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. 2002 Aug 15;543(Pt 1):289–296. doi: 10.1113/jphysiol.2002.023861

Distribution of the forces produced by motor unit activity in the human flexor digitorum profundus

S L Kilbreath *, R B Gorman *, J Raymond †, S C Gandevia †
PMCID: PMC2290486  PMID: 12181299

Abstract

In humans, the flexor digitorum profundus (FDP), which is a multi-tendoned muscle, produces forces that flex the four distal interphalangeal joints of the fingers. We determined whether the force associated with activity in a single motor unit in the FDP was confined to a single finger or distributed to more than one finger during a natural grasp. The discharge of single low-threshold motor units (n = 69) was recorded at sites across the muscle during weak voluntary grasping involving all fingers and spike-triggered averaging of the forces under each of the finger pads was used to assess the distribution pattern. Spike-triggered averaging revealed that time-locked changes in force occurred under the ‘test’ finger (that finger on which the unit principally acted) as well as under the ‘non-test’ fingers. However, for the index-, middle- and ring-finger units, the changes in force under non-test fingers were typically small (< 20 % of those under the test finger). For little-finger units, the mean changes in force under the adjacent ring finger were large (>50 % of those under the test finger). The distribution of forces by little-finger units differed significantly from that for each of the other three fingers. Apart from increases in force under non-test fingers, there was occasional unloading of adjacent fingers (22/267 combinations), usually affecting the index finger. The increases in force under the test finger correlated significantly with the background force for units acting on the middle, ring and little fingers. During a functional grasp, the activity of single units in the FDP allows for a relatively selective control of forces at the tips of the index, middle and ring fingers, but this is limited for little-finger units.

The human hand is a unique structure containing 27 bones and 20 intrinsic muscles with their origin and insertion within the hand itself. Eight muscles with their origin in the forearm also move the fingers, of which three, the flexor digitorum profundus (FDP), flexor digitorum superficialis and extensor digitorum communis, connect to each of the four fingers. Even though control of the digits in the human hand surpasses that of other primates (Napier, 1980), the types of movements that it can perform are limited (Santello et al. 1998).

One factor that could limit the independent control of the position and force of the fingers may be related to the force distribution from the multi-tendoned muscles. Each of the three ‘extrinsic’ muscles divides distally in the forearm to provide a single tendon to each finger. The degree to which these muscles produce force and movement at each of the fingertips would then depend upon the degree to which the muscles were subdivided into separate ‘anatomical compartments’ controlling each finger (English & Weeks, 1984) and the degree to which the motor units in these compartments could be accessed independently by the central nervous system.

The deep finger flexor, the FDP, is of special interest, not only because it is active in grasping (e.g. Long & Brown, 1962; Boivin et al. 1969; Close & Kidd, 1969; Kilbreath & Gandevia, 1993), but because it is the only flexor muscle that attaches to the distal phalanx (Wood-Jones, 1949) and is thus solely responsible for flexing the distal interphalangeal joint. The muscle has some anatomical compartmentalization, especially for the component involved in flexion of the index finger (e.g. Kilbreath & Gandevia, 1994), but there are limits to which the central nervous system recruits motor units involved in the motion of one finger during voluntary tasks, especially as the force increases (Kilbreath & Gandevia, 1994; Li et al. 1998a,b; Zatsiorsky et al. 2000). The present study was designed to examine the mechanical consequences of activation of motor units in the FDP during a natural grasp that involved all fingers. The discharge of single motor units was recorded during weak voluntary grasping and spike-triggered averaging (STA) of the forces under each of the finger pads was used to estimate whether the motor unit exerted force on one or more of the fingers. A preliminary report has been presented (Kilbreath et al. 1998).

Methods

Five female and two male volunteer subjects, aged 28–43 years, participated in the current study in which data were obtained from 69 motor units. Six subjects were studied on more than two occasions. Informed written consent to participate was given prior to the experiments. The procedures were approved by the local ethics committee and studies were conducted in accordance with the Declaration of Helsinki.

