Selective recruitment of single motor units in human flexor digitorum superficialis muscle during flexion of individual fingers
1 School of Physiotherapy, University of Sydney, Australia
2 Prince of Wales Medical Research Institute, University of New South Wales, Sydney, NSW 2036, Australia
Abstract
Flexor digitorum superficialis (FDS) is an extrinsic multi-tendoned muscle which flexes the proximal interphalangeal joints of the four fingers. It comprises four digital components, each with a tendon that inserts onto its corresponding finger. To determine the degree to which these digital components can be selectively recruited by volition, we recorded the activity of a single motor unit in one component via an intramuscular electrode while the subject isometrically flexed each of the remaining fingers, one at a time. The finger on which the unit principally acted was defined as the ‘test finger’ and that which flexed isometrically was the ‘active’ finger. Activity in 79 units was recorded. Isometric finger flexion forces of 50% maximum voluntary contraction (MVC) activated less than 50% of single units in components of FDS acting on fingers that were not voluntarily flexed. With two exceptions, the median recruitment threshold for all active–test finger combinations involving the index, middle, ring and little finger test units was between 49 and 60% MVC (60% MVC being the value assigned to those not recruited). The exceptions were flexion of the little finger while recording from ring finger units (median: 40% MVC), and vice versa (median: 2% MVC). For all active–test finger combinations, only 35/181 units were activated when the active finger flexed at less than 20% MVC, and the fingers were adjacent for 28 of these. Functionally, to recruit FDS units during grasping and lifting, relatively heavy objects were required, although systematic variation occurred with the width of the object. In conclusion, FDS components can be selectively activated by volition and this may be especially important for grasping at high forces with one or more fingers.
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Introduction
Independent finger movements are a characteristic of the human hand that allows superior manual dexterity compared with non-human primates. Despite this ability to move fingers separately, there is a limit to the extent of this independence (e.g. Kilbreath & Gandevia, 1994; Hager-Ross & Schieber, 2000; Zatsiorsky et al. 2000; Kilbreath et al. 2002; Reilly & Schieber, 2003; for review see Schieber & Santello, 2004). One reason for this limitation may reside in the control of the multi-tendoned extrinsic muscles of the hand, which have bellies in the forearm and tendons to individual fingers. It is unlikely to be limited by control of the intrinsic muscles, which have their origins and insertions within the hand, as they can be independently recruited for individual fingers, even in the absence of peripheral feedback (Gandevia et al. 1990). The ability to produce independent finger movements must therefore be affected by the degree to which the extrinsic ‘muscles’ are divided into separate anatomical ‘compartments’ and the degree to which the central nervous system can recruit independently motor units within these compartments.
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Studies of flexor digitorum profundus (FDP) have revealed that it is not possible to selectively flex one distal interphalangeal joint, even at low forces, without inadvertent recruitment of motor units involved in the flexion of adjacent fingers (Kilbreath & Gandevia, 1994; Reilly & Schieber, 2003). It is unknown whether the other multi-tendoned extrinsic flexor, flexor digitorum superficialis (FDS), which flexes the proximal interphalangeal joint, behaves similarly. The anatomical arrangement of the FDS muscle bellies is more complex than for FDP (Wood Jones, 1949). For example, the little and index fingers have separate muscle bellies arising from an intermediate tendon from a proximal common muscle belly whereas the middle digital component arises from the radius and interosseous membrane. The present study was therefore designed to investigate the degree of independence among the digital components of the FDS muscle using intramuscular single motor unit recordings during voluntary contractions. In addition, we assessed the recruitment of FDS during grasping with the fingers and thumb.
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Methods
One male and five female volunteer subjects participated. They ranged in age from 24 to 49 years. Subjects did not have any neurological or musculoskeletal disorder affecting the hand. The right hand was tested in all but one subject and 5 of the 6 subjects were right-handed. The subject who was tested on the left side was right-handed but previous surgery prevented use of that side. Informed consent was given prior to the experiment. The procedures were approved by the local ethics committee and the study was conducted according to guidelines in the Declaration of Helsinki. There were 26 experimental recording sessions, with each subject studied between one and seven times.
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Experimental design
The activity of a single motor unit was recorded from one digital component of FDS with intramuscular electrodes. The aim was to identify the force at which a unit first began to fire repetitively when another component of FDS contracted isometrically to flex another finger. The finger on which the motor unit principally acted was termed the ‘test’ finger, and the finger exerting volitional force, or flexing, was termed the ‘active’ finger.
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To determine the finger on which the motor units principally acted, the subject performed a series of gentle contractions in which no external resistance was applied. The dorsum of the hand and forearm rested on the table, and all joints of the hand were immobilized except for the one that the subject was instructed to flex. The subject systematically flexed, in turn, each proximal and each distal interphalangeal (IP) joint of all fingers and the IP joint of the thumb. To differentiate specifically between the activity produced with flexion of the distal or proximal IP joint, the proximal and middle finger phalanges were restrained for flexion of the distal IP joint whereas only the proximal phalanx was restrained for flexion of the proximal IP joint. Units were only accepted if they were recruited during flexion of the proximal IP joint but not the distal IP joint of only one finger. Few units were rejected because of ambiguity about their identification (< 5%). This approach is the same as that used previously to examine FDP (Kilbreath & Gandevia, 1994).
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After identification of the finger on which the unit acted, the forearm was pronated 90 deg and, with the forearm resting on the table, the hand was placed in the experimental apparatus (Fig. 1A), the unit was checked with weak voluntary contractions, and formal sequences of contractions began. A data set was defined as ‘complete’ for one motor unit when data were collected from four ‘sequences’, i.e. when each finger flexed at the proximal IP joint. We aimed to collect two complete sets of data for each test finger from each subject. However, relatively few units were obtained for the little finger component of FDS, probably due to its small size and occasional absence in humans (Ohtani, 1979; Gray, 1989; Bickerton et al. 1997; Gonzalez et al. 1997). This approach is similar to that used previously to examine FDP (Kilbreath & Gandevia, 1994).
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A, diagram of testing position for the main experiment and for measurement of the maximum force produced by isometric flexion at the proximal IP joint. B, coordinates for electrode insertion sites in the right forearm for the digital components of the flexor digitorum superficialis (FDS) muscle in all subjects. The x-axis represents standardized forearm length and the y-axis the forearm width. Dotted lines represent the midlines in the vertical and horizontal planes of the forearm. The apparent overlap of territories for each unit type reflects the complex, layered structure of FDS and individual variation.
