Coupling between mechanical and neural ... - Wiley Online Library

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J Physiol 587.4 (2009) pp 917–926

Coupling between mechanical and neural behaviour in the human first dorsal interosseous muscle Anna L. Hudson, Janet L. Taylor, Simon C. Gandevia and Jane E. Butler Prince of Wales Medical Research Institute and the University of New South Wales, Sydney 2031, Australia

The neural drive to a muscle and its biomechanical properties determine the force at a joint. These factors may be centrally linked. We studied the relationship between the ability of first dorsal interosseous muscle (FDI) to generate index flexion force around the metacarpophalangeal joint and the neural drive it receives in a voluntary contraction. The role of FDI was assessed in two thumb postures, thumb ‘down’ (thumb abducted) and thumb ‘up’ (thumb extended), and at different thumb carpometacarpal angles. These postures were designed to change acutely the flexion moment arm for FDI. The flexion twitch force evoked by supramaximal stimulation of the ulnar nerve was measured in the two postures and the change in moment arm was assessed by ultrasonography. Subjects also made voluntary flexion contractions of the index finger of ∼5 N in both postures during which neural drive to FDI and the long finger flexor muscles was measured using surface EMG. Recordings of FDI EMG were normalized to the maximal M wave. Five of the 15 subjects also had a radial nerve block to eliminate any co-contraction of the extensor muscles, and extensor muscle EMG was monitored in subjects without radial nerve block. Compared to thumb up, flexion twitch force was ∼60% greater, and the flexion moment arm was ∼50% greater with the thumb down. There was minimal effect of altered carpometacarpal angle on flexion twitch force for either thumb posture. During voluntary flexion contractions, normalized FDI EMG was ∼28% greater with thumb down, compared to thumb up, with no consistent change in neural drive to the long flexors. Hence, the contribution of FDI to index finger flexion can be altered by changes in thumb position. This is linked to changes in neural drive to FDI such that neural drive increases when the mechanical contribution increases, and provides a central mechanism to produce efficient voluntary movements. (Received 15 October 2008; accepted after revision 23 December 2008; first published online 5 January 2009) Corresponding author S. Gandevia: Prince of Wales Medical Research Institute, Barker St Randwick, NSW 2031 Australia. Email: [email protected]

The amount of force that a muscle can produce depends on several key biomechanical factors such as its length–tension relation, the muscle’s physiological cross-sectional area and specific tension, the pennation angle of the muscle fibres, and the moment arm of the muscle–tendon unit (Gordon et al. 1966; Otten, 1988; Zajac, 1992; Maganaris, 2001, 2004). In addition, the degree of voluntary activation, i.e. neural drive to the muscle, influences force generation (e.g. Adrian & Bronk, 1929). The amount of force a muscle can produce (due to the biomechanical factors listed above), and the neural drive it receives in a voluntary contraction, may be coupled. In the human intercostal muscles, inspiratory neural drive is related to the specific mechanical advantage of the different regions of the muscle (De Troyer et al. 2003; Gandevia et al. 2006; for review see De Troyer et al. 2005). We have studied, in first dorsal interosseous (FDI), the relationship between the amount of force that the muscle C 2009 The Authors. Journal compilation C 2009 The Physiological Society

can generate, and how the muscle is ‘driven’ in a voluntary contraction. FDI is a bipennate muscle with two distinct heads (Masquelet et al. 1986; Fig. 1A). The deep muscle head originates on the lateral, palmar surface of the second metacarpal, and the superficial head, which is ∼70% larger in volume than the deep head (Chao et al. 1989), originates on the medial aspect of the first metacarpal. The fibres from the superficial head twist as they approach the metacarpophalangeal (MCP) joint such that those with a more distal origin insert more dorsally. Fibres from the two muscle heads converge to form a tendinous sheet that inserts on the lateral tubercle on the base of the proximal phalanx of the index finger, and it also blends into the interosseous hood (or extensor aponeurosis; Jones, 1949; Masquelet et al. 1986). As a result of its intricate anatomy, FDI has both a flexion and abduction moment arm at the MCP joint DOI: 10.1113/jphysiol.2008.165043

