagittal plane and the elbow at ⬃135° of flexion. The forearm was secured by Velcro straps flat on the supporting surface that was at the same height as the support point of the hand fixation device. The hand fixation device was located at the bottom of the frame and was used to stabilize the palm of the hand and to ensure a constant hand configuration throughout the experiment. The wrist was at 20° of extension (hand and forearm aligned correspond to 0°). The MCP joints were at 20°. The thumb was positioned under the bar on which the palms rested. Because of the experimental procedure, all four finger forces were parallel to each other. All precautions were taken to avoid motion of the forearm or hand during the tests without compromising the subjects’ comfort. Procedure. Force was applied under two conditions: at DP and at PP. In the PP condition, the experimenter always ensured that the subjects maintained the distal joints of the fingers extended. The order of the conditions was pseudorandomized across subjects. In each condition, subjects were instructed to press as hard as possible (MVC) with all four fingers together (IMRL) or with one particular finger: index (I), middle (M), ring (R), or little (L). The order of the finger(s) was pseudorandomized across subjects. During each trial, all the fingers were in the loops, and subjects were explicitly instructed not to lift other “uninvolved” fingers off the loops. None of the subjects perceived this as a complicating condition compromising their comfort during the tests. The subjects were asked not to pay attention to possible force generation by those fingers as long as the force by the instructed finger was maximal. The combined force produced by the explicitly involved fingers was displayed on-line on the screen in front of the subject. At the beginning of each MVC trial, the computer generated two tones (“get ready”); then a trace showing the total force produced by the explicitly involved fingers started to move across the screen. The subjects were asked to produce peak force within a 2-s interval shown on the screen by two vertical lines and then to relax. Each subject performed three trials using each finger combination. In addition, maximal abduction force of the index finger was measured during isometric contraction of the first dorsal interosseous muscle. Another unidirectional piezoelectric sensor (model 208C02, PCB Piezotronics) was attached to the side of the frame, to which a wire was connected. An aluminum loop located at the bottom of the wire was placed on the proximal interphalangeal joint of the index finger. The index finger applied abduction force to this loop. The abduction force signal was processed in the same way as for the finger flexion force signals. The interval between successive trials was 1 min, whereas intervals between series were ⬎5 min. Subjects never reported fatigue. Data processing. For each MVC trial, the instantaneous force produced by each finger was measured at the moment when the maximal force value was reached by the explicitly involved fingers (MVC force). These data were used to compute enslaving force during single-finger trials, force deficit J Appl Physiol • VOL

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during four-finger trials, and force sharing during four-finger trials. Enslaving forces were produced by the slave fingers, i.e., fingers that were not explicitly involved in a task. They were measured at a time when the explicitly instructed finger reached its peak force. For each slave finger, the enslaving force was expressed as a percentage with respect to this finger’s MVC force in its single-finger task. These indexes of enslaving were averaged across all slave fingers for further comparisons. Force deficit for a finger was defined as the difference between this finger’s MVC force in its single-finger task and its force when peak force was reached during the four-finger task. Force deficit was expressed as a percentage of the finger’s peak force in its single-finger MVC task. Thereafter, indexes of force deficit were averaged across all fingers for further comparisons. Force sharing was calculated by dividing the force of each finger in a four-finger MVC task by the four-finger peak force. Statistics. Standard descriptive statistics and ANOVAs with or without repeated measures were used. Factors were chosen on the basis of particular comparisons. Factors included age (elderly and young), gender (male and female), task (I, M, R, L, and IMRL), finger (I, M, R, and L), and site (PP and DP). For tests performed by the index finger, a factor, i.e., action, was also used with three levels: PP flexion MVC, DP flexion MVC, and abduction MVC. For comparisons that included task or finger, repeated-measures ANOVAs were used. For comparison of force-sharing patterns, multivariate ANOVA was used, including age, gender, and site factors, and Rao’s R was used to assess significance. Only three shared forces (shared forces by M, R, and L) were used for comparison of sharing patterns, because the four individual shares did not constitute a set of independent variables (the sum of the 4-finger shared forces is always 100%). Post hoc analysis was performed using Newman-Keuls test or t-tests with Bonferroni’s correction. Linear regression analysis was used to analyze relations between indexes of finger interaction (enslaving and force deficit) and MVC force during a four-finger task. Regression lines were compared with respect to residuals, slope, and intercept (analysis of covariance) (41). Level of significance was set at P ⫽ 0.05. Values are means ⫾ SD, except as noted otherwise. RESULTS