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In a separate experimental session for each subject, the maximal force produced by isometric flexion at the proximal IP joint of each finger was measured in turn, with the hand in the same position as that used for the main experiment involving motor unit recording (Fig. 1A). The subject's forearm was positioned in neutral rotation, resting on the table, and the forearm and wrist were stabilized with external supports. The fingers were loosely positioned around a vertical pillar with the metacarpophalangeal joints in approximately 20 deg flexion. The proximal IP joint was positioned in approximately 60 deg flexion. An adjustable clamp held the proximal phalanges of all fingers tightly against the pillar to minimize any movement of proximal joints. A solid ring attached to a calibrated load cell was placed over the centre of the middle phalanx of the finger being tested, with the line of pull perpendicular to the phalanx (Fig. 1A). Three maximal voluntary contractions (MVCs) were recorded for flexion at the proximal IP joint of each finger and the highest peak force was recorded as the maximum. The average maximal force was 95.1 N (range: 68.6–107.9 N) for the index, 104.0 N (range: 65.7–138.3 N) for the middle, 79.4 N (range: 49.0–99.1 N) for the ring, and 49 N (range: 23.5–65.7 N) for the little finger. Subjects received visual feedback of force and verbal encouragement during all maximal efforts.
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EMG recording and electrode sites
Optimal locations for insertion of electrodes into the digital components of FDS were determined in separate investigations based on examination of cadavers, ultrasonography combined with recording EMG with monopolar needle electrodes, and descriptions by other investigators (Bickerton et al. 1997; Burgar et al. 1997). After each successful recording, the location of the point of electrode insertion was recorded based on the distance along the forearm from the medial epicondyle of the elbow and the distance from the medial border of the forearm. These values were then expressed as percentages of the length of the forearm from the medial epicondyle of the elbow to the ulnar styloid of the wrist, and the width of the forearm (Fig. 1B).
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Intramuscular fine-wire electrodes, made from two strands of Teflon-coated stainless-steel wire (75 μm diameter), were inserted using a stainless-steel needle (38 mm length, 22–25 gauge) into the volar surface of the forearm. Up to 1 mm of insulation was removed from the ends of the wires. The needle was inserted perpendicular to the skin with the forearm supinated on the table, but for some ring finger units, the needle was inserted on a slightly radial angle. To minimize discomfort, electrodes were inserted with the forearm muscles relaxed and the fingers held in comfortable flexion, mimicking the position used for testing. Once placed, the needle was withdrawn to leave the wires hooked in the muscle and the subject performed a strong isometric contraction of all finger flexors to embed the electrodes.
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The EMG was amplified (3000–30 000 times), filtered (16–3000 Hz) and then directed to a dual-time amplitude window discriminator with delay (BAK DDIS-1, Germantown, MD, USA) so that the shape of the recruited single motor unit potential could be displayed on a digital storage oscilloscope. The shape of the test motor unit potential was monitored continuously and this enabled the experimenters to ensure that activity was recorded from the same unit. Definitive analysis occurred off-line.
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A recording site was acceptable if single motor unit activity was recorded only with isolated flexion of the proximal IP joint of one finger, with the hand resting on the table (see above). Thus, single unit activity was not produced by flexion at the distal IP joint of the same finger or flexion at the proximal IP or distal IP joints of the other fingers. If this criterion was not met, the electrode was withdrawn. This criterion was necessary because intramuscular electrodes can record single unit activity in anatomically adjacent muscles (Hodges & Gandevia, 2000). The location points for successful electrode insertions for individual digital components of FDS were then used as a reference for further testing on the same subject. EMG and force data were collected and stored to disk via an interface (CED 1401, Cambridge Electronic Design, Cambridge, UK) and all off-line analyses were performed using Spike 2 (version 4.05).
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Once single units had been fully identified, the subject's hand was positioned in the testing apparatus (Fig. 1A). The ring attached to the load cell was placed around the centre of the middle phalanx of the active finger. The subject then flexed the proximal IP joint of the active finger isometrically, following a visual target on a monitor, which ramped to 50% MVC over 5 s.
For each finger, subjects performed a minimum of three ramps. The order of testing the active fingers was varied between units. Activity in the test unit was recorded before and after each set of ramp contractions to ensure the electrode remained positioned correctly. For this, a subject gently flexed the test finger isometrically until the motor unit was recruited. Thus, data collection consisted of recording of the test unit followed by three ramp contractions followed by recording the test unit again (Fig. 2). The ring attached to the load cell was then moved to another finger and the procedure repeated. All fingers, including the test finger, were tested if the electrode remained stable. Typically, activity from two or three units in digital components of the muscle was tested in one experimental session.
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A, single unit activity of the middle finger component of FDS recorded during weak contractions of the middle finger before and after contractions of the index finger. B, recording of single unit activity of the index finger component of FDS during weak contractions of the index finger and during three ramp contractions of the little finger to 50% maximum voluntary contraction (MVC). Note that forces close to 50% MVC were reached before recruitment occurred. Recruitment of the test unit was checked before and after the ramps and in both panels potentials from the unit have been superimposed.
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Additional studies
In six studies, FDS activity was also monitored while the subject grasped and lifted an upright cylinder. Two differently sized cylinders were used: a wide cylinder (75 mm wide x 110 mm, initial weight 0.40 kg) and a narrow cylinder (40 mm x 110 mm, initial weight 0.18 kg). The subject was asked to grasp the middle of the cylinder in a natural way using the thumb and all fingers, and then to lift it approximately 100 mm vertically and then replace it on the table. Thus, the cylinder was held with the distal phalanx. Lead shot was added in 0.25 N increments to each cylinder and the lifting repeated until the test unit was recruited. The procedure was then repeated with the other cylinder to determine if the width of grasp influenced FDS involvement in the task. Two index finger units, one middle finger unit, seven ring finger units and one little finger unit were studied.
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Data processing and analysis
Off-line, the recruitment threshold was determined for each active–test finger combination. The threshold was defined as the minimum force exerted by the active finger to recruit the test unit and was expressed as a percentage of MVC at the proximal IP joint of the active finger. An arbitrary value of 60% MVC was assigned to any ramp in which there was no recruitment of the test unit with contractions of the active finger up to 50% MVC (Fig. 2). The recruitment threshold in the three ramps was recorded and the mean of the three values was obtained.
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To determine the degree of independence among the digital components of the FDS, a two-way analysis of variance (ANOVA) was used in which the threshold forces that produced activity in a test finger unit were compared. For this analysis, the between-group factor was the test finger on which the unit acted, and the within-group factor was the active finger. In addition, each group of test units was also analysed separately to determine whether the recruitment thresholds among the active fingers differed. Where significant differences were identified, planned contrasts were used.
