The hands, and in particular the fingers, are the most effective and indispensable tools for carrying out daily activities. Deterioration of hand and finger function due to illness or aging limits independence in activities of daily living as well as reduces the quality of life. Indeed, elderly individuals often experience increased difficulties performing daily tasks such as opening medicine bottles (13) and removing coins from a wallet (21). Hackel et al. (8) reported that a broad range of hand functions required for activities of daily living, as measured by the Jebsen test, decreased with age. There is also age-related decline in an ability to control grip force appropriately tuned for given friction between the digits and object held by the two digits (7,14).
Several quantitative techniques have been used to measure age-related changes in the hand function (7,8,14,24), but there are few quantitative methods available for measuring age-related changes in finger motor function (18,23). It has been reported that elderly adults produced a lower maximum pinch force between the thumb and each of the four fingers (18) as well as a lower maximum flexion force by each finger (23) compared with young adults. The static and dynamic motor abilities of the fingers allow the functional capability of our hand, including postural maintenance of the fingers as well as movement of the fingers. Thus, both the static and dynamic abilities of individual fingers are important for determining the functional state of the hand. There is, however, little available information on age-related changes in dynamic aspects of the motor capacity of individual fingers.
Using force sensor keys, we recently examined dynamic motor function during maximum-speed finger movements in single-finger tapping and alternate tapping with two fingers (double-finger tapping) (1-3). In healthy young nonmusicians, the tapping rates were significantly different among the fingers in the single-finger tapping as well as among the finger-pairs in the double-finger tapping (1). In addition, the tapping rate for each finger during double-finger tapping was always reduced when compared with the single-finger tapping. Recently, using positron emission tomography, it has been found that auditory-paced (2 Hz) tapping of the finger or finger-pair with greater difficulty in movement (e.g., the ring finger or ring-little finger-pair) required more extensive activation in the cortical and subcortical areas compared with the finger or finger-pair with less difficulty in movement (e.g., the index finger or index-middle finger-pair), respectively (4). More extensive brain activation was also observed during double-finger tapping compared with single-finger tapping. Thus, rapid single-finger and double-finger tapping can be a useful tool for assessing the dynamic aspects of motor function of the individual fingers, strongly reflecting brain function. The purpose of the present study, therefore, was to compare the dynamic aspects of the motor capacities of the index, middle, ring, and little fingers between elderly and young adults using rapid single-finger and double-finger tapping. Because the task, equipment, and data analysis are simple and can easily be adapted to the clinic setting, rapid tapping with a single finger (10,22) and less commonly with two fingers (17) have previously been used to examine fine motor function. However, these previous studies used tapping by the index and/or middle finger(s) only, and the tapping tasks usually included hand movements. Therefore, the present study is the first to examine age-related decline in dynamic motor function of individual fingers including all fingers.
The subjects were 14 elderly adults (7 males and 7 females) ranging in age from 65 to 77 yr (mean ± SD = 69.3 ± 3.5 yr) and 14 young adults (5 males and 9 females) ranging in age from 18 to 25 yr (19.7 ± 1.7 yr). The elderly subjects were recruited from a healthy population who were capable of carrying out the activities of normal and independent daily living. All of the elderly and young subjects were right-handed as determined by the Edinburgh MRC Handedness Inventory (16). None had a history of major disorders of either their upper extremities or their brain function. In addition, none had specific training in playing musical instruments or experience in any occupation that required skillful hand and finger activities. All subjects gave their written informed consent before the study. The human ethics committee at the Prefectural University of Kumamoto approved the protocol.
Five miniature force transducers (the contact area: 20 × 20 mm; USL06-H5-50N-D-FZ; Tec Gihan, Co., Uji, Japan) were used to monitor the forces generated by the tips of the thumb, index, middle, ring, and little fingers during tapping (Fig. 1). These transducers were screwed to an aluminum plate that was bolted to the upper surface of a 70-cm-high testing table. The apparatus also included a palm rest and a forearm rest with wrist belt. The rests and wrist belt were used to minimize the effects of the forces exerted by the hand and arm during tapping. These alignments were determined on the basis of data obtained in a pilot study (n = 36; 16 males and 20 females). Before the data collection, the positions of the five transducers, palm rest, and forearm rest were fine-tuned to fit the right hand of each subject.