MVC force. Across all tests with maximal force production, elderly subjects showed smaller peak forces than young subjects, whereas women showed smaller forces than men. Comparisons of peak forces at the two sites of force production, DP and PP, were run to test the hypothesis of the predominant weakening of intrinsic muscles with age. Additionally, this hypothesis was tested by comparisons of the index finger peak forces in three MVC tests: flexion at DP, flexion at PP, and abduction. Four-finger tests. Peak forces for each finger during the four-finger maximal force production task are presented in Table 2, and the total force (the sum of the forces by the 4 fingers) is presented in Fig. 2. Averaged across fingers, genders, and sites of force application, peak force was 25% less in elderly than in young subjects [66.7 ⫾ 23.5 vs. 89.0 ⫾ 31.3 N, F(1,20) ⫽ 13.24, P ⬍ 0.01, main effect of age in a 4-way ANOVA with repeated measures (age ⫻ gender ⫻ site ⫻ finger)]. The

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Table 2. Peak force of each finger during MVC Index Proximal

MVC in 1-finger tasks, N Young Elderly Male Female MVC in 4-finger tasks, N Young Elderly Male Female Force sharing in 4-finger tasks, % Young Elderly Male Female

Middle Distal

Proximal

Ring Distal

Proximal

Little Distal

Proximal

Distal

41.18 ⫾ 7.09 35.04 ⫾ 8.93‡ 43.69 ⫾ 6.07 32.52 ⫾ 6.76‡

34.02 ⫾ 8.02† 30.74 ⫾ 6.38†‡ 37.93 ⫾ 4.99† 26.83 ⫾ 4.34†‡

39.69 ⫾ 7.16 31.36 ⫾ 8.47‡ 41.67 ⫾ 4.96 29.38 ⫾ 7.33‡

31.53 ⫾ 9.49† 25.46 ⫾ 7.29†‡ 35.04 ⫾ 6.90† 21.95 ⫾ 4.70†‡

32.62 ⫾ 9.60 25.40 ⫾ 10.67‡ 35.70 ⫾ 8.04 22.33 ⫾ 8.51‡

23.67 ⫾ 9.75† 18.55 ⫾ 6.33†‡ 27.54 ⫾ 6.93† 14.68 ⫾ 3.35†‡

26.83 ⫾ 10.54 24.72 ⫾ 7.61‡ 32.50 ⫾ 7.41 19.05 ⫾ 4.24‡

19.17 ⫾ 7.16† 17.67 ⫾ 5.72†‡ 23.42 ⫾ 4.75† 13.42 ⫾ 2.83†‡

28.98 ⫾ 10.98 21.28 ⫾ 9.11‡ 31.80 ⫾ 10.51 18.45 ⫾ 5.31‡

25.53 ⫾ 7.33† 19.78 ⫾ 6.28†‡ 26.30 ⫾ 6.55† 17.00 ⫾ 3.29†‡

27.27 ⫾ 10.23 17.04 ⫾ 8.58‡ 29.08 ⫾ 9.96 15.23 ⫾ 5.62‡

23.77 ⫾ 8.80 19.75 ⫾ 8.73† 28.44 ⫾ 6.34 15.08 ⫾ 4.98†

21.64 ⫾ 8.07 14.19 ⫾ 7.63‡ 22.20 ⫾ 7.53 13.62 ⫾ 7.54‡

20.01 ⫾ 8.24 15.30 ⫾ 5.81‡ 22.99 ⫾ 6.02 12.32 ⫾ 3.94‡

19.41 ⫾ 8.91 13.40 ⫾ 6.40† 15.77 ⫾ 6.10‡ 10.35 ⫾ 4.88†‡ 22.36 ⫾ 6.78 15.54 ⫾ 5.11† 12.82 ⫾ 5.31‡ 8.21 ⫾ 3.82†‡