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Additional analyses were undertaken to examine other aspects of the data. They included (i) a repeated-measures analysis of variance to determine if there were any differences in recruitment thresholds among the three ramp contractions, (ii) 2 tests to determine if the proportion of units not recruited with flexion of the active finger to 50% MVC was the same among the different fingers, (iii) paired t tests to determine whether the recruitment threshold differed when the two different cylinders were lifted, and (iv) Spearman's rank correlation to determine whether the location of the finger influenced the weight at which it was activated during the grasping task. Lastly, data for FDS were compared with the results for FDP (Kilbreath & Gandevia, 1994) using t tests.
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Results
Data were collected from 79 low threshold motor units of FDS. These units produced force that acted on the digits of the hand: 21 acted on the index finger, 18 on the middle finger, 32 on the ring finger and 8 on the little finger. Most of the test units were recruited at less than 1% MVC for flexion at the proximal IP joint of the test finger (range for index finger, 0.2–6.2% MVC; middle finger, 0.01–2.0% MVC; ring finger, 0.03–2.2% MVC; and little finger, 0.3–1.02% MVC). These recruitment thresholds did not differ between fingers (F = 0.317, P = 0.813).
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The digital components of FDS were usually activated selectively in voluntary contractions. Thus, when adjacent or more remote fingers flexed at the proximal IP joint, there was frequently (although not exclusively) no recruitment of the motor unit that acted on the test finger. A typical example is shown in Fig. 2A. Furthermore, when the recruitment thresholds from ‘complete sets’ were analysed, there was no significant difference in selectivity among the three groups of units (index, middle and ring units; P = 0.530); however, there was an interaction between the finger on which the units acted and the force at which flexion of the other fingers produced activity in the test finger unit (P = 0.001) suggesting that the recruitment thresholds were not similar among the fingers. Little finger units were not included in this analysis as there was only one complete set of data. Pooled data from a single subject are shown in Fig. 3 and are representative of the data derived from the group of subjects (Fig. 4). In both figures, the median recruitment thresholds for motor units acting on a finger are joined by a line.
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Separate panels show the recruitment thresholds for motor units in the index, middle and ring digital components of FDS during flexion of the index, middle, ring and little fingers at the proximal interphalangeal (IP) joint. The open circles indicate that digit on which the units principally acted and the numbers below reflect the number of units from which recordings were made. The numbers under the filled circles (i.e. the non-test fingers) reflect the number of successful recordings made in which the non-test finger flexed. The line indicates the median threshold for that finger. Units had low force thresholds when the test finger flexed (< 5% MVC), but usually had much higher thresholds when other fingers flexed. Units were classified as ‘not recruited’ if they were not active at contraction strengths of 50% MVC (shown above dotted horizontal lines).
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‘All data’ consists of complete and incomplete sets of data, i.e. data from the test unit combined with data from one, two or three active fingers. ‘Complete sets’ consists only of data from the test unit when combined with data from three active fingers. The line indicates the median threshold for that finger. Data are plotted in the same way as in Fig. 3. The total number of finger flexions that were assigned 60% as they did not produce activity in the test units were 36 of 61 and 70 of 120 for the incomplete and complete data sets, respectively.
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When each group of units was analysed separately to determine if the recruitment thresholds for the three non-test fingers were similar, we found that the recruitment thresholds for the non-test fingers were not significantly different for the index and middle finger units (index finger units, P = 0.687; middle finger units, P = 0.395). In contrast, the recruitment thresholds for the three non-test fingers of the ring finger units were significantly different (P = 0.017). Planned contrasts revealed that the recruitment threshold when the little finger flexed was significantly different to that for when the index finger flexed (P = 0.004) but not for when the middle finger flexed (P = 0.141). When the little finger flexed, there was a lower recruitment threshold in ring finger units than when the middle and index fingers flexed (Figs 3 and 4). Sixteen of 27 ring finger units were recruited with little finger flexion.
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Analyses of recruitment may have been biased by assignation of a recruitment value of 60% MVC for units not recruited at the top of the ramped voluntary contraction to 50% MVC (see Methods). Thus, to check that this had not unduly influenced the main result, the number of active finger contractions (excluding those involving the test finger) that did not recruit the test unit with contractions reaching 50% MVC was compared among the groups of units. Overall, 24 of 42 contractions resulted in no recruitment of index finger test units, 30 of 44 resulted in no recruitment of middle finger units, 47 of 81 resulted in no recruitment of ring finger units and 5 of 14 resulted in no recruitment of little finger units (Fig. 5). These frequencies did not differ between the index, middle, ring and little finger units (2 = 1.49; P > 0.05).
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For contractions of non-test fingers, more than 50% of units were not recruited with contraction ramps to 50% MVC, except for little finger units when the ring finger was contracting.
Recordings were made from only eight little finger units from two subjects and included only one complete set of data. However, activity occurred in these little finger units when the ring finger exerted significantly lower force compared with that exerted by flexion of either the index or middle fingers (P = 0.004). Five of the eight little finger units were recruited when the ring finger exerted very low forces (Fig. 4).
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While data in Figs 3 and 4 reveal that median recruitment thresholds were high for most combinations of test and active fingers, some recruitment thresholds were well below 50% MVC. This phenomenon occurred mostly with the little and ring finger combination, but occasionally it applied to the other digital components of FDS. Overall, 35/181 (19%) of combinations were recruited at less than 20% MVC. For example, for index finger test units there were 8 occasions (out of 42) in which motor unit recruitment occurred at less than 20% MVC when another finger flexed (specifically middle finger, 3; ring finger, 3; and little finger, 2). Examination of the units recruited at forces < 20% MVC revealed that when this occurred for one active finger, it was not necessarily evident for flexion of the remaining two fingers. Recruitment at force < 20% MVC occurred when the active finger was adjacent to the test finger on 28 of the 35 occasions, and when the test finger was 2 or 3 away from the active finger recruitment at low force occurred on only 7 of the 35 occasions.
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To assess whether recruitment thresholds for contractions involving the non-test finger varied in the set of three ramps, thresholds were compared for those sequences in which the three consecutive ramp contractions occurred at intervals of approximately 5 s, and recruitment occurred in at least two of the three ramps. A small ‘warm-up’ effect occurred (P = 0.005), such that the test unit was recruited at greater force during the first ramp (mean ± S.D.: 27.8 ± 22.0% MVC) than during either the second (20.5 ± 18.7% MVC) or third ramp (21.0 ± 17.8% MVC, P = 0.013). There was no difference between the second and third ramps.
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Finally, to determine when the units in FDS were recruited during grasping, subjects were required to grasp, lift and then replace cylinders of different widths (see Methods). The threshold weight that recruited the FDS units was between 0.4 and 1.0 kg for the wide cylinder, and between 0.18 and 0.58 kg for the narrow cylinder. The recruitment thresholds were lower when lifting the narrow cylinder (paired t test: P = 0.006). The threshold weight increased progressively for fingers towards the ulnar side of the hand when grasping the wide cylinder (r = 0.637; P = 0.035).