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(An et al. 1983). At 0 deg of flexion of the index finger, the moment arm for flexion forces is ∼4 mm for the superficial head of FDI, and 0 mm for the deep head (An et al. 1983). The deep head has a peak flexion moment arm of ∼5 mm at ∼45 deg of index finger flexion. In this study (An et al. 1983), tendon excursion was measured in the index finger taken from amputated limbs and the effect of movement of the thumb was not studied. When considering the action of the superficial head, isolation of the index finger presents a difficulty as FDI originates on the first metacarpal of the thumb. A change in thumb posture should alter the biomechanics of the superficial head of FDI for finger flexion, but there are no reports of the effect of thumb posture on the flexion moment arm of FDI. Studies of human skeletal muscles have suggested that some motor units or muscles are recruited with regard to their direction of pull or contribution to force (e.g. Desmedt & Godaux, 1981; ter Haar Romeny et al. 1982; McMillan & Hannam, 1992; Kennedy & Cresswell,

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2001). However, they have not specifically linked changes in motor unit recruitment to known changes in the contribution of a muscle at a joint, i.e. its ‘mechanical advantage’ or ‘mechanical effectiveness’. We studied the contribution of FDI to flexion forces at the index finger, and the neural drive to this muscle during voluntary flexion contractions, in two thumb postures that were designed to change the flexion moment arm of the superficial head of the muscle originating on the thumb. We hypothesized that the contribution of FDI for flexion forces at the MCP joint, i.e. the flexion moment arm of FDI, could be increased by a change in thumb posture, and that this change in muscle-tendon mechanics would lead to increased neural drive to FDI during a voluntary contraction. If this occurred, it would indicate that the central nervous system takes into account the mechanical effectiveness of a muscle when executing a voluntary task. Our hypothesis is in contrast to what would be expected if the joint were controlled by a single muscle. There, an increase in mechanical effectiveness of the muscle would decrease the neural drive required to produce the same force. Methods The contribution of FDI to index finger flexion force at the MCP joint in two thumb postures (‘thumb down’ and ‘thumb up’, see below for details) was assessed by measuring flexion twitch force at different thumb carpometacarpal joint angles over the physiological range. To determine the mechanism underlying the contribution of FDI to flexion forces, the flexion moment arm of FDI was assessed by ultrasonography. In a second experiment, electromyographic (EMG) recordings from FDI and the long flexors of the index finger were made during voluntary flexion contractions of the index finger in the two thumb postures. A total of 15 healthy adult volunteers participated (32 ± 10 years of age, mean ± S.D., seven females). The procedures were approved by the local ethics committee and conformed with the Declaration of Helsinki, and all subjects gave their informed written consent prior to participation.

Figure 1. First dorsal interosseous and thumb posture A, diagram of the two muscle heads of first dorsal interosseous (FDI). The muscle originates on the first and second metacarpal bones. Its fibres converge, and insert on the lateral aspect of the proximal phalanx, distal to the metacarpophalangeal (MCP) joint. A carpometacarpal angle of ∼38 deg is shown. The dashed box over the MCP joint indicates the location of the ultrasound transducer (see Fig. 3). B, schematic drawing to show the thumb postures in which flexion twitch force was evoked, the flexion moment arm of FDI was measured, and subjects made voluntary contractions (see Methods). Left, thumb down; right, thumb up.

Study 1: effect of thumb posture on flexion twitch force and flexion moment arm of FDI

Subjects were seated with their right arm resting on a table on the ulnar side of the forearm with the wrist held straight. They were instructed to relax at the wrist, elbow and shoulder. The arm was held firmly in this position, in particular, at the metacarpals and wrist. The index finger was splinted but movement around the MCP joint was not constrained. To measure isometric force in the flexion direction, a ring around the splinted index finger, C 2009 The Authors. Journal compilation C 2009 The Physiological Society

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Mechanical and neural behaviour in first dorsal interosseous muscle