29.67 ⫾ 4.02 31.67 ⫾ 8.00 29.87 ⫾ 7.57 31.47 ⫾ 4.86

29.79 ⫾ 4.17 31.33 ⫾ 6.20 28.09 ⫾ 4.05 33.03 ⫾ 5.24

28.07 ⫾ 3.99 24.48 ⫾ 6.21 27.32 ⫾ 6.44 25.24 ⫾ 4.20

29.68 ⫾ 5.34* 29.53 ⫾ 4.56* 30.69 ⫾ 4.25* 28.52 ⫾ 5.35*

22.79 ⫾ 5.78 20.05 ⫾ 4.92 21.10 ⫾ 4.86 21.74 ⫾ 6.16

24.38 ⫾ 3.77† 23.32 ⫾ 4.01† 24.58 ⫾ 3.89† 23.13 ⫾ 3.82†

19.47 ⫾ 5.26 23.80 ⫾ 6.34 21.72 ⫾ 6.67 21.54 ⫾ 5.79

16.13 ⫾ 4.54† 15.83 ⫾ 5.20† 16.64 ⫾ 4.80† 15.32 ⫾ 4.86†

Values are means ⫾ SD. MVC, maximal voluntary contraction. * P ⬍ 0.05; † P ⬍ 0.01 for site of force application. ‡ P ⬍ 0.01 for subject group (young vs. elderly or male vs. female).

drop in the maximal force with age depended on the site of force application. In elderly subjects, peak force reached at DP was only slightly different from peak force reached at PP (65.2 ⫾ 22.4 vs. 68.3 ⫾ 25.5 N, nonsignificant), whereas in young subjects, peak force was significantly lower at DP than at PP (80.7 ⫾ 28.4 vs. 97.3 ⫾ 32.9 N, P ⬍ 0.01, 2-tailed Student’s t-test). As a result, there was a significant 29.8% difference between the peak forces produced by the elderly and the young subjects at PP (P ⬍ 0.01, 2-tailed Student’s

t-test) in the absence of a significant difference at DP. This result was confirmed by a significant age ⫻ site interaction [F(1,20) ⫽ 6.78, P ⬍ 0.05] in the age ⫻ gender ⫻ site ANOVA. These data support the hypothesis of the greater age-related weakening of the intrinsic than the extrinsic hand muscles. The maximal total force was less in female than in male subjects at both sites [F(1,20) ⫽ 49.30, P ⬍ 0.01, main effect of gender in a 3-way ANOVA with repeated measures (age ⫻ gender ⫻ site)]. The force was 56.4 ⫾

Fig. 2. Maximal total force [maximal voluntary contraction (MVC) force] during 4-finger tasks, force deficit during 4-finger tasks, and enslaving during single-finger tasks. Values are group means ⫾ SE. *P ⬍ 0.05; **P ⬍ 0.01 for site of force application. #P ⬍ 0.05; ##P ⬍ 0.01 for subject group (young vs. elderly or male vs. female).