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Discussion
The present study demonstrates a high degree of independence among the digital components of the human FDS muscle during voluntary contractions, particularly for the index and middle components. Commonly, isometric finger flexion forces up to 50% MVC activated less than half of the motor units from which we recorded in a component of FDS acting on another finger that was not voluntarily flexing. With two exceptions, the median recruitment threshold for all active–test finger combinations involving the index, middle, ring and little finger test units was between 49 and 60% MVC. The exceptions were flexion of the little finger while recording from ring finger units, and flexion of the ring finger while recording from little finger units. Regardless of which of these fingers was flexing, the recruitment threshold for units from the other finger were low (median recruitment thresholds: 2–40%).
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In comparison to the other multi-tendoned extrinsic finger muscles of the human hand, FDS is anatomically more compartmentalized. The middle digital component arises from the radius and interosseous membrane, and is more distinct from the remaining three digital components. The little and index fingers have separate muscle bellies arising from an intermediate tendon from a proximal common muscle belly. The ring finger also has its own muscle belly but derives some fibres from the proximal common muscle belly (Wood Jones, 1949; Ohtani, 1979; Brand & Hollister, 1999). In contrast, the other multi-tendoned extrinsic finger muscles, FDP and the extensor digitorum communis (EDC), probably have a higher degree of mechanical connection between their digital components. As examples, the EDC tendons at the level of the dorsum of the hand are joined by juncturae tendinum (e.g. Wood Jones, 1949; von Schroeder & Botte, 2001), while FDP has connective tissue links at the level of the carpal tunnel and between distinct digital components (Wood Jones, 1949; Leijinse et al. 1997).
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Given the anatomy described above, there are likely to be separate neuromuscular compartments within FDS. A neuromuscular compartment is a region of relatively uniform muscle architecture, innervated by a primary nerve branch (English & Weeks, 1984; Liu et al. 1997). Some evidence exists for such compartments for FDP in the macaque and rhesus monkey (Schieber, 1993; Serlin & Schieber, 1993) and in humans (Fleckenstein et al. 1992; Danion et al. 2002). There is also evidence for compartmentalization of human EDC which is responsible for extending the fingers (Keen & Fuglevand, 2004). This muscle consists of four discrete regions of muscle fibres with each region acting predominantly on one finger (Keen & Fuglevand, 2004).
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A feature of these findings may be that descending motor commands can be selectively directed to components of FDS. In monkeys, the descending inputs from the single corticomotoneuronal cells to motoneurones of intrinsic hand muscles are less divergent than to extrinsic hand muscles (Lemon & Muir, 1983; Buys et al. 1986; Maier et al. 1993). Such data are not available for digital components of the extrinsic muscles. However, in monkeys, direct corticomotoneuronal connections may not be essential for dextrous finger movements (Sasaki et al. 2004). FDS in humans may receive more focally directed descending inputs than other extrinsic hand muscles, making relatively independent movements generated by parts of this muscle possible. Thus, FDS may have a special role in independent finger control when higher forces are applied at or beyond the proximal IP joint.
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There were two exceptions to the high degree of volitional selectivity in the majority of the FDS recordings. Single motor unit activity occurred in the test ring finger at lower forces when the little finger flexed, and vice versa (Figs 3 and 4). This suggests that the descending commands to these two digital components of FDS are functionally less well differentiated. In addition, motor units from these components of FDS may distribute tension to more than one digital component. Single motor units distribute force to adjacent fingers in the cat EDC muscle (Fritz et al. 1992) and the extensor digiti quarti et quinti in the macaque monkey (Schieber et al. 1997). Motor units containing sets of muscle fibres that act on more than one finger, and in particular for the little finger, may also exist within the FDP (Kilbreath et al. 2002). Lateral force transmission could also contribute to the distribution of force between the ring and little finger components of FDS via tissue interconnections as the ring finger component of FDS lies superficial to the little finger component. Wood Jones (1949) describes the little finger component of FDS as being connected variably by muscle fibres to the ring finger component and Ohtani (1979) describes connections between the intermediate tendon and the ring finger component.
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Our recordings were from the distal muscle bellies of FDS, and not from its proximal common muscle. It is possible that this proximal section of the muscle does not have as high a degree of volitional selectivity as the main index, middle and ring distal digital components, and its motor units distribute tension to more than one finger.
Comparison of recruitment thresholds for FDS when non-test fingers are flexing with data from a similar study for FDP suggests that these two extrinsic flexors of the fingers behave differently for the index, middle and ring finger but similarly for the little finger (Fig. 6). Using the same selection criteria for motor units, Kilbreath & Gandevia (1994) found that flexion at the distal IP joint of one finger in human subjects resulted in single motor unit activity in adjacent fingers at very low forces (commonly less than 5%). However, in the current study of FDS, and as shown in Fig. 5, flexion at the individual proximal IP joint up to 50% MVC did not usually recruit low-threshold single motor units for the index, middle and ring fingers. In contrast, flexion at the proximal IP joint of the ring finger at low forces produced single motor unit activity in little finger components for both FDP and FDS.
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Means and standard deviation for the thresholds of recruitment of the index, middle, ring and little finger units are shown. t tests revealed that FDS was recruited at higher forces than FDP for most combinations: * P < 0.01, + P < 0.05. The difference between the two finger flexors may be underestimated as a value of 60% MVC was arbitrarily used when FDS was not recruited (see Methods). The exception was recruitment of little finger units of FDS which behaved similarly to those of FDP.
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Previous EMG studies have found that FDS is recruited during active power grip (Long et al. 1970) and that FDP is the primary contributor to unloaded finger flexion (Long & Brown, 1962, 1964; Long, 1968; Kinoshita et al. 1995; Li, 2002). In the present study, the recruitment thresholds for FDS were lower when grasping a narrow compared with a wide cylinder. In addition, recruitment thresholds were lower for motor units acting on the radial compared with the ulnar side of the hand. Both results may reflect the length–tension relationships of the flexors, and the distribution of force between FDP and FDS. In a full grasp, fingers on the radial side of the hand exert more force when lifting as compared to those on the ulnar side of the hand (Kinoshita et al. 1995; Li, 2002).
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In conclusion, the index, middle and ring digital components of the FDS appear to be activated by volition in a more selective way than for FDP. Typically, large forces up to 50% MVC in an active finger recruited less than half the single motor units in another digital component of FDS not voluntarily flexing. In contrast, but similar to FDP, motor units in little finger components of FDS were activated by flexion of the adjacent ring finger at low forces. One explanation for the observed arrangement is that it may reduce the neural demands during grasping at high forces, with the object secured firmly on the ulnar side of the hand while it is positioned using the index finger and thumb. Additionally, it may assist grasps involving fewer than the four fingers.