To accustom the subjects to the testing apparatus and tapping tasks, each subject participated in a practice session several days before the experiment. After receiving a detailed explanation of the tapping tasks, the subjects were seated comfortably in a chair facing the testing table. The subject's right upper arm was parallel with his/her torso, and the forearm was extended horizontally and parallel to the sagittal plane (Fig. 1). The subjects performed maximum frequency tapping by the index, middle, ring, or little finger (single-finger tapping) and with alternate movement of the index-middle (IM), middle-ring (MR), or ring-little (RL) finger-pair (double-finger tapping). The subjects used a designated finger to repetitively strike its corresponding key in the single-finger tapping, whereas two designated fingers were used to alternately strike each of their corresponding keys in the double-finger tapping. During both tapping tasks, the subjects were instructed to repeatedly tap the key(s) with the finger(s) as rapidly and consistently as possible for 7 s. They were also asked to maintain contact between the tips of the "resting" (nontapping) fingers and their respective keys during tapping. Only the right hand was tested in the present investigation. The order of conditions in the tapping tasks was randomized. Data were collected during one trial for each finger in the single-finger tapping, whereas two trials were conducted for each finger-pair in the double-finger tapping. If a subject has perceived that he/she had failed to perform the tapping as instructed, he/she was asked to report this and then to repeat the trial. A 1-min rest was secured between the trials to minimize the effect of fatigue.
Amplified force transducer signals were digitized via a 12-bit analog-to-digital converter at a sampling rate of 400 Hz for each channel and were then stored on a personal computer. Beginning 1 s after the initiation of tapping for each trial, data from 10 consecutive taps by each finger were subjected to analysis. A threshold force of 0.03 N was used to determine the moments of finger-key contact and release. The time duration between the detection of successive finger-key contacts (intertap interval) was generated from the data obtained from each trial. For double-finger tapping, the data obtained from the two fingers in each trial were averaged for the parameter, and then the values for the two trials were averaged. The apparatus, procedure, and data analysis were similar to those used in our previous papers (1-3).
Maximum pinch force test.
The maximum isometric pinch force between the thumb and each finger was measured using a hydraulic pinch gauge (MG-4310NC; Nihonmedix, Co., Chiba, Japan). For the measurement of maximum pinch force, the pinch gauge was gripped between the mound of the right thumb and one of the four fingers. The subjects were asked to squeeze the two digits as hard as possible for approximately 3 s. The other fingers were kept away from the finger being tested to prevent them from assisting the pinch action. Two trials were performed for each finger with a 1-min rest between trials, and the greater force recorded in the two trials was adopted for the subsequent statistical analysis. The order of the fingers was randomized for each subject.
Semmes-Weinstein monofilament test.
A Semmes-Weinstein monofilament test was conducted to assess the threshold for light touch pressure on each fingertip of the right hand. For the test, an experimenter applied monofilaments (Touch-Test Sensory Evaluators; North Coast Medical, Inc., Morgan Hill, CA) to the subject's fingertip and the subject reported the occurrence of stimulation. Each of the 20 filaments was calibrated to provide a specific force. The filaments were presented in a sequence of increasing difficulty, and the tests were repeated until a consistent result was obtained. The minimum force that the subject could perceive was then regarded as the tactile threshold for the finger. The order of the fingers was randomized for each subject.
To evaluate the hand-eye coordination needed to perform a manual task quickly and accurately, a pegboard test was conducted. The pegboard (T.K.K.1302; Takei Scientific Instruments, Co., Niigata, Japan) had 48 holes. The 48 pegs were placed in the pegboard holes. The subjects were instructed to lift and rotate the peg in the upper left corner (first line) of the pegboard and insert it into the original hole as fast as possible. The subjects then continued on to the second peg in the same line and kept going down the line. After finishing the first line, the subjects proceeded with the next. There were six lines total on the pegboard. The time taken to complete the task was recorded. Only the right hand was tested.
For the single-finger tapping, the mean of the intertap interval was computed on the basis of 10 taps performed by each subject under each of the fingers. The mean intertap interval for the double-finger tapping was computed on the basis of 20 taps performed by each subject under each of finger-pairs. A repeated-measure mixed two-way ANOVA was performed to examine the group and condition effects on each of the intertap interval values of the single-finger tapping, the intertap interval values of the double-finger tapping, the maximum pinch forces, and the tactile sensitivities of the Semmes-Weinstein monofilament test. Tukey post hoc tests were also performed if needed. A one-way repeated-measure ANOVA was performed to examine the group effect on the time to complete the pegboard test. Pearson's correlation was performed to determine the relationships between different conditions in the tapping test as well as between the tapping test and the other tests. The correlation coefficients were only calculated for the data of elderly subjects. Statistical significance was accepted at P < 0.05.