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17.4 N in women and 99.4 ⫾ 22.9 N in men when averaged across ages and sites of force application. The difference between male and female subjects was independent of the site of force application: 43.0% and 43.6% at PP and DP, respectively. These findings support the hypothesis of similar relative differences in MVC force between male and female subjects at both sites of force application. Force sharing in four-finger tests. The shared force during the four-finger MVC tests was the greatest for the index finger, followed by the middle, ring, and little fingers, across subject groups (Table 2). The sharing pattern (relative contribution of each finger force to the total force) was not affected by age or gender but showed an effect of the site of force application [P ⬍ 0.01, Rao’s R(3,18) ⫽ 8.664 for an age ⫻ gender ⫻ site multivariate ANOVA for shared forces among M, R, and L]. The relative contribution of the middle and ring fingers was less with PP than with DP by 2.4% (P ⬍ 0.05) and 3.3% (P ⬍ 0.01), respectively, which was counterbalanced by the 5.7% greater contribution by the little finger (P ⬍ 0.01, Newman-Keuls test). Single-finger tests. During single-finger maximal force production tests, peak force reached by the subjects differed among the fingers (Table 2). The strongest finger was the index finger, followed by the middle, ring, and little fingers, across subject groups and sites of force application (P ⬍ 0.01 for all pairwise comparisons with Newman-Keuls test). Subjects produced higher peak forces at the proximal site (PP) than at the distal site (DP). Averaged across fingers and subject groups, this difference was 27.9% [32.1 ⫾ 10.4 N at PP vs. 25.1 ⫾ 9.5 N at DP, F(1,20) ⫽ 65.35, P ⬍ 0.01, main effect of site in a 4-way ANOVA with repeated measures (age ⫻ gender ⫻ site ⫻ finger)]. Elderly subjects produced less force by each of the fingers (Table 2). The average MVC force across the fingers and sites of force application was significantly less in elderly than in young subjects [26.1 ⫾ 9.5 vs. 31.1 ⫾ 11.0 N, F(1,20) ⫽ 10.92, P ⬍ 0.01, main effect of age in a 4-way ANOVA with repeated measures (age ⫻ gender ⫻ site ⫻ finger)]. The decline in the maximal force with age was 14.7% at DP (27.1 ⫾ 10.3 and 23.1 ⫾ 8.3 N in young and elderly subjects, respectively) and 17.1% at PP (35.1 ⫾ 10.3 and 29.1 ⫾ 9.7 N in young and elderly subjects, respectively), but the difference between the PP and DP data was not statistically significant. Women produced less force by each of the fingers. The average maximal force was 35.1% lower in female than in male subjects [22.5 ⫾ 8.3 vs. 34.7 ⫾ 8.9 N, F(1,20) ⫽ 65.35, P ⬍ 0.01, main effect of gender in a 4-way ANOVA with repeated measures (age ⫻ gender ⫻ site ⫻ finger)]. The difference between male and female subjects was 38.0% at DP (31.0 ⫾ 8.2 and 19.2 ⫾ 6.7 N in male and female subjects, respectively) and 32.7% at PP (38.4 ⫾ 7.9 and 25.8 ⫾ 8.6 N in male and female subjects, respectively). The difference between the PP and DP data was not statistically significant. J Appl Physiol • VOL

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Index finger tests. Comparison of the peak force of the index finger in three tests, across genders and ages, shows similar forces during the flexion at PP and abduction tests (36.2 ⫾ 10.7 and 38.1 ⫾ 8.5 N, respectively), which were both significantly higher than the forces during the flexion at DP (32.4 ⫾ 7.3 N). These differences were confirmed by Newman-Keuls tests after a main effect in a three-way ANOVA [age ⫻ gender ⫻ action, F(1,40) ⫽ 6.46, P ⬍ 0.01]. The ANOVA also showed main effects of age [F(1,20) ⫽ 9.98, P ⬍ 0.01] and gender [F(1,20) ⫽ 37.29, P ⬍ 0.01]. Young subjects produced 19.2% more force during abduction, 14.9% more force during flexion at PP, and 9.7% more force during flexion at DP than elderly subjects. Female subjects produced 26.1% less force during abduction, 25.6% less force during flexion at PP, and 29.3% less force during flexion at DP than male subjects. Taken together, these data corroborate the hypothesis of a higher age-related force loss during tasks that rely more on intrinsic muscles, whereas all three tasks show similar differences in peak force between male and female subjects. Force deficit. When the maximal forces of individual fingers during the single-finger tests were summed, the total sum was larger than the maximal total force during the four-finger test. Thus there was a certain amount of force deficit during the four-finger tests. Force deficit is presented as the difference between the peak forces in single-finger and four-finger tests expressed as percentage with respect to the maximal force during the single-finger tests and averaged across fingers (Fig. 2). Force deficit was 23–45%. Force deficit was greater at PP than at DP across subject groups. On average, it was 36.1 ⫾ 11.1% at PP and 27.7 ⫾ 10.8% at DP [F(1,20) ⫽ 14.52, P ⬍ 0.05, main effect of site in a 3-way ANOVA with repeated measures (age ⫻ gender ⫻ site)]. The relative difference in force deficit between the two sites was 30.3%. The force deficit was similar among the individual fingers at PP, but it varied across the fingers at DP [Fig. 3; F(3,60) ⫽ 13.10, P ⬍ 0.01, site ⫻ finger interaction in a 4-way ANOVA

Fig. 3. Force deficit of individual fingers during 4-finger tasks. Values are group means ⫾ SE averaged across age and gender. **P ⬍ 0.01 for site of force application.