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2 Prince of Wales Medical Research Institute, University of New South Wales, Sydney, NSW 2036, Australia
Abstract
Flexor digitorum superficialis (FDS) is an extrinsic multi-tendoned muscle which flexes the proximal interphalangeal joints of the four fingers. It comprises four digital components, each with a tendon that inserts onto its corresponding finger. To determine the degree to which these digital components can be selectively recruited by volition, we recorded the activity of a single motor unit in one component via an intramuscular electrode while the subject isometrically flexed each of the remaining fingers, one at a time. The finger on which the unit principally acted was defined as the ‘test finger’ and that which flexed isometrically was the ‘active’ finger. Activity in 79 units was recorded. Isometric finger flexion forces of 50% maximum voluntary contraction (MVC) activated less than 50% of single units in components of FDS acting on fingers that were not voluntarily flexed. With two exceptions, the median recruitment threshold for all active–test finger combinations involving the index, middle, ring and little finger test units was between 49 and 60% MVC (60% MVC being the value assigned to those not recruited). The exceptions were flexion of the little finger while recording from ring finger units (median: 40% MVC), and vice versa (median: 2% MVC). For all active–test finger combinations, only 35/181 units were activated when the active finger flexed at less than 20% MVC, and the fingers were adjacent for 28 of these. Functionally, to recruit FDS units during grasping and lifting, relatively heavy objects were required, although systematic variation occurred with the width of the object. In conclusion, FDS components can be selectively activated by volition and this may be especially important for grasping at high forces with one or more fingers.
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Introduction
Independent finger movements are a characteristic of the human hand that allows superior manual dexterity compared with non-human primates. Despite this ability to move fingers separately, there is a limit to the extent of this independence (e.g. Kilbreath & Gandevia, 1994; Hager-Ross & Schieber, 2000; Zatsiorsky et al. 2000; Kilbreath et al. 2002; Reilly & Schieber, 2003; for review see Schieber & Santello, 2004). One reason for this limitation may reside in the control of the multi-tendoned extrinsic muscles of the hand, which have bellies in the forearm and tendons to individual fingers. It is unlikely to be limited by control of the intrinsic muscles, which have their origins and insertions within the hand, as they can be independently recruited for individual fingers, even in the absence of peripheral feedback (Gandevia et al. 1990). The ability to produce independent finger movements must therefore be affected by the degree to which the extrinsic ‘muscles’ are divided into separate anatomical ‘compartments’ and the degree to which the central nervous system can recruit independently motor units within these compartments.
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Studies of flexor digitorum profundus (FDP) have revealed that it is not possible to selectively flex one distal interphalangeal joint, even at low forces, without inadvertent recruitment of motor units involved in the flexion of adjacent fingers (Kilbreath & Gandevia, 1994; Reilly & Schieber, 2003). It is unknown whether the other multi-tendoned extrinsic flexor, flexor digitorum superficialis (FDS), which flexes the proximal interphalangeal joint, behaves similarly. The anatomical arrangement of the FDS muscle bellies is more complex than for FDP (Wood Jones, 1949). For example, the little and index fingers have separate muscle bellies arising from an intermediate tendon from a proximal common muscle belly whereas the middle digital component arises from the radius and interosseous membrane. The present study was therefore designed to investigate the degree of independence among the digital components of the FDS muscle using intramuscular single motor unit recordings during voluntary contractions. In addition, we assessed the recruitment of FDS during grasping with the fingers and thumb.
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Methods
One male and five female volunteer subjects participated. They ranged in age from 24 to 49 years. Subjects did not have any neurological or musculoskeletal disorder affecting the hand. The right hand was tested in all but one subject and 5 of the 6 subjects were right-handed. The subject who was tested on the left side was right-handed but previous surgery prevented use of that side. Informed consent was given prior to the experiment. The procedures were approved by the local ethics committee and the study was conducted according to guidelines in the Declaration of Helsinki. There were 26 experimental recording sessions, with each subject studied between one and seven times.
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Experimental design
The activity of a single motor unit was recorded from one digital component of FDS with intramuscular electrodes. The aim was to identify the force at which a unit first began to fire repetitively when another component of FDS contracted isometrically to flex another finger. The finger on which the motor unit principally acted was termed the ‘test’ finger, and the finger exerting volitional force, or flexing, was termed the ‘active’ finger.
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To determine the finger on which the motor units principally acted, the subject performed a series of gentle contractions in which no external resistance was applied. The dorsum of the hand and forearm rested on the table, and all joints of the hand were immobilized except for the one that the subject was instructed to flex. The subject systematically flexed, in turn, each proximal and each distal interphalangeal (IP) joint of all fingers and the IP joint of the thumb. To differentiate specifically between the activity produced with flexion of the distal or proximal IP joint, the proximal and middle finger phalanges were restrained for flexion of the distal IP joint whereas only the proximal phalanx was restrained for flexion of the proximal IP joint. Units were only accepted if they were recruited during flexion of the proximal IP joint but not the distal IP joint of only one finger. Few units were rejected because of ambiguity about their identification (< 5%). This approach is the same as that used previously to examine FDP (Kilbreath & Gandevia, 1994).
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After identification of the finger on which the unit acted, the forearm was pronated 90 deg and, with the forearm resting on the table, the hand was placed in the experimental apparatus (Fig. 1A), the unit was checked with weak voluntary contractions, and formal sequences of contractions began. A data set was defined as ‘complete’ for one motor unit when data were collected from four ‘sequences’, i.e. when each finger flexed at the proximal IP joint. We aimed to collect two complete sets of data for each test finger from each subject. However, relatively few units were obtained for the little finger component of FDS, probably due to its small size and occasional absence in humans (Ohtani, 1979; Gray, 1989; Bickerton et al. 1997; Gonzalez et al. 1997). This approach is similar to that used previously to examine FDP (Kilbreath & Gandevia, 1994).
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A, diagram of testing position for the main experiment and for measurement of the maximum force produced by isometric flexion at the proximal IP joint. B, coordinates for electrode insertion sites in the right forearm for the digital components of the flexor digitorum superficialis (FDS) muscle in all subjects. The x-axis represents standardized forearm length and the y-axis the forearm width. Dotted lines represent the midlines in the vertical and horizontal planes of the forearm. The apparent overlap of territories for each unit type reflects the complex, layered structure of FDS and individual variation.