Experimental design

Intramuscular electrodes were inserted into the right FDP, at a level approximately halfway down the forearm. The FDP is organized topographically, with the index-finger portion located towards the radial side of the forearm, and the little-finger portion located on the ulnar side and posteriorly (Kilbreath & Gandevia, 1994). The electrodes were composed of two strands of Teflon-covered stainless-steel wire (75 μm diameter) threaded through a 23 or 25 gauge, short-bevelled needle (50 mm long), with up to 2 mm of insulation removed from the tips of the wires. Following placement, the needle was withdrawn, leaving the two wires ‘hooked’ in place within the muscle.

Only units that were active during attempted voluntary flexion of a single finger at very low forces (< 2 % maximum) were studied. This criterion has been used previously (Kilbreath & Gandevia, 1994). In brief, a subject flexed each finger in turn voluntarily at the distal interphalangeal joint against gravity. If the unit discharged consistently during repetitive flexion of one finger but did not discharge when the subject flexed the unloaded finger against gravity with each of the other fingers, the unit was included in the study. The finger with which the unit was recruited during fingertip flexion is referred to as the ‘test’ finger throughout the text. Using this procedure, more than 90 % of possible single motor units were classified as acting on a test finger.

The right hand of the subject was subsequently positioned to gently grasp an instrumented cylinder. To measure the forces under each finger, the fingertips of the subject were placed on flaps positioned over button load cells embedded in the cylinder (Fig. 1). The range of force measured by the load cells was 0–20 N. The cylinder was 100 mm high, 65 mm in diameter and weighed 200 g. The position of the load cells was designed to provide measurements for average-sized right hands. To determine the position of these load cells, 10 adults of varying hand size grasped the cylinder. Subjects positioned the pulp of the tip of their middle finger over the load cell for that finger and the position of contact for each of the other fingers was marked. The average position from these subjects was then used to position the remaining load cells.

Figure 1. Experimental set-up.

Figure 1

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Each of the fingers was positioned over small load cells embedded in the cylinder. Fine-wire EMG electrodes were used to record from single motor units.

Subjects were instructed to grasp the object as if to lift it and to apply sufficient force so that the unit fired slowly and steadily, at about 8–10 Hz. To assist them, subjects were provided with both visual and audio feedback relating to the firing of the unit. Nonetheless, subjects had occasional brief pauses in firing of the unit. The coefficient of variation of the interdischarge intervals over the prolonged recording period was approximately 20 % (Table 1). The EMG signal was amplified and filtered (bandpass 3–3000 Hz with a 50 Hz notch filter) and then directed to a dual time-amplitude window discriminator with delay so that the shape of a recruited motor unit could be identified and displayed on an oscilloscope (BAK DDIS-1, Germantown, MD, USA). Data were collected from each unit for between 3 and 60 min.

Table 1.

Firing rate of motor units in the flexor digitorum profundus during grasping and force under the test finger (mean ± s.d.)

Test finger No. of units Firing rate (Hz) Coefficient of variation (96) Background force under test finger (mN) STA* force forest finger (mN) Time to peak force (ms)
Index 13 9.1 ± 1.1 18.5 ± 4.0 952 ± 690 53 ± 53 63 ± 19
Middle 15 9.2 ± 1.2 20.6 ± 3.8 1330 ± 1174 47 ± 52 61 ± 18
Ring 27 10.0 ± 1.3 21.3 ± 5.4 453 ± 668 49 ± 57 59 ± 22
Little 14 9.6 ± 1.3 22.8 ± 4.9 427 ± 293 43 ± 35 73 ± 32
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*

STA force: force increment obtained by spike-triggered averaging.