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Fig. 4. Force deficit (FD) and enslaving (Ensl) in relation to maximal total force during 4-finger task at proximal phalanges (PP) and distal phalanges (DP). Values are group means ⫾ SE for young male, young female, elderly male, and elderly female subjects. Linear regression lines are superimposed. Regression line for force deficit of PP was above that of DP (P ⬍ 0.01).

with repeated measures (age ⫻ gender ⫻ site ⫻ finger)]. As a result, greater force deficit at PP was seen for the middle and ring fingers (P ⬍ 0.05, NewmanKeuls test) but not for the index and little fingers. Force deficit was 26.5% greater in elderly than in young subjects, indicating that elderly subjects lose a greater amount of force when pressing with four fingers simultaneously. Force deficit was 35.7 ⫾ 10.8% in elderly subjects and 28.2 ⫾ 11.4% in young subjects [P ⬍ 0.05, F(1,20) ⫽ 4.66, main effect of age in a 3-way ANOVA with repeated measures (age ⫻ gender ⫻ site)] when averaged across genders and sites of force application. Women showed higher force deficit than men. On average, force deficit was 35.7 ⫾ 11.8% in female subjects and 28.2 ⫾ 11.4% in male subjects [F(1,20) ⫽ 4.75, P ⬍ 0.01, main effect of gender in a 3-way ANOVA with repeated measures (age ⫻ gender ⫻ site)]. As a result, during the four-finger MVC tests, the largest force deficit was seen in elderly women pressing at PP (45.2 ⫾ 8.2%), and the lowest force deficit was seen in young men pressing at DP (23.1 ⫾ 11.2%). To study a possible relation between force deficit and peak force, the data were averaged over each of the four subject groups separately. Figure 4 shows that force deficit was negatively related to maximal total force (significant at PP, P ⬍ 0.05, R ⫽ 0.964; below the level of significance at DP, R ⫽ 0.843). In other words, subjects with greater total force lose less force during the four-finger tests than the sum of peak forces in single-finger tests. In addition, the relation between the force deficit and the maximal total force at PP was not the same as the relation at DP but was above it [F(1,5) ⫽ 26.95, P ⬍ 0.01 for intercept, analysis of covariance]. The different relations between the sites of force application indicate that the greater force deficit at PP was not due to the greater maximal total force at PP that at DP. J Appl Physiol • VOL

Enslaving. During the single-finger MVC tests, force was produced by the finger that was instructed to press as well as by other fingers (enslaving). This enslaving force for each finger was expressed as percentage of the maximal force of the finger and then averaged across fingers. Its magnitude was 8–27% depending on age, gender, and site of force application. Higher enslaving was observed when force was produced at PP than at DP. Averaged across all subjects, enslaving was 17.2 ⫾ 9.4% at PP and 14.9 ⫾ 8.8% at DP [F(1,20) ⫽ 4.85, P ⬍ 0.01, main effect of site in a 3-way ANOVA with repeated measures (age ⫻ gender ⫻ site)]. The relative difference in enslaving between the sites was ⬃15.7%. Less unintended force was produced by the elderly than by the young subjects. Enslaving force was 12.9 ⫾ 8.9% in the elderly subjects and 19.2 ⫾ 8.3% in the young subjects [F(1,20) ⫽ 5.21, P ⬍ 0.05, main effect of age in a 3-way ANOVA with repeated measures (age ⫻ gender ⫻ site)] when averaged across gender and site of force application. Women showed lower enslaving than men [11.3 ⫾ 7.3% vs. 20.8 ⫾ 8.3%, F(1,20) ⫽ 11.89, P ⬍ 0.05, main effect of gender in a 3-way ANOVA with repeated measures (age ⫻ gender ⫻ site)] when averaged across ages and sites of force application. To study a possible relation between enslaving and peak force, the data were averaged over each of the four subject groups separately (Fig. 4). Linear regression analyses show an increase in enslaving with peak force for both sites of force application (P ⬍ 0.05, R ⫽ 0.978 at PP; P ⬍ 0.05, R ⫽ 0.977 at DP). The regression lines for DP and PP nearly overlapped. DISCUSSION