just proximal to the proximal interphalangeal (PIP) joint was attached to a load cell (Xtran, Melbourne, Australia) via a rigid rod. The arm and finger remained in this set-up throughout the study, but the thumb was placed at different angles (relative to the index finger) in two thumb postures (Fig. 1B). In one posture, ‘thumb down’, the thumb was abducted at an angle, so that it was parallel to the table (Fig. 1B, left panel). In the other posture, the thumb was extended, and in the same vertical plane as the wrist and index finger, and this is referred to as ‘thumb up’ (Fig. 1B, right panel). In each posture (i.e. thumb down or up), a range of carpometacarpal joint angles was tested to look for the effect of changes in FDI muscle length. For thumb down, we measured twitch force as close as possible to full adduction (i.e. ∼0 deg abduction) and then at 7.5 deg increments to full abduction, while the thumb remained parallel to the table. For thumb up, we measured twitch force at 7.5 deg increments from as close as possible to full flexion, to full extension, while the thumb remained in the vertical plane. For each subject, at least five, and up to nine different angles were measured depending on the passive range of movement at the carpometacarpal joint. The maximal M wave (M max , see below) was determined at the longest muscle length, i.e. full abduction for thumb down, or full extension for thumb up, and the twitch force was determined for the longest muscle length first, and then for progressively shorter lengths. The thumb was taped firmly to a support at all angles, and the order in which the postures were tested was random. To determine maximal twitch force in the flexion direction, electrical stimuli were delivered via surface electrodes over the ulnar nerve, usually a few centimetres proximal to the wrist. The cathode was on the palmar side of the wrist, and the anode on the dorsal side. EMG was recorded from FDI with surface electrodes (see Study 2 for details). The stimulus intensity (66–209 mA, 100 μs duration, DS7AH constant-current stimulator; Digitimer, Welwyn Garden City, UK) was at least 10% above that required to produce M max in FDI. At each thumb posture and angle, supramaximal stimuli were delivered 5–10 s apart (5 in total). In a separate session, in six subjects, an ultrasound unit (Phillips iU22, Bothell, WA, USA) was used to determine the effect of thumb posture on the position of the FDI tendon relative to the MCP joint. The moment arm of a muscle is the perpendicular distance between the muscle-tendon unit and centre of joint rotation (e.g. Smidt, 1973; Rugg et al. 1990). Here, the distance between the FDI tendon and the lateral tubercle on the second metacarpal head was used to estimate changes in the flexion moment arm of FDI. For the ultrasound study, subjects were seated with their right hand resting on the ulnar side of the forearm and the wrist and index finger were held straight. The thumb C 2009 The Authors. Journal compilation C 2009 The Physiological Society

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was positioned in a thumb down posture at ∼38 deg of carpometacarpal flexion. Surface electrodes were placed over FDI to monitor FDI EMG. Axial images were obtained with a 32 mm 15–7 MHz linear transducer placed transversally on, or just proximal (by no more than ∼5 mm) to the axis of rotation for flexion of the index finger at the MCP joint. The possible error in placement (< 5 mm from the axis of rotation) is similar to that in studies of moment arm in vivo that simply estimate the joint centre location using anatomical landmarks (Fowler et al. 2001). The transducer was adjusted so that optimal images of the FDI tendon and the lateral edge of the head of the second metacarpal could be visualized. Once the images were optimal, the transducer was manually stabilized while the thumb was moved passively from a thumb down, to a thumb up posture. The carpometacarpal angle was maintained between thumb postures. Subjects were instructed to relax during the study and had visual feedback of FDI EMG. Repeated sequences (5 s duration) were captured before, during and after thumb movement. The images were displayed in real time and digitally sampled at 30 Hz for analysis.

Study 2: effect of thumb posture on FDI EMG activity in a voluntary contraction

The set-up was similar to Study 1, but to measure flexion force, the ring at the PIP joint was attached to the load cell via a wire. Subjects received visual feedback of force throughout the experiment and made voluntary isometric flexion contractions of the index finger at the MCP joint to 5 N (∼5–10% maximal voluntary contraction). Contractions were made with the thumb in the two postures, thumb down and thumb up (as above), at a carpometacarpal angle of ∼38 deg. Care was taken to ensure the angle was the same in both postures. Contractions were repeated 20 times in each thumb posture, with at least 10 s between contractions. M max in FDI was also determined at each thumb posture. The order in which the postures were tested was random. EMG was recorded from FDI, the long flexors of the index finger (flexor digitorum superficialis and profundus), and the extensor muscles (extensor digitorum communis and indicis), via adhesive surface electrodes (Ag–AgCl; 10 mm diameter; Cleartrace, ConMed Corporation, Utica, NY, USA) placed ∼5 cm apart. For FDI, one electrode was placed on the proximal part of the muscle close to the second metacarpal (to minimize movement artefact with changes in thumb posture) and the other electrode was ∼5 cm distally, over the MCP joint. For the long finger flexors and extensors, electrode placement on the volar and dorsal surface of the forearm was approximately two-thirds of the distance between the styloid, and the medial or lateral epicondyle,