A signal from the discriminator indicating the discharge of the test motor unit triggered an offset amplifier that was automatically reset every 1 s (Hales & Gandevia, 1988). This meant that small changes in force could be further amplified (× 10), regardless of the background force. The amplified forces for each finger and an event marker for the unit discharge were sampled at 1000 Hz on a computer via a CED 1401 Plus interface using Spike 2 software (Cambridge Electronics Design, Cambridge, UK). Other signals that were recorded included the raw EMG (sampling rate: 7000 Hz) and the absolute force under each finger (sampling rate: 1000 Hz). During data collection, EMG trigger pulses and the preliminary STA of the force for each finger were displayed and, at the conclusion of a recording, the interspike interval histogram was viewed. Figure 2 shows the final data from a single subject for four motor units: the STA forces under each finger, the interspike interval histograms of the units and their EMG potentials.

Figure 2. Data from a single subject.

Figure 2

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Each column of data represents data from a single unit. The spike-triggered average (STA) change in force under each finger from that unit is displayed as well as the interspike interval histogram and the shape of the unit potential. Change in force under the test finger was consistently greater than under the non-test fingers. However, both the ring -finger and little-finger units also produced relatively large forces under the adjacent finger (I.E. the little and ring fingers, respectively).

Data processing and analysis

Data were formally reanalysed after the studies to identify a number of variables. For each single-unit recording, the usual forces with which a subject grasped the cylinder were ascertained (i.e. ‘background forces'). For each STA, we identified the mean and standard deviation of the baseline force for 20 ms prior to the discharge of the unit, the change from baseline to the peak force in the 150 ms after the trigger, and the latency of this change in force. As with the background force, these variables were measured for the ‘test’ and ‘non-test’ fingers. We also checked the firing statistics for each unit (mean interspike interval and the coefficient of variation). The mean number of spikes for each STA was approximately 5500.

Data were pooled for each of the four test fingers. Comparison of the effect that units had on a test finger and non-test fingers were analysed using two-way analyses of variance (ANOVA). The effects that were compared from the STAs included the average amplitude of the peak force, the average size of the peak force relative to the total force, and the latency at which the peak force occurred. As identical results were obtained when the data were analysed as absolute or relative forces on the various digits, probabilities are given in the text for analysis of absolute forces. In addition, the background forces among the test fingers during the grasp were similarly compared.

When significant differences were identified among the groups of units, Duncan's post-hoc analysis was used, and when significant differences were identified among test and non-test fingers, planned contrasts were examined. To determine whether the absolute change in force in the STA was significant, we required the peak to be greater than two standard deviations from the baseline force. Chi-squared (χ2) tests were used to examine the relative distribution of force under digits adjacent to the test finger. To examine the relationship between the background force and the changes in force, Pearson product correlations were used. Significance was set at P < 0.05. Statistical analyses were performed using SPSS (Chicago, IL, USA).

Results

Data were collected from 69 low-threshold motor units in the FDP. The units were grouped for analysis according to the finger on which they acted preferentially during voluntary contractions. There were 13 index-finger units, 15 middle-finger units, 27 ring-finger units, and 14 little-finger units. The firing rates of the units during testing and the coefficient of variation related to their firing did not differ across the different portions of the FDP (Table 1).

The background force generated under the fingers on the lifting cylinder varied among the fingers (Table 1). When pooled across all recordings, the mean background force under the fingers was 715 mN for the index finger, 710 mN for the middle finger, 1277 mN for the ring finger and 346 mN for the little finger. These values represented background forces of approximately 1–2 % of maximal voluntary force (Kilbreath & Gandevia, 1996).

STA revealed that time-locked changes in force occurred under the test finger (Table 1) as well as under non-test fingers (Fig. 2 and Fig. 3). The change in force was typically greatest for the finger on which the unit principally acted (i.e. the test finger; 64/69 units). In all instances, the spike-triggered force under the test finger increased in response to the firing of the unit (Table 1) and, for 68/69 units, this increase was significant (i.e. > 2 s.d. of the force before unit discharge, see Methods).