An ANOVA revealed the significant effects of age group and finger on the intertap interval in the single-finger tapping. Post hoc analyses indicated that the intertap intervals of the index and middle fingers were significantly shorter than those of the ring and the little fingers for both elderly and young subjects (Fig. 2A). However, the intertap intervals were significantly longer in the elderly subjects than the young subjects in all fingers. The values of the elderly subjects in the single-finger tapping ranged between 116% and 126% of the young subjects. In the double-finger tapping, all elderly subjects could perform the IM finger-pair as instructed. However, only 13 could perform the MR and RL finger-pairs, respectively. The young subjects, however, were able to perform all finger-pairs as instructed. An ANOVA revealed that the group and finger-pair differences were significant. The mean value of intertap interval for the IM finger-pair of those who were able to complete the task was significantly shorter than the MR and RL finger-pairs in both elderly and young subjects (Fig. 2B). The mean value of the MR finger-pair was also significantly shorter than the RL finger-pair in both elderly and young subjects. The intertap intervals for the elderly subjects were significantly longer than for the young subjects in all of the finger-pairs. The values of the elderly subjects in the double-finger tapping ranged from 147% to 206% of the young subjects.
Maximum pinch force test.
The maximum pinch force between the thumb and each of the four fingers was greatest for the index finger, and it was followed by the middle, ring, and little fingers in both elderly and young subjects (Fig. 3A). The differences between the fingers were all significant. However, a significant group difference was not found in any finger.
Semmes-Weinstein monofilament test.
The tactile threshold was similar among the fingers in each age group (Fig. 3B). However, the older subjects required significantly greater forces by the filaments to sense the stimuli than the young subjects for all fingers.
The time taken to rotate all pegs was 64.6 ± 8.6 s for the older subjects and 54.9 ± 9.8 s for the young subjects. The older subjects needed 18% more time than the young subjects. An ANOVA revealed that the group difference was significant.
Relationships between different conditions in the tapping test and between the tapping test and other tests.
The correlation coefficients between different conditions in the tapping test were calculated in the elderly subjects (Table 1). As expected, significant correlations were found between the different fingers in the intertap intervals for the single-finger tapping. The exceptions were the values between the index and ring fingers as well as between the middle and little fingers. As in the case of single-finger tapping, significant correlations were observed between all finger-pairs in the double-finger tapping. Significant correlation was also observed between the ring finger in the single-finger tapping and each of the finger-pairs in the double-finger tapping.
The correlation coefficient between the intertap interval of each finger and the maximum pinch force by the corresponding finger was calculated in the elderly subjects (Table 2). In the double-finger tapping, the correlation coefficient was calculated between the intertap interval of each tapping finger and pinch force of the finger. However, significant correlation was not observed between the intertap interval and maximum pinch force in any finger. The correlation coefficient between the intertap interval of each finger and the tactile threshold of the corresponding finger was also computed for the elderly subjects (Table 2). However, the correlations were not significant in any finger. Finally, the correlation coefficient between the intertap interval of each tapping condition and time taken for the pegboard test was calculated in the elderly subjects (Table 2). Significant correlation was only found between the intertap interval of the ring finger in the single-finger tapping and the time for the pegboard test.
The main finding in the present study was that finger motor function as evaluated by the tapping test declined in the elderly subjects than the young subjects for all fingers in the single-finger tapping and all finger-pairs in the double-finger tapping. The age-related decline was more prominent in the double-finger tapping, which was the more complex motor task, compared with the single-finger tapping.
It is presumed that numerous factors collectively contributed to the age-related decline in finger motor function observed in the present study. One of these is the decreased functional properties of the muscles of the hand and forearm in elderly individuals. However, our results showed that the maximum pinch force between the thumb and each finger was similar between the elderly and young subjects (Fig. 3A). In addition, the intertap interval of each finger did not correlate with the maximum pinch force of the corresponding finger in the elderly subjects (Table 2). Our previous study reported that expert pianists who could attain faster tapping movements did not produce greater maximum pinch force of any finger than the nonmusician controls (2). Therefore, muscle properties allowing strong force production do not seem to be the major contributor to the faster movements of young adults during tapping. In contrast to our present results, previous studies have reported that elderly adults produced a lower maximum finger force compared with young adults (18,23). One reason for this discrepancy between those results and ours for isometric force production might be that the elderly subjects in the present study are quite active, with all participating in physical activities through either a public temporary employment agency for seniors or local sports club. The other reason may be the differences in the tasks. In the present study, the subjects gripped the pinch gauge by two digits opposing parallel to the table surface. However, one previous study (18) measured the pinch force when the subjects gripped the pinch gauge by two digits opposing vertical to the table surface. Another previous study (23) measured flexion forces when the subjects were asked to press a key using one of the four fingers.