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respectively. The sites were confirmed by palpation of the relevant muscles. The electrodes on the forearm are likely to record activity in other finger and wrist flexor and extensor muscles activated inadvertently. As in Study 1, supramaximal stimuli (110% M max , 55–200 mA) were delivered at the ulnar nerve to determine M max in FDI. To measure the activity in FDI and the long finger flexors during flexion contractions at the MCP joint, without co-contraction of the extensor muscles, 5 of the 15 subjects had a radial nerve block at the mid-humerus level which paralysed the wrist extensors and long extensors of the thumb and fingers. This was produced by injection of local anaesthetic (2% lignocaine with adrenaline, 2–3 mg kg−1 , and 0.5% bupivacaine with adrenaline, 1–1.5 mg kg−1 ), around the radial nerve at the mid-humerus level. Injections were guided by stimulation via the injecting needle (Stimuplex A 22-G, B. Braun, Melsungen, Germany). The nerve block was complete as judged by paralysis of radial innervated muscles, loss of response to radial nerve stimulation, and loss of sensation in the territory of the superficial radial nerve. In subjects with radial nerve block, EMG was not measured from the extensor muscles. For Studies 1 and 2, the EMG signals were amplified, filtered (16–1000 Hz), and sampled at 2000 Hz for off-line analysis using customised software (Grass amplifier, Warwick, RI, USA; CED 1902 amplifiers, CED 1401 with Signal and Spike2 software, Cambridge Electronic Design, Cambridge, UK). Force was sampled at 1000 Hz.

Analysis

Mean maximal flexion twitch force was calculated from the peak amplitudes of five twitches evoked by ulnar nerve stimulation (e.g. Fig. 2A). For thumb down and thumb up postures, the average twitch force was calculated for six angles, or ∼38 deg range of thumb abduction or extension (more angles were tested in some subjects, but were not included in the analysis). A missing value for one subject with the thumb up at ∼38 deg was replaced with the group mean for analysis (Tabachnick & Fidell, 1989). Absolute values are reported in the text, but data were normalized to the average twitch force at full adduction in the thumb down posture in Fig. 4. The ultrasound images were viewed off-line (Sante DICOM Viewer). We tracked the position of the FDI tendon and the lateral tubercle of the second metacarpal head. The FDI tendon was visualized for several cycles of movement between thumb postures, but for one cycle, the first (thumb down) and last (thumb up) frames were selected for analysis (Fig. 3A and B). There was little or no FDI EMG (< 0.5% of EMG in a maximal effort) during the ultrasound recordings (e.g. Fig. 3C). For each image, the perpendicular distance between the centroid of the FDI

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tendon, and a reference point on the lateral tubercle of the metacarpal was measured using in-built software callipers. The reference point was clearly identified throughout the ultrasound recordings. In Study 2, subjects without radial nerve block had some EMG activity in finger extensors during the flexion contractions (e.g. Fig. 2C). Therefore, of the 20 contractions recorded, those with matched extensor activity in each thumb posture were selected and analysed. Five to ten contractions were analysed for each subject and thumb posture. For subjects with a radial nerve block, 10 contractions were analysed. Flexion force and EMG levels (root mean square (r.m.s.); time constant, 0.05 s) were measured over ∼3 s of each contraction at the target force (Fig. 2C). Baseline force, and r.m.s. EMG during complete relaxation were measured (to estimate background noise) and subtracted from values during the test contractions. To correct for changes in EMG amplitude associated with positional changes of the thumb, mean FDI r.m.s. EMG was normalized to the (average) r.m.s. of the M max potentials for each subject and thumb posture (Fig. 2B). EMG data are reported as absolute values in the text, but are illustrated in Fig. 5 normalized to thumb down for each subject. Statistics

Group data from the 15 subjects are presented as means ± S.D. in the text and means ± S.E.M. are shown in the figures. In Study 1, comparison between the twitch force at different angles of carpometacarpal abduction or extension, and between thumb down and thumb up were made by a two-way repeated-measures analysis of variance (ANOVA), with angle and thumb posture as factors, and post hoc testing using Tukey’s procedure. For the ultrasound study, and in Study 2, Student’s paired t test was performed to assess differences in all parameters between thumb down and thumb up, and unpaired t tests were performed to compare between subjects with, and without a radial nerve block. Statistical significance was set at P < 0.05. Results Study 1