Figure 3. Summary of change in force under the digit for the population of 69 single motor units in flexor digitorum profundus.

Figure 3

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Group data (mean ± s.e.m.) are displayed. The change in force under the non-test finger was significantly different from that under the test finger for all digits except the little-finger units: the horizontal line indicates the lack of significant difference between force changes under the little and ring fingers for little-finger units. The change in force under the non-test units was typically small, with the exception of that under the ring finger for little-finger units

To ascertain whether the four groups of units produced similar patterns of force distribution, we pooled the data and performed a two-way ANOVA with the two dependent variables, ‘motor unit’ classification (i.e. index-, middle-, ring- or little-finger unit) and the finger upon which the forces were exerted. The independent variable was the change in force. There was a significant interaction between the groups of units and the fingers on which the units acted (P < 0.001), indicating that the pattern of changes in force was not the same for each group of units. Therefore, we then explored each group of units separately, using one-way repeated-measures ANOVAs.

For each group of units (index-, middle-, ring- and little-finger units), the STA force distribution among the fingers was not uniform (Fig. 3; repeated-measures ANOVA, index: P = 0.02; middle, P = 0.01; ring, P = 0.001; little, P = 0.001). Post-hoc analysis revealed that index-, middle- and ring-finger units produced significantly greater changes in force under the test finger than under all non-test fingers. For the index-, middle- and ring-finger units, the changes in force under their non-test fingers were not significantly different (i.e. the small forces occurring under non-test fingers were of similar magnitude, but less than under the test finger). In contrast, the force produced by little-finger units under the ring finger was significantly greater than that under the index and middle fingers.

In Fig. 4, the change in force under the test finger is plotted against that under the adjacent (non-test) finger(s). As expected from the main statistical analysis, for index-, middle- and ring-finger units, there were relatively small changes in force under the adjacent fingers compared with the change under the test finger. For these fingers, the averaged STA force under the adjacent finger, expressed as percentage of that under the test finger, ranged from −5 % (STA force under index finger for middle finger units) to +17 % (STA force under middle finger for index-finger units). In contrast, for many little-finger units, there were significant increases in force under the ring finger, such that the average change in force under the ring finger was approximately 62 % of that under the little finger. Comparison of little-finger units and the units of the other fingers that produced forces greater than 25 mN on an adjacent finger also showed that little-finger units produced a greater STA force under its adjacent finger. While 8 (of 14) little-finger units pulled greater than 25 mN on the ring finger, only 1 (of 13) index-finger units, 4 (of 15) middle-finger units and 3 (of 27) ring-finger units pulled greater than 25 mN on the adjacent finger (χ2 = 21.6, P < 0.001).

Figure 4. Relationship between the changes in force of the test finger with that under the adjacent finger(s).

Figure 4

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Data for forces on the adjacent finger medial to the test one are shown as open circles and those on the lateral finger are shown as filled circles. A, data from all units. One unit with large unloading of the adjacent fingers is indicated in parenthesis. B, the x-axis has been expanded to display data from the low-force units. The horizontal reference line is arbitrarily set at 25 mN.

We examined the direction of changes in force evoked by the test motor units. While they pulled on or ‘loaded’ the test finger (in 245 of 267 combinations; see Fig. 4), sometimes there were significant reductions in force or ‘unloading’ under the non-test fingers (in 22 of 267 combinations). The mean magnitude of the unloading was 13.5 mN, whereas the mean force increase under test fingers was 82.8 mN. As it was not common for unloading to occur, it was difficult to discern a pattern in its distribution. However, a total of nine middle-, ring- and little-finger units were associated with a reduction in force under the index finger. An example is shown in Fig. 5.

Figure 5. Data from a single subject for a middle-finger unit that produced unloading under the index finger.