Within the study, we manipulated the relative contribution of intrinsic and extrinsic hand muscles to finger-pressing force by varying the site of force production along the finger. Our main hypothesis of the larger decrease in the force-generating capabilities of intrinsic hand muscle leads to two predictions. First, we predicted that peak forces in tasks when intrinsic muscles serve as focal force generators, such as pressing at PP or generating index finger abduction MVC, should decrease more with age than those that depend more on the action of extrinsic muscles, such as pressing at DP. In addition, we predicted that the earlier reported similarities of the effects of age and gender on finger forces and indexes of finger interaction (39) should show signs of breaking down when forces are produced at PP. The observations supported these two major predictions and also confirmed a dominant role of neural factors in phenomena of finger interaction such as enslaving and force deficit across ages and genders. However, quantitative assessment of indexes of finger interaction has shown that the relation of these indexes to peak finger forces differs at the two sites of force production. Effects of age on intrinsic and extrinsic hand muscles. The different sites of tendon attachment result in different degrees of involvement of intrinsic and extrinsic hand muscles in tasks when flexion MVC is pro-

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duced at PP and at DP (1, 9, 30). In particular, MVC produced at the fingertips requires peak force production by extrinsic flexors, whereas intrinsic muscle involvement has been assessed as 10–30% of their MVC (18, 30). In contrast, when a person presses maximally by PP, intrinsic muscles are expected to produce forces close to their MVC, whereas extrinsic muscles are counterbalancing forces produced by the action of the extensor mechanism. Existing assessments of forces produced by the extensor mechanism (8, 18, 24, 30, 40) suggest that they require the two major extrinsic flexors to produce ⬍20% of their maximal forces. Peak finger forces were smaller in elderly than in young subjects at both sites of force production. However, the difference was larger for forces produced at PP than at DP: 29.8% vs. 19.2% during force production by all four fingers and 17.1% vs. 14.7% during single-finger force production. Another test, index finger abduction MVC, was added to more directly assess force-generating capabilities of an intrinsic muscle, the first dorsal interosseous. In this test, forces generated by elderly subjects were ⬃19.2% smaller than those generated by young subjects, which was somewhat higher than the age-related drop in the MVC flexion force at PP (14.9%) and nearly twice as high as the drop in MVC flexion force at DP (9.7%). These data are comparable to reports of an age-related decrease in index finger abduction MVC of 19.7% by Semmler et al. (38) and 15.2% by Laidlaw et al. (23). Taken together, these observations support our hypothesis of a larger decrease with age in the peak force of intrinsic than of extrinsic hand muscles. These results correspond with earlier reports on distal muscles, in that they are more affected by age than are proximal muscles (10, 14, 42). In particular, Viitasalo et al. (42) reported greater decline of strength in handgrip (42%) than in elbow flexion (35%) when 180 young men (31–35 yr of age) and 180 older men (71–75 yr of age) were compared. Our experiments do not allow us to distinguish between possible age-related changes in different groups of intrinsic hand muscles such as lumbricals and interossei. Potentially, this can be done by expanding the set of tests to involve actions that can be used to distinguish between these groups, such as the Bunnel-Littler test, which is routinely performed in clinical practice (3). However, the observation of qualitatively similar effects in the index finger abduction test suggests that the greater weakening of intrinsic hand muscles may be a common phenomenon across different intrinsic muscle groups. In contrast to the findings in young and elderly subjects, male and female subjects showed similar differences in the peak forces at the two sites of flexion force production and in comparisons of the index finger MVC during three actions at which this finger was tested. This confirms our second prediction and provides further support for the hypothesis of greater weakening of intrinsic muscles with age. Changes in indexes of finger interaction with age. Phenomena of finger interaction have been discussed as resulting from peripheral factors and/or a central J Appl Physiol • VOL