To determine the effect of thumb posture and thumb (carpometacarpal) angle on the contribution of FDI to index finger flexion at the MCP joint, angle–twitch force curves were determined for the thumb up and thumb down (Fig. 4). With the thumb up, flexion twitch force evoked by supramaximal stimulation of the ulnar nerve was similar at all six carpometacarpal angles (over a range of ∼38 deg; P > 0.05). It was 1.2 ± 0.7 N (mean ± S.D.) at the largest angle analysed (∼38 deg extension), and C 2009 The Authors. Journal compilation C 2009 The Physiological Society


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1.4 ± 0.8 N at the smallest angle with the joint close to full flexion. With the thumb down, there was an effect of carpometacarpal angle on flexion twitch force at the smallest angle only. Flexion twitch force was 2.3 ± 1.0 N at the largest angle (∼38 deg abduction), and similar at other angles, except the smallest angle (close to full adduction). Here, the average twitch force was 1.9 ± 0.7 N (P < 0.001). Compared to thumb up, twitch force was ∼60% greater with the thumb down at all joint angles tested (Fig. 4; P < 0.001). Using ultrasonography, the tendon of FDI was visualized on the palmar side of the second metacarpal

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(Fig. 3). The perpendicular distance between the centroid of the FDI tendon and the lateral tubercle of the second metacarpal head was 9.1 ± 2.4 mm with thumb down, and 6.5 ± 2.5 mm when the thumb was moved passively to the thumb up posture (P < 0.001). The tendon moved, on average, 2.6 mm (range 1.9–3.4 mm in 6 subjects). Study 2

Subjects made flexion contractions of the index finger at the MCP joint to a target force of 5 N with the thumb supported in extension in the ‘thumb up’ posture, or

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Figure 2. Data from a single subject for flexion twitch force and voluntary contractions A, flexion twitch force was evoked by supramaximal stimulation of the ulnar nerve in the two thumb postures, and at different carpometacarpal angles. Five twitches (grey traces) and the average (black traces) are superimposed for the thumb down, and thumb up postures at a carpometacarpal angle of ∼38 deg. B, M max in FDI was determined in the two thumb postures. Shaded regions indicate the area used to determine the root mean square (r.m.s.) of M max potentials. FDI EMG was normalized to r.m.s. amplitude at each thumb posture. Arrows indicate time of stimulation. C, typical recordings from an intact subject during voluntary flexion contractions at the index MCP joint of ∼5 N with the thumb down (left panel) and up (right panel). From top to bottom, panels show finger flexion force, and surface EMG recordings from first dorsal interosseous (FDI), the long finger flexors, and long finger extensors. The voluntary isometric contractions lasted ∼5 s. Force and r.m.s. EMG were measured over ∼3 s (between vertical lines). Vertical calibrations: 250 μV for FDI and 10 μV for long flexors and extensors. C 2009 The Authors. Journal compilation C 2009 The Physiological Society

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Figure 3. Data from a single subject for analysis of the flexion moment arm in FDI Ultrasound images of the FDI tendon and distal head of the second metacarpal captured with the thumb down (panel A) and thumb up (panel B). The perpendicular distance between the centroid of the tendon (shown with cross) and reference point on the metacarpal (shown with arrow) was measured to estimate the flexion moment arm. Ultrasound images were taken in passive conditions as confirmed by a lack of FDI EMG during the ultrasound capture (panel C). The time at which frames were selected for analysis are indicated by the arrows (A: thumb down; B: thumb up). Vertical calibration: 100 μV.

in abduction with the ‘thumb down’. For the 15 subjects, the targeted voluntary force produced with the thumb up (5.1 ± 0.2 N) did not differ from thumb down contractions (5.2 ± 0.2 N; P > 0.05). For subjects without a radial nerve block (n = 10), finger extensor r.m.s. EMG did not differ between contractions in the two thumb postures (2.8 ± 1.9 μV for both; P > 0.05).

Figure 4. Angle–twitch force relationships for flexion of the index finger evoked by stimulation of the ulnar nerve in the two thumb postures Flexion twitch force for the index finger was measured over a ∼38 deg range from near full adduction to ∼38 deg of abduction with the thumb down (◦), and over a ∼38 deg range from near full flexion to ∼38 deg of extension with the thumb up (•). Twitch force was normalized to that at near full adduction with the thumb down for each subject (n = 15). There was minimal change in mean (± S.E.M.) flexion twitch force with altered carpometacarpal angle within a thumb posture, but twitch force was always 30–60% greater when the thumb was down, compared to the thumb up.