Figure 5

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STAs shown for the action of this unit under the index, middle and ring fingers. Averages have been superimposed for data from the first and second half of the recording (929 and 924 triggers, respectively). The dotted line indicates the timing of the unit discharge. Superimpositions below show the shape of the motor unit potential.

Separate analysis of the latencies from each group of units revealed that the change in peak force occurred at a similar time under each test finger for index-, middle- and ring-finger units (Table 1). The latency for little-finger units was slightly longer, but this was not significant (P = 0.40). For the population of units, the latency to peak force under the test finger was significantly correlated with the latency under the non-test fingers (P < 0.01). The latency to peak force was not different between the test and non-test fingers.

Finally, the relationship between the change in force under the finger on which the unit acted and the absolute background force applied by the same finger to the cylinder was examined (Fig. 6). The size of the increase in STA force was positively correlated with the absolute force applied for the middle-, ring- and little-finger units (P < 0.05), but not for the index-finger units. Thus, the units active when small forces were generated at the fingertip were associated with small force increments, but when the background force was higher the active units generated larger force increments.

Figure 6. Relationship between the change in force under the test finger and the background force for that finger.

Figure 6

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Except for index-finger units, the changes in force under the test finger correlated significantly with the background forces exerted by that finger.

Discussion

Humans have remarkable manual dexterity, with selective control of the operation of individual digits, but there are some limits to performance. Regardless of whether the measured output is isolated recruitment of single motor units (Kilbreath & Gandevia, 1994), high voluntary muscle forces (Zatsiorsky et al. 1998), or somewhere between these two extremes (Kilbreath & Gandevia, 1994; Hager-Ross & Schieber, 2000), tension is generated by the non-test fingers. The underlying mechanisms are both central and peripheral in origin, and include both neural limits to motor unit recruitment and mechanical limits imposed by motor unit anatomy and digital tendon interconnections. The present study provides new information about these mechanisms in humans when the hand is engaged in a functional task involving all fingers (i.e. a grasp). Such information is needed to understand how the central nervous system must organize motor commands to motoneurones innervating finger flexors.

Voluntary activation of motor units in the FDP associated primarily with the index, middle and ring fingers produced force changes predominantly under the ‘test’ finger, with the force changes under the non-test fingers usually being much smaller than those under the test fingers. Thus, these motor units could be driven voluntarily to produce relatively selective forces under the fingertips. Little-finger units appeared to behave differently: they produced relatively large force increases under the ring finger. The majority of little-finger units produced STA forces that were greater than 25 mN under the adjacent ring finger, while fewer than 15 % of units for the other fingers produced such a large change under adjacent fingers.

One explanation for the change in force observed under the non-test finger is the distribution of tension from a single-motor unit due to the spatial distribution of its muscle fibres. In the extensor digiti quarti et quinti in the macaque monkey (Schieber et al. 1997), and extensor digitorum communis in the cat, Fritz et al. 1992), single-motor units can distribute force to adjacent digits. In the human FDP, the tension produced by little-finger units was relatively unselective between the ring and little fingers. The STA force produced by the little-finger units under the ring finger was 62 % of that produced under the little finger.

A second and related mechanism for force distribution for single-motor units is lateral force transmission through shearing of the interfaces between muscle fibres (Huijing, 1999; Monti et al. 1999) or other connective tissue links (Kawakami & Lieber, 2000; Maas et al. 2001). There were small but significant changes in force under the middle, ring and little finger with activation of the index-finger units. The mean change under the index finger was 53 ± 53 mN compared with 7 ± 9 mN under the adjacent middle finger. If this occurs, the present data indicate an upper limit to this mechanism of transmission. This mechanism may not be the full explanation because for the index-, middle- and ring-finger units, the ‘transmission’ to adjacent and more remote fingers was equal in size, rather than being focused around the test finger.