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In a separate experimental session for each subject, the maximal force produced by isometric flexion at the proximal IP joint of each finger was measured in turn, with the hand in the same position as that used for the main experiment involving motor unit recording (Fig. 1A). The subject's forearm was positioned in neutral rotation, resting on the table, and the forearm and wrist were stabilized with external supports. The fingers were loosely positioned around a vertical pillar with the metacarpophalangeal joints in approximately 20 deg flexion. The proximal IP joint was positioned in approximately 60 deg flexion. An adjustable clamp held the proximal phalanges of all fingers tightly against the pillar to minimize any movement of proximal joints. A solid ring attached to a calibrated load cell was placed over the centre of the middle phalanx of the finger being tested, with the line of pull perpendicular to the phalanx (Fig. 1A). Three maximal voluntary contractions (MVCs) were recorded for flexion at the proximal IP joint of each finger and the highest peak force was recorded as the maximum. The average maximal force was 95.1 N (range: 68.6–107.9 N) for the index, 104.0 N (range: 65.7–138.3 N) for the middle, 79.4 N (range: 49.0–99.1 N) for the ring, and 49 N (range: 23.5–65.7 N) for the little finger. Subjects received visual feedback of force and verbal encouragement during all maximal efforts.
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EMG recording and electrode sites
Optimal locations for insertion of electrodes into the digital components of FDS were determined in separate investigations based on examination of cadavers, ultrasonography combined with recording EMG with monopolar needle electrodes, and descriptions by other investigators (Bickerton et al. 1997; Burgar et al. 1997). After each successful recording, the location of the point of electrode insertion was recorded based on the distance along the forearm from the medial epicondyle of the elbow and the distance from the medial border of the forearm. These values were then expressed as percentages of the length of the forearm from the medial epicondyle of the elbow to the ulnar styloid of the wrist, and the width of the forearm (Fig. 1B).
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Intramuscular fine-wire electrodes, made from two strands of Teflon-coated stainless-steel wire (75 μm diameter), were inserted using a stainless-steel needle (38 mm length, 22–25 gauge) into the volar surface of the forearm. Up to 1 mm of insulation was removed from the ends of the wires. The needle was inserted perpendicular to the skin with the forearm supinated on the table, but for some ring finger units, the needle was inserted on a slightly radial angle. To minimize discomfort, electrodes were inserted with the forearm muscles relaxed and the fingers held in comfortable flexion, mimicking the position used for testing. Once placed, the needle was withdrawn to leave the wires hooked in the muscle and the subject performed a strong isometric contraction of all finger flexors to embed the electrodes.
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The EMG was amplified (3000–30 000 times), filtered (16–3000 Hz) and then directed to a dual-time amplitude window discriminator with delay (BAK DDIS-1, Germantown, MD, USA) so that the shape of the recruited single motor unit potential could be displayed on a digital storage oscilloscope. The shape of the test motor unit potential was monitored continuously and this enabled the experimenters to ensure that activity was recorded from the same unit. Definitive analysis occurred off-line.
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A recording site was acceptable if single motor unit activity was recorded only with isolated flexion of the proximal IP joint of one finger, with the hand resting on the table (see above). Thus, single unit activity was not produced by flexion at the distal IP joint of the same finger or flexion at the proximal IP or distal IP joints of the other fingers. If this criterion was not met, the electrode was withdrawn. This criterion was necessary because intramuscular electrodes can record single unit activity in anatomically adjacent muscles (Hodges & Gandevia, 2000). The location points for successful electrode insertions for individual digital components of FDS were then used as a reference for further testing on the same subject. EMG and force data were collected and stored to disk via an interface (CED 1401, Cambridge Electronic Design, Cambridge, UK) and all off-line analyses were performed using Spike 2 (version 4.05).
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Once single units had been fully identified, the subject's hand was positioned in the testing apparatus (Fig. 1A). The ring attached to the load cell was placed around the centre of the middle phalanx of the active finger. The subject then flexed the proximal IP joint of the active finger isometrically, following a visual target on a monitor, which ramped to 50% MVC over 5 s.
For each finger, subjects performed a minimum of three ramps. The order of testing the active fingers was varied between units. Activity in the test unit was recorded before and after each set of ramp contractions to ensure the electrode remained positioned correctly. For this, a subject gently flexed the test finger isometrically until the motor unit was recruited. Thus, data collection consisted of recording of the test unit followed by three ramp contractions followed by recording the test unit again (Fig. 2). The ring attached to the load cell was then moved to another finger and the procedure repeated. All fingers, including the test finger, were tested if the electrode remained stable. Typically, activity from two or three units in digital components of the muscle was tested in one experimental session.
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A, single unit activity of the middle finger component of FDS recorded during weak contractions of the middle finger before and after contractions of the index finger. B, recording of single unit activity of the index finger component of FDS during weak contractions of the index finger and during three ramp contractions of the little finger to 50% maximum voluntary contraction (MVC). Note that forces close to 50% MVC were reached before recruitment occurred. Recruitment of the test unit was checked before and after the ramps and in both panels potentials from the unit have been superimposed.
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Additional studies
In six studies, FDS activity was also monitored while the subject grasped and lifted an upright cylinder. Two differently sized cylinders were used: a wide cylinder (75 mm wide x 110 mm, initial weight 0.40 kg) and a narrow cylinder (40 mm x 110 mm, initial weight 0.18 kg). The subject was asked to grasp the middle of the cylinder in a natural way using the thumb and all fingers, and then to lift it approximately 100 mm vertically and then replace it on the table. Thus, the cylinder was held with the distal phalanx. Lead shot was added in 0.25 N increments to each cylinder and the lifting repeated until the test unit was recruited. The procedure was then repeated with the other cylinder to determine if the width of grasp influenced FDS involvement in the task. Two index finger units, one middle finger unit, seven ring finger units and one little finger unit were studied.
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Data processing and analysis
Off-line, the recruitment threshold was determined for each active–test finger combination. The threshold was defined as the minimum force exerted by the active finger to recruit the test unit and was expressed as a percentage of MVC at the proximal IP joint of the active finger. An arbitrary value of 60% MVC was assigned to any ramp in which there was no recruitment of the test unit with contractions of the active finger up to 50% MVC (Fig. 2). The recruitment threshold in the three ramps was recorded and the mean of the three values was obtained.
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To determine the degree of independence among the digital components of the FDS, a two-way analysis of variance (ANOVA) was used in which the threshold forces that produced activity in a test finger unit were compared. For this analysis, the between-group factor was the test finger on which the unit acted, and the within-group factor was the active finger. In addition, each group of test units was also analysed separately to determine whether the recruitment thresholds among the active fingers differed. Where significant differences were identified, planned contrasts were used.
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Additional analyses were undertaken to examine other aspects of the data. They included (i) a repeated-measures analysis of variance to determine if there were any differences in recruitment thresholds among the three ramp contractions, (ii) 2 tests to determine if the proportion of units not recruited with flexion of the active finger to 50% MVC was the same among the different fingers, (iii) paired t tests to determine whether the recruitment threshold differed when the two different cylinders were lifted, and (iv) Spearman's rank correlation to determine whether the location of the finger influenced the weight at which it was activated during the grasping task. Lastly, data for FDS were compared with the results for FDP (Kilbreath & Gandevia, 1994) using t tests.