The size of M max was similar in the two thumb postures (e.g. Fig. 2B). For the group, M max amplitude was 19.4 ± 4.2 mV and 20.5 ± 4.3 mV for the thumb up and thumb down, respectively, and the r.m.s. of M max was also similar for thumb up and thumb down (5.1 ± 1.2 and 5.2 ± 1.2 mV, respectively; P > 0.05). To control for any artefactual change in EMG with altered thumb posture, FDI r.m.s. EMG was normalized to the r.m.s. of M max at each thumb posture. During the voluntary flexion contractions of similar absolute force (and similar level of extensor EMG, see above), EMG from FDI and the long finger flexors was measured. FDI activity was 28% greater during voluntary contractions with the thumb down (Fig. 5). The ratio of FDI r.m.s. EMG to the r.m.s. of M max was 0.011 ± 0.006 with the thumb up, and 0.014 ± 0.006 with the thumb down (P < 0.01). Changes in long flexor r.m.s. EMG between thumb positions were more variable, and overall there was no significant change. Long flexor r.m.s. EMG was 32.4 ± 20.5 μV with the thumb up, and 30.6 ± 22.3 μV during contractions with the thumb down (Fig. 5B). FDI, or long flexor EMG did not differ between groups of subjects with, and without radial nerve block (P > 0.05). Discussion The novel aspect of this study is that when the mechanical effectiveness of a muscle is increased at a joint where more than one muscle can exert force, there is an adaptive increase in the neural drive to that muscle. Based on flexion twitch force, the contribution of FDI to finger flexion at the MCP joint can be altered by positional changes to the thumb, but there is limited change at different C 2009 The Authors. Journal compilation C 2009 The Physiological Society


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carpometacarpal angles. As measured with ultrasound, the flexion moment arm changes with thumb posture, and like flexion twitch force, it is greater with the thumb down. In voluntary flexion contractions at the MCP joint, there is greater EMG in FDI with the thumb down, compared to contractions of the same force with the thumb up. Thus, neural drive to FDI is distributed according to the muscle’s ability to contribute force in a finger flexion task, and the change in drive is consistent with a central strategy which would produce movements efficiently (see also De Troyer et al. 2005).

FDI and mechanical effectiveness: the effect of thumb posture

FDI has a greater contribution to flexion force at any muscle length tested across all joint angles with the thumb down, compared to thumb up, and this increase is most likely to be due to an increase in the flexion moment arm of this muscle. The effect of thumb posture on the moment arm of FDI has not been determined previously. Investigations of the moment arm of FDI in amputated limbs used an isolated index finger (An et al. 1983), and measurement of the moment arm in vivo maintained the position of the thumb (Fowler et al. 2001). We found that when the thumb was moved from up to down, the tendon of FDI moved in a palmar direction such that the distance between the FDI tendon and metacarpal bone (close to the

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axis of rotation for flexion) was 2.6 mm greater with the thumb down. The change in the moment arm is likely to be due to the superficial head of the muscle, as the position of the second metacarpal, to which the deep head of FDI attaches, was constant. We did not measure the distance between the FDI tendon and the centre of rotation of the MCP joint, as only the edge of the metacarpal bone could be visualized with ultrasound. However, if we express the change in distance between the tendon and metacarpal edge, relative to the moment arm found in isolated index fingers from amputated limbs (4 mm at 0 deg index finger flexion; An et al. 1983), the change represents a 65% increase in the moment arm of FDI when the thumb is repositioned to a down posture. By comparison, there was a 60% increase in the maximal flexion twitch force of FDI with the thumb down. Other factors which could influence the ability of FDI to produce flexion forces at the MCP joint include a shift on the length–tension curve of FDI, and a change in the pennation angle of the muscle fascicles. However, these factors appear less important than changes in moment arm. The changes in FDI muscle length and pennation angle with changes in the angle of carpometacarpal extension or abduction did not alter the contribution of FDI to flexion force at the MCP joint across most of the physiological range. Carpometacarpal angle had a moderate effect on the maximal flexion twitch force at full adduction for the thumb down posture. This