Second, one may speculate that impaired tactile information in elderly people contribute to their slower tapping movements. The elderly subjects in our study showed lower tactile sensitivities of all fingers than the young subjects (Fig. 3B), and this decreased tactile feedback may have affected their performance of the tapping tasks. However, our results also showed that the intertap interval of each finger did not correlate with the tactile sensitivity of the corresponding finger in the elderly subjects (Table 2). A previous study (5) that examined the contribution of tactile afferent information to finger movements during tapping tasks has reported that the tapping rate in maximum frequency tapping was similar between the condition with peripheral nerve block and the control condition. They concluded that tactile information can play a minor role in maximum frequency tapping. Therefore, decreased tactile sensitivity of the fingertips in the elderly subjects seems not to be a major factor contributing to the slower tapping movements in the present study.
Third, in the elderly adults, the anatomical and neural interactions among the fingers that prevent the performance of isolated finger movements (9,27) could have been changed. The underlying mechanisms that prevent isolated finger movements have been discussed in the previous studies (9,27). These included biomechanical connections between the fingers in multitendoned finger muscles (26), functionally coupled motor units acting on different fingers in multitendoned finger muscles (12,19), and the convergence and divergence of output from the primary motor cortex for the activation of hand muscles (15,25). However, the age-induced changes in the anatomical and neural interactions affecting finger independence are still unknown.
It is then possible that age-related changes in central neural function were the main reason why tapping performance declined in elderly subjects because the age-related decline in the tapping rates, in particular, the remarkable decline in the double-finger tapping, may not be explained by the factors discussed above. In other words, the tapping rates of the double-finger tapping may be more sensitive to age-related changes in central neural function comparing with those of the single-finger tapping. Previous imaging studies for elderly adults have frequently found greater activation in elderly subjects in several regions compared with young subjects even when simple motor tasks were performed by the elderly subjects at the same level of accuracy and speed as the young subjects' (6,11,20). It is not clear what accounts for the age-related changes in the brain activation. One explanation is that the changes in the brain activation for older people may reflect compensatory processes in cortical and subcortical function allowing the performance level to be maintained at the same level as young people. Our positron emission tomography study demonstrated that more extensive cortical and subcortical activation was required when young adults performed more difficult motor tasks (e.g., the double-finger tapping) comparing with less difficult motor tasks (e.g., the single-finger tapping) (4). Thus, with increasing demands, more regions of the motor network may be recruited when the young adults perform the double-finger tapping. Taken together, the age-related decline in all conditions of the tapping test and more prominent decline in the double-finger tapping suggest that additional brain activation in elderly adults may no longer be sufficient to maintain the performance level at the level of young adults when the task is extremely difficult, as in the case of the tapping tasks used here.
Finally, the results of correlation analysis indicate that the double-finger tapping has a potential to explore different aspects of motor function from the single-finger tapping (Table 1). With the selection of specific fingers in the single-finger tapping as well as finger-pairs in the double-finger tapping, it is possible to produce a gradation of task difficulty, which can demand different levels of brain activation. This is not the case with motor tasks such as simple tapping with hand movements or pegboard tests, which were often used in previous studies. The independence of the tapping rate from the time taken for the pegboard test (Table 2) also supports the idea that the tapping test used here is specific to dynamic motor function of the fingers and not simply a reflection of slower movements in the elderly adults. It is proposed that the tapping test that we used can be used to create a database from a broader population including normal and pathological individuals. Ultimately, the technique may provide a useful tool for the detection of functional abnormalities of the fingers, which are sensitive to brain function.
This work was supported in part by grant 18800041 from the Japan Society for the Promotion of Science and by a grant from the Uehara Memorial Foundation, Japan. The authors thank Dr. Taizo Sadahiro, Prefectural University of Kumamoto, and Dr. Hiroshi Kinoshita, Osaka University, for their advice about statistics. The authors thank Mr. Masato Nishiwaki, Prefectural University of Kumamoto, for technical support. The authors are also truly thankful for the anonymous reviewers' valuable and constructive comments. The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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