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Results
Data were collected from 79 low threshold motor units of FDS. These units produced force that acted on the digits of the hand: 21 acted on the index finger, 18 on the middle finger, 32 on the ring finger and 8 on the little finger. Most of the test units were recruited at less than 1% MVC for flexion at the proximal IP joint of the test finger (range for index finger, 0.2–6.2% MVC; middle finger, 0.01–2.0% MVC; ring finger, 0.03–2.2% MVC; and little finger, 0.3–1.02% MVC). These recruitment thresholds did not differ between fingers (F = 0.317, P = 0.813).
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The digital components of FDS were usually activated selectively in voluntary contractions. Thus, when adjacent or more remote fingers flexed at the proximal IP joint, there was frequently (although not exclusively) no recruitment of the motor unit that acted on the test finger. A typical example is shown in Fig. 2A. Furthermore, when the recruitment thresholds from ‘complete sets’ were analysed, there was no significant difference in selectivity among the three groups of units (index, middle and ring units; P = 0.530); however, there was an interaction between the finger on which the units acted and the force at which flexion of the other fingers produced activity in the test finger unit (P = 0.001) suggesting that the recruitment thresholds were not similar among the fingers. Little finger units were not included in this analysis as there was only one complete set of data. Pooled data from a single subject are shown in Fig. 3 and are representative of the data derived from the group of subjects (Fig. 4). In both figures, the median recruitment thresholds for motor units acting on a finger are joined by a line.
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Separate panels show the recruitment thresholds for motor units in the index, middle and ring digital components of FDS during flexion of the index, middle, ring and little fingers at the proximal interphalangeal (IP) joint. The open circles indicate that digit on which the units principally acted and the numbers below reflect the number of units from which recordings were made. The numbers under the filled circles (i.e. the non-test fingers) reflect the number of successful recordings made in which the non-test finger flexed. The line indicates the median threshold for that finger. Units had low force thresholds when the test finger flexed (< 5% MVC), but usually had much higher thresholds when other fingers flexed. Units were classified as ‘not recruited’ if they were not active at contraction strengths of 50% MVC (shown above dotted horizontal lines).
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‘All data’ consists of complete and incomplete sets of data, i.e. data from the test unit combined with data from one, two or three active fingers. ‘Complete sets’ consists only of data from the test unit when combined with data from three active fingers. The line indicates the median threshold for that finger. Data are plotted in the same way as in Fig. 3. The total number of finger flexions that were assigned 60% as they did not produce activity in the test units were 36 of 61 and 70 of 120 for the incomplete and complete data sets, respectively.
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When each group of units was analysed separately to determine if the recruitment thresholds for the three non-test fingers were similar, we found that the recruitment thresholds for the non-test fingers were not significantly different for the index and middle finger units (index finger units, P = 0.687; middle finger units, P = 0.395). In contrast, the recruitment thresholds for the three non-test fingers of the ring finger units were significantly different (P = 0.017). Planned contrasts revealed that the recruitment threshold when the little finger flexed was significantly different to that for when the index finger flexed (P = 0.004) but not for when the middle finger flexed (P = 0.141). When the little finger flexed, there was a lower recruitment threshold in ring finger units than when the middle and index fingers flexed (Figs 3 and 4). Sixteen of 27 ring finger units were recruited with little finger flexion.
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Analyses of recruitment may have been biased by assignation of a recruitment value of 60% MVC for units not recruited at the top of the ramped voluntary contraction to 50% MVC (see Methods). Thus, to check that this had not unduly influenced the main result, the number of active finger contractions (excluding those involving the test finger) that did not recruit the test unit with contractions reaching 50% MVC was compared among the groups of units. Overall, 24 of 42 contractions resulted in no recruitment of index finger test units, 30 of 44 resulted in no recruitment of middle finger units, 47 of 81 resulted in no recruitment of ring finger units and 5 of 14 resulted in no recruitment of little finger units (Fig. 5). These frequencies did not differ between the index, middle, ring and little finger units (2 = 1.49; P > 0.05).
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For contractions of non-test fingers, more than 50% of units were not recruited with contraction ramps to 50% MVC, except for little finger units when the ring finger was contracting.
Recordings were made from only eight little finger units from two subjects and included only one complete set of data. However, activity occurred in these little finger units when the ring finger exerted significantly lower force compared with that exerted by flexion of either the index or middle fingers (P = 0.004). Five of the eight little finger units were recruited when the ring finger exerted very low forces (Fig. 4).
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While data in Figs 3 and 4 reveal that median recruitment thresholds were high for most combinations of test and active fingers, some recruitment thresholds were well below 50% MVC. This phenomenon occurred mostly with the little and ring finger combination, but occasionally it applied to the other digital components of FDS. Overall, 35/181 (19%) of combinations were recruited at less than 20% MVC. For example, for index finger test units there were 8 occasions (out of 42) in which motor unit recruitment occurred at less than 20% MVC when another finger flexed (specifically middle finger, 3; ring finger, 3; and little finger, 2). Examination of the units recruited at forces < 20% MVC revealed that when this occurred for one active finger, it was not necessarily evident for flexion of the remaining two fingers. Recruitment at force < 20% MVC occurred when the active finger was adjacent to the test finger on 28 of the 35 occasions, and when the test finger was 2 or 3 away from the active finger recruitment at low force occurred on only 7 of the 35 occasions.
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To assess whether recruitment thresholds for contractions involving the non-test finger varied in the set of three ramps, thresholds were compared for those sequences in which the three consecutive ramp contractions occurred at intervals of approximately 5 s, and recruitment occurred in at least two of the three ramps. A small ‘warm-up’ effect occurred (P = 0.005), such that the test unit was recruited at greater force during the first ramp (mean ± S.D.: 27.8 ± 22.0% MVC) than during either the second (20.5 ± 18.7% MVC) or third ramp (21.0 ± 17.8% MVC, P = 0.013). There was no difference between the second and third ramps.
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Finally, to determine when the units in FDS were recruited during grasping, subjects were required to grasp, lift and then replace cylinders of different widths (see Methods). The threshold weight that recruited the FDS units was between 0.4 and 1.0 kg for the wide cylinder, and between 0.18 and 0.58 kg for the narrow cylinder. The recruitment thresholds were lower when lifting the narrow cylinder (paired t test: P = 0.006). The threshold weight increased progressively for fingers towards the ulnar side of the hand when grasping the wide cylinder (r = 0.637; P = 0.035).