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Figure 5. Muscle activation during a voluntary flexion contraction of 5 N at the index MCP joint in the two thumb postures Panels show individual (open symbols) and mean ± S.E.M. (filled circles) from 15 subjects. Data from subjects with a radial nerve block are shown as open diamonds (n = 5). Data are normalized to values with the thumb down for each subject. A, for 14/15 subjects and the group, FDI activity was greater during voluntary contractions with the thumb down compared to those with the thumb up. One subject had almost no activation of FDI during contractions with the thumb up and showed a marked increase in its activity when the thumb was down. Irrespective of whether data from this subject were included, FDI activity was significantly greater in the posture with a greater mechanical effectiveness (thumb down; P < 0.01). B, the change in activity in the long flexors during flexion contractions was variable. For the majority of subjects (10/15 subjects), there was less long flexor EMG in contractions with the thumb down, but this was not statistically significant for the group. C 2009 The Authors. Journal compilation C 2009 The Physiological Society

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contrasts with other muscles, for example, the elbow flexor (Prasartwuth et al. 2006), and ankle dorsiflexor (Koh & Herzog, 1995) muscles, in which large increases (∼30% or more) in evoked torque occur with altered joint angle. Either FDI muscle fibre length is less sensitive to changes in joint angle, or the length–tension curve for FDI is relatively flat (for flexion force). The pennation angle of FDI fibres is low (∼9 deg), but values were not given for the two heads of FDI, or for different thumb postures (Jacobson et al. 1992).

Neural drive to FDI during voluntary flexion contractions

In concert with the greater mechanical effectiveness of FDI for flexion force at the index finger with the thumb down, the neural drive to FDI increased during voluntary contractions with the thumb down, as evidenced by a 28% increase in FDI EMG. EMG was recorded with surface electrodes near the second metacarpal and will include activity from both superficial and deep muscle compartments although the component of FDI attached to the first metacarpal is larger and superficial (Chao et al. 1989). As the increase in flexion mechanical effectiveness of FDI with positional changes to the thumb is likely to be due to the movement of the moment arm of the superficial head, the increase in FDI EMG in voluntary flexion contractions may reflect an increase in neural drive to this region also. However, in two subjects, both heads of FDI were active in index flexion against resistance, with more activity reported in the deep compared to the superficial head (Masquelet et al. 1986). Unfortunately, the flexion angle of the MCP joint at which the contractions were made was not given (Masquelet et al. 1986). The moment arms of the two heads of FDI vary with the degree of index finger flexion (An et al. 1983), and therefore, their relative activity may alter with flexion angle. In voluntary contractions, the first lumbrical muscle may have contributed to the recorded EMG and flexion force at the MCP joint, but its contribution is likely to be small, and unaltered by changes in thumb posture (Lauer et al. 1999). To produce the same finger flexion force, an increase in FDI activity should be accompanied by a decrease in activation of synergistic muscles. However, no decrease in activity of the long flexors was seen. Although care was taken to place the electrodes over the long flexor muscles of the index finger, surface EMG recordings are unselective, and the expected decrease in activity was presumably masked by activity in nearby finger and wrist flexor muscles. The level of agonist muscle activity required to produce a set force must increase if the antagonist muscle contracts. To minimize this potential error, we matched

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finger extensor EMG during contractions in the two thumb postures in 10 ‘intact’ subjects, and completely eliminated differences in co-contraction in five subjects by a radial nerve block. In subjects with radial nerve block, in whom voluntary extension at the MCP joint was abolished, there was less long flexor EMG with the thumb down for 4 out of 5 subjects.