Another mechanism that might contribute to the change in force under non-test fingers is the interconnections between the tendons. There are interconnections between tendons of the FDP (Verdan, 1960; Rank et al. 1968; Fahrer, 1971; Malerich et al. 1987; Leijnse, 1997), and between the tendons of the index portion of the FDP and flexor pollicis longus (Linburg & Comstock, 1979). These connections occur within the palm (Fahrer, 1981) or at the carpal tunnel (Leijnse et al. 1997).

An additional explanation for the observed distribution of forces from single motor units within the FDP is that there is a degree of short-term neural synchronization among motor units acting on individual fingers (e.g. Kirkwood & Sears, 1978; Kirkwood, 1979; Nordstrom et al. 1992; Farmer et al. 1997; Stephens et al. 1999). This has not been formally investigated for the FDP, and while this mechanism may contribute, it is unlikely to be the full explanation for the observed results. As the whole hand grasped the cylinder, and thus all parts of FDP were activated (Table 1), it would be expected that any effect due to synchronization be equally partitioned across the muscle, according to the sharing principle described by (Stephens et al. 1999). However, in our study the pattern of force distribution was unequal and asymmetrical: little-finger units produced, on average over half their ‘test’ force under the ring finger, while index-, middle- and ring-finger units typically produced much smaller forces under adjacent fingers. Synchronization of ring- with little-finger units is unlikely to be sufficient to explain this size of force under the ring finger (e.g. Nordstrom et al. 1992). In addition, ring-finger units behaved similarly to middle- and index-finger units, and they did not pull strongly on the adjacent little finger. This would have been expected if synchronization between ring- and little-finger units explained the observations. Further evidence against synchronization as the full explanation is that during the grasp, some units unloaded, rather than loaded, adjacent fingers. Given the uniform nature of the task performed by all fingers, this unloading is likely to be a mechanical consequence of elements ‘in parallel’ (e.g. as with unloading of muscle spindle endings).

Notwithstanding the above, it must be conceded that a degree of synchronization probably occurred in the grasping task. It is clear from modelling (Fuglevand, 2001) and microstimulation studies (Keen & Fuglevand, 2001) that the forces obtained with STA overestimate twitch forces. They observed the distribution of force from single units innervating the extensor digitorum communis with STA during contractions but not with microstimulation of the otherwise relaxed muscle. This may reflect a loss of synchronization or a difference in the biomechanics of the muscle between rest and contraction. Unfortunately, it is problematic to apply intraneural microstimulation to motor axons of the FDP during grasping.

Forces produced by single motor units correlated positively with the background voluntary force for middle-, ring- and little-finger units. The positive correlation is indicative of Henneman's size principle, based on work on animals and, more latterly, humans, in which motoneuronal properties were linked to the force-generating properties of their muscle fibres (Henneman & Mendell, 1981). The lack of correlation for index-finger units may reflect the narrower range of forces generated by these units. Interestingly, the relationship was detected in our study when the force increments were plotted against background force for 8–10 Hz firing of the motor unit, rather than against a threshold force for minimal firing. A similar tendency to recruit units generating larger forces as background voluntary force increases has been noted in humans for the extensor digitorum communis, first dorsal interosseous and masseter muscles (Milner-Brown et al. 1973; Freund et al. 1975; Monster & Chan, 1977; Desmedt & Godaux, 1979).

In conclusion, activation of single-motor units in the human FDP produces complex patterns of force change at the fingertips. The forces are well ‘translated’ from the level of the motor unit to the tip of the finger for the parts of the FDP innervating the index, middle and ring fingers. For motor units innervating the little finger, there is some spread of force from the little finger to the adjacent ring finger. Nonetheless, compared with the macaque monkey (Schieber et al. 2001), the overall evolutionary development would allow more selective movement of the tips of the fingers in humans.

Acknowledgments

This work was supported by funding from the University of Sydney and the National Health and Medical Research Council (item 3206). We thank Dr Robert Herbert for comments on the manuscript.

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