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organization of neural commands (21, 27–29, 36). Consistent with the previous findings (13, 26, 46), indexes of finger interactions in young subjects were greater at PP than at DP. The present results show that this finding is common across ages and genders. Intrinsic hand muscles, which are focal force generators during finger flexion action at PP, are finger specific, and the strength of their tendinous connections is relatively low (21, 37). If the finger interactions mostly originated from peripheral factors, less finger interaction would have been expected at PP. Our observations of opposite results indicate that the finger interactions are predominantly central in origin. We found in a previous study (39) that indexes of finger interactions show similar differences between elderly and young subjects and between women and men, including the smaller enslaving and higher force deficit in elderly subjects and women. These indexes were linearly related to the four-finger MVC force across ages and genders when the subjects pressed with the fingertips. Enslaving was larger and force deficit was smaller in persons with larger four-finger MVC forces. In the present study, this was confirmed and generalized to finger force application at PP. This is not a trivial observation, because, as mentioned above (see Effects of age on intrinsic and extrinsic hand muscles), force-generating capabilities of different muscle groups are likely to change differently with age, although this is not expected across genders. Among possible origins of the larger force deficit in elderly subjects are the alterations in motor unit properties [increased innervation ratio (16, 25, 35) and altered force-frequency relation of motor units (11, 33)], as well as changes in the strategy of supraspinal control (reduced maximal discharge rate) (19, 34), which could lead to a greater loss of force after a standard drop in the recruitment or discharge rate of motor units. In the present study, the increase in force deficit with age was similar at the two sites of force application. Hence, we assume that a shift in the forcefrequency relation invoked as a major contributor to increased force deficit in elderly subjects (39) is likely to be similar across the intrinsic and extrinsic hand muscles. Implications for changes in neural control of the hand with age. Previously, we suggested an adaptation hypothesis which implies that a loss of the muscle force (39), whether due to aging or fatigue (13), leads to changes in neural control, the purpose of which is to optimize the functioning of the hand across functionally important everyday tasks. Changes in the muscle properties with fatigue and with age show similarities, including slowing of the contractile properties, which could lead to an increase in the slope of the forcefrequency relation (7, 20). The steep portion of the force-frequency curve is steeper after fatigue in flexor pollicis longus (15) and quadriceps femoris (6). Also, a reduction in the maximal discharge rate of motor units has been observed under muscle fatigue (4, 5), resembling changes that occur with age (19, 32).

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The present findings may be viewed as supporting the adaptation hypothesis. In particular, a drop in enslaving across the sites of force application may be viewed as contributing to better individual control of fingers, although not without a price, because higher enslaving may be helpful in prehension tasks that involve stabilization of an object grasped by the hand (43, 44). However, the finding of disproportional losses of force at the two sites, PP and DP, suggests potentially detrimental effects on muscle synergies involved in finger force production. Most everyday tasks involve force application by the fingertips. These forces generate moments in finger joints that need to be balanced by muscle action. In particular, intrinsic muscles are required to balance moments in the MCP joints. Hence, commands to extrinsic and intrinsic muscles need to be accurately balanced to prevent joint motion under fingertip force production. Such combinations of commands are probably elaborated and refined by the central nervous system (CNS) on the basis of the individual’s anatomy and the range of everyday tasks. If the force-generating capabilities of muscles involved in a synergy change disproportionately, previously elaborated combinations of neural commands to the muscles are likely to become suboptimal. If such changes in the muscle properties are permanent, as with aging, previously elaborated muscle synergies likely need to be adjusted. This may not be a simple task for the CNS, resulting in application of inadequate muscle synergies and decreased motor performance of the hand (12, 17, 39). One may suggest two ways to deal with this problem. First, massive practice may help the CNS revise the inadequate muscle synergies and elaborate new ones. However, the continuing changes in the muscle properties with age may prevent the CNS from elaborating new optimal sets of commands to hand muscles. Alternatively, efforts can be directed at restoring the balance between the force-generating capabilities of the intrinsic and extrinsic muscles. This goal may be more realistic with the help of specifically focused training programs. Our study has a number of limitations. Our tests could not distinguish between possibly different changes in the force-generating capabilities of different groups of intrinsic muscles with age. Finger joint angles were not recorded, and we relied on the fixation system, visual observation, and instruction to ensure unchanged finger joint angles during the tests. The pressing tests were relatively artificial, and generalization of our conclusions to everyday hand motor function requires confirmation of the main findings in such tests as grasping and manipulating objects. The authors are grateful to the staff and participants at Foxdale Village (State College, PA) for their cooperation. The screening process of the elderly subjects was conducted by Candace Kugel and Elizabeth Abraham under the supervision by Harold Bassett at the General Clinical Research Center (The Pennsylvania State University). J Appl Physiol • VOL

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