Coupling of mechanical effectiveness and neural drive

When performing the same flexion task with different thumb postures, the neural drive to FDI changed according to its mechanical effectiveness. Hence, it may be recruited in a task-dependent way in which the amount of force it produces and the neural drive it receives are linked. Task-related changes in the discharge behaviour of motor units in FDI have been reported. FDI contributes to abduction and flexion forces (Thomas et al. 1986; Enoka et al. 1989; Kutch et al. 2007). However, in ∼10% of FDI motor unit pairs, the threshold force at which units are recruited is less in abduction compared to flexion (Desmedt & Godaux, 1981; Enoka et al. 1989), or the recruitment order in pairs of motor units is altered (Desmedt & Godaux, 1981; Thomas et al. 1986), particularly when pairs are sampled from different recording sites in FDI (Desmedt & Godaux, 1981). There are similar examples of task-dependent alterations of motor unit behaviour in other muscles of the limb, jaw and thorax (e.g. ter Haar Romeny et al. 1982; McMillan & Hannam, 1992; Kennedy & Cresswell, 2001; De Troyer et al. 2003; Mottram et al. 2005; Gandevia et al. 2006). In the human intercostal muscles, there is recruitment according to a principle of neuromechanical matching (Butler et al. 2007), whereby parts of an intercostal muscle are recruited according to their relative inspiratory mechanical advantage. Although recruitment of motor units by this principle maximizes the efficiency of ventilation (De Troyer et al. 2005), it should be applicable to other muscles, such as FDI, to maximize movement efficiency. If there is a coupling of or mechanical effectiveness and neural drive, what is the mechanism responsible for the matching? Receptors, such as those in the skin, muscles and joints, signal muscle length, force and joint angle, and these inputs could be integrated by the central nervous system to determine the overall biomechanical state of a multijoint system, and recruit muscles and/or motor units accordingly with the most efficient strategy. For the intercostal muscles, recruitment by inspiratory mechanical advantage remains even when afferent feedback is altered or removed (De Troyer & Legrand, 1995; De Troyer et al. 1996; Legrand et al. 1996). A similar invariance has been reported for recruitment of two C 2009 The Authors. Journal compilation C 2009 The Physiological Society

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human inspiratory muscles operating on the upper rib cage (Hudson et al. 2007). This suggests that the pattern of respiratory neural drive to the inspiratory muscles is ‘preset’. However, in all these studies, mechanical advantage was not changed acutely, and therefore the altered afferent feedback was not appropriate to signal a change in mechanical advantage. For FDI, where mechanical effectiveness can change depending on posture or position, neural recruitment strategies can also change. This suggests that the mechanical performance of FDI is either signalled acutely by afferents or is known from prior experience. References Adrian ED & Bronk DW (1929). The discharge of impulses in motor nerve fibres: Part II. The frequency of discharge in reflex and voluntary contractions. J Physiol 67, 119–151. An KN, Ueba Y, Chao EY, Cooney WP & Linscheid RL (1983). Tendon excursion and moment arm of index finger muscles. J Biomech 16, 419–425. Butler JE, De Troyer A, Gandevia SC, Gorman RB & Hudson AL (2007). Neuromechanical matching of central respiratory drive: a new principle of motor unit recruitment? Physiology News 67, 22–24 (http://www.physoc.org). Chao EYS, An K-N, Cooney WP & Linscheid RL (1989). Quantitative analysis of the intrinsic and extrinsic musculature of the hand. Biomechanics of the Hand: A Basic Research Study, pp. 31–51. World Scientific Publishing Co., Singapore. De Troyer A, Gorman RB & Gandevia SC (2003). Distribution of inspiratory drive to the external intercostal muscles in humans. J Physiol 546, 943–954. De Troyer A, Kirkwood PA & Wilson TA (2005). Respiratory action of the intercostal muscles. Physiol Rev 85, 717–756. De Troyer A & Legrand A (1995). Inhomogenous activation of the parasternal intercostals during breathing. J Appl Physiol 79, 55–62. De Troyer A, Legrand A, Gayan-Ramirez G, Cappello M & Decramer M (1996). On the mechanism of the mediolateral gradient of parasternal activation. J Appl Physiol 80, 1490–1494. Desmedt JE & Godaux E (1981). Spinal motoneuron recruitment in man: rank deordering with direction but not with speed of voluntary movement. Science 214, 933–936. Enoka RM, Robinson GA & Kossev AR (1989). Task and fatigue effects on low-threshold motor units in human hand muscle. J Neurophysiol 62, 1344–1359. Fowler NK, Nicol AC, Condon B & Hadley D (2001). Method of determination of three dimensional index finger moment arms and tendon lines of action using high resolution MRI scans. J Biomech 34, 791–797. Gandevia SC, Hudson AL, Gorman RB, Butler JE & De Troyer A (2006). Spatial distribution of inspiratory drive to the parasternal intercostal muscles in humans. J Physiol 573, 263–275. Gordon AM, Huxley AF & Julian FJ (1966). The variation in isometric tension with sarcomere length in vertebrate muscle fibres. J Physiol 184, 170–192. C 2009 The Authors. Journal compilation C 2009 The Physiological Society

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Acknowledgements This work was supported by grants from the National Health and Medical Research Council.

C 2009 The Authors. Journal compilation C 2009 The Physiological Society