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Discussion
The present study demonstrates a high degree of independence among the digital components of the human FDS muscle during voluntary contractions, particularly for the index and middle components. Commonly, isometric finger flexion forces up to 50% MVC activated less than half of the motor units from which we recorded in a component of FDS acting on another finger that was not voluntarily flexing. With two exceptions, the median recruitment threshold for all active–test finger combinations involving the index, middle, ring and little finger test units was between 49 and 60% MVC. The exceptions were flexion of the little finger while recording from ring finger units, and flexion of the ring finger while recording from little finger units. Regardless of which of these fingers was flexing, the recruitment threshold for units from the other finger were low (median recruitment thresholds: 2–40%).
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In comparison to the other multi-tendoned extrinsic finger muscles of the human hand, FDS is anatomically more compartmentalized. The middle digital component arises from the radius and interosseous membrane, and is more distinct from the remaining three digital components. The little and index fingers have separate muscle bellies arising from an intermediate tendon from a proximal common muscle belly. The ring finger also has its own muscle belly but derives some fibres from the proximal common muscle belly (Wood Jones, 1949; Ohtani, 1979; Brand & Hollister, 1999). In contrast, the other multi-tendoned extrinsic finger muscles, FDP and the extensor digitorum communis (EDC), probably have a higher degree of mechanical connection between their digital components. As examples, the EDC tendons at the level of the dorsum of the hand are joined by juncturae tendinum (e.g. Wood Jones, 1949; von Schroeder & Botte, 2001), while FDP has connective tissue links at the level of the carpal tunnel and between distinct digital components (Wood Jones, 1949; Leijinse et al. 1997).
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Given the anatomy described above, there are likely to be separate neuromuscular compartments within FDS. A neuromuscular compartment is a region of relatively uniform muscle architecture, innervated by a primary nerve branch (English & Weeks, 1984; Liu et al. 1997). Some evidence exists for such compartments for FDP in the macaque and rhesus monkey (Schieber, 1993; Serlin & Schieber, 1993) and in humans (Fleckenstein et al. 1992; Danion et al. 2002). There is also evidence for compartmentalization of human EDC which is responsible for extending the fingers (Keen & Fuglevand, 2004). This muscle consists of four discrete regions of muscle fibres with each region acting predominantly on one finger (Keen & Fuglevand, 2004).
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A feature of these findings may be that descending motor commands can be selectively directed to components of FDS. In monkeys, the descending inputs from the single corticomotoneuronal cells to motoneurones of intrinsic hand muscles are less divergent than to extrinsic hand muscles (Lemon & Muir, 1983; Buys et al. 1986; Maier et al. 1993). Such data are not available for digital components of the extrinsic muscles. However, in monkeys, direct corticomotoneuronal connections may not be essential for dextrous finger movements (Sasaki et al. 2004). FDS in humans may receive more focally directed descending inputs than other extrinsic hand muscles, making relatively independent movements generated by parts of this muscle possible. Thus, FDS may have a special role in independent finger control when higher forces are applied at or beyond the proximal IP joint.
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There were two exceptions to the high degree of volitional selectivity in the majority of the FDS recordings. Single motor unit activity occurred in the test ring finger at lower forces when the little finger flexed, and vice versa (Figs 3 and 4). This suggests that the descending commands to these two digital components of FDS are functionally less well differentiated. In addition, motor units from these components of FDS may distribute tension to more than one digital component. Single motor units distribute force to adjacent fingers in the cat EDC muscle (Fritz et al. 1992) and the extensor digiti quarti et quinti in the macaque monkey (Schieber et al. 1997). Motor units containing sets of muscle fibres that act on more than one finger, and in particular for the little finger, may also exist within the FDP (Kilbreath et al. 2002). Lateral force transmission could also contribute to the distribution of force between the ring and little finger components of FDS via tissue interconnections as the ring finger component of FDS lies superficial to the little finger component. Wood Jones (1949) describes the little finger component of FDS as being connected variably by muscle fibres to the ring finger component and Ohtani (1979) describes connections between the intermediate tendon and the ring finger component.
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Our recordings were from the distal muscle bellies of FDS, and not from its proximal common muscle. It is possible that this proximal section of the muscle does not have as high a degree of volitional selectivity as the main index, middle and ring distal digital components, and its motor units distribute tension to more than one finger.
Comparison of recruitment thresholds for FDS when non-test fingers are flexing with data from a similar study for FDP suggests that these two extrinsic flexors of the fingers behave differently for the index, middle and ring finger but similarly for the little finger (Fig. 6). Using the same selection criteria for motor units, Kilbreath & Gandevia (1994) found that flexion at the distal IP joint of one finger in human subjects resulted in single motor unit activity in adjacent fingers at very low forces (commonly less than 5%). However, in the current study of FDS, and as shown in Fig. 5, flexion at the individual proximal IP joint up to 50% MVC did not usually recruit low-threshold single motor units for the index, middle and ring fingers. In contrast, flexion at the proximal IP joint of the ring finger at low forces produced single motor unit activity in little finger components for both FDP and FDS.
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Means and standard deviation for the thresholds of recruitment of the index, middle, ring and little finger units are shown. t tests revealed that FDS was recruited at higher forces than FDP for most combinations: * P < 0.01, + P < 0.05. The difference between the two finger flexors may be underestimated as a value of 60% MVC was arbitrarily used when FDS was not recruited (see Methods). The exception was recruitment of little finger units of FDS which behaved similarly to those of FDP.
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Previous EMG studies have found that FDS is recruited during active power grip (Long et al. 1970) and that FDP is the primary contributor to unloaded finger flexion (Long & Brown, 1962, 1964; Long, 1968; Kinoshita et al. 1995; Li, 2002). In the present study, the recruitment thresholds for FDS were lower when grasping a narrow compared with a wide cylinder. In addition, recruitment thresholds were lower for motor units acting on the radial compared with the ulnar side of the hand. Both results may reflect the length–tension relationships of the flexors, and the distribution of force between FDP and FDS. In a full grasp, fingers on the radial side of the hand exert more force when lifting as compared to those on the ulnar side of the hand (Kinoshita et al. 1995; Li, 2002).
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In conclusion, the index, middle and ring digital components of the FDS appear to be activated by volition in a more selective way than for FDP. Typically, large forces up to 50% MVC in an active finger recruited less than half the single motor units in another digital component of FDS not voluntarily flexing. In contrast, but similar to FDP, motor units in little finger components of FDS were activated by flexion of the adjacent ring finger at low forces. One explanation for the observed arrangement is that it may reduce the neural demands during grasping at high forces, with the object secured firmly on the ulnar side of the hand while it is positioned using the index finger and thumb. Additionally, it may assist grasps involving fewer than the four fingers.
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