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Department of Physiology, University of Arizona, Tucson, Arizona
Submitted 8 October 2006; accepted in final form 7 November 2006
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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; Heffner and Masterton 1983; Lawrence and Kuypers 1968; Palmer and Ashby 1992; Porter and Lemon 1993). This privileged monosynaptic input from the cerebral cortex is thought to underlie the adaptability and unique dexterity associated with voluntary movements of the hand (see review by Lemon and Griffiths 2005). In general, these inputs appear to diverge extensively to contact many neurons within a motor nucleus (Lawrence et al. 1985; Mantel and Lemon 1987) and may also ramify to contact multiple motor nuclei, particularly those supplying extrinsic hand muscles (Asanuma et al. 1979; Buys et al. 1986; Fetz and Cheney 1980; Hockensmith et al. 2005; Shinoda et al. 1981). However, the precise organization of these descending inputs to motor neurons supplying specified hand muscles, and in particular to multitendoned muscles that serve as the main finger flexor and extensors, is not fully understood.
In humans there are three multitendon extrinsic finger muscles, two flexors [flexor digitorum superficialis (FDS); flexor digitorum profundus (FPD)], and one extensor [extensor digitorum (ED)], located in the forearm, that give rise to four parallel tendons that cross multiple joints and insert onto the four fingers. These muscles, and homologous muscles in nonhuman primates, appear to be composed of relatively distinct compartments (Keen and Fuglevand 2003, 2004a; Kilbreath and Gandevia 1994; Schieber 1991), each of which operates on a separate digit. Recent studies of ED (Keen and Fuglevand 2004b) and FDP (Reilly et al. 2004; Winges and Santello 2004) indicate that the subsets of motor neurons that innervate different muscular compartments within these multitendoned muscles do not receive entirely segregated synaptic inputs. Instead, last-order inputs that are primarily destined to supply motor neurons innervating one compartment also appear to ramify to contact motor neurons innervating other compartments. Such divergence of synaptic input may limit the ability to differentially activate separate muscular compartments in these multitendoned muscles and thereby contribute to the lack of fully independent actions of the fingers (Aoki et al. 2003; Häger-Ross and Schieber 2000; Kilbreath and Gandevia 1994; Reilly and Hammond 2000; Schieber 1991; Zatsiorsky et al. 2000).
Comparative information about the extent of such divergence for the different multitendoned muscles of the hand would be beneficial for understanding the facility with which each muscle potentially contributes to fractionated movements of the digits. Work done in nonhuman primates indicates a greater degree of divergence in corticospinal projections across motor nuclei supplying extensor muscles compared with flexor muscles of the hand (Fetz and Cheney 1980), implying less independence for extensor muscles. For the two extrinsic flexor muscles, there appears to be an enhanced capacity in humans to selectively activate compartments of the FDS compared with FDP (Butler et al. 2005; Kilbreath and Gandevia 1994). On this basis then, we hypothesized that the breadth of divergence of last-order synaptic inputs would be greatest for ED motor neurons and least for FDS. To address this hypothesis, we estimated the extent of divergence of last-order inputs to FDS motor neurons by measuring the degree of short-term synchrony between motor units residing in different compartments of FDS. These data were then compared, using the same metric, to those previously reported for ED (Keen and Fuglevand 2004b) and FDP (Winges and Santello 2004).
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Forty-two experiments were performed on the right FDS muscle in 28 healthy human volunteers (20 women, eight men, ages 19–54 yr). Five subjects participated in three experimental sessions, five other subjects participated in two sessions, and the remaining subjects participated in one session. Based on the Edinburgh Handedness Inventory (Oldfield 1971), 26 of the subjects were right-hand dominant (laterality quotient range 0.47–1.0), of which 18 were strongly right-hand dominant (laterality quotient 
0.75), one subject had no hand preference (laterality quotient = 0.0), and one subject was left-hand dominant (laterality quotient = –0.67). Procedures were approved by the Institutional Human Investigation Committee at the University of Arizona. All subjects gave informed consent as required by the Helsinki Declaration.
The FDS originates from the humerus and proximal ulna and typically gives rise to four tendons that insert on the middle phalanges of the index (digit 2, D2), middle (D3), ring (D4), and little (D5) fingers. One of the main functions of FDS is thus to flex the proximal interphalangeal (IP) joint without concurrent flexion of the distal IP joint, which is controlled by FDP. There are a number of anatomical anomalies noted for FDS, especially related to the tendon to the little finger, including absence of the tendon (Furnas 1965; Gonzalez et al. 1997; Kaplan 1969). An absent FDS tendon to the little finger precludes the ability to isolate volitional flexion to the proximal IP joint, leaving flexion to occur through the action of the FDP to the distal segment. Therefore before each experiment, we screened for the presence of an FDS tendon to the little finger by having each subject attempt to selectively flex the proximal IP joint of the little finger (Stein et al. 1990). We subsequently attempted to record from the little finger compartment of the FDS only in those subjects who could perform this maneuver.
Experimental setup
Subjects were comfortably seated in a dental chair with the right arm supported on a horizontal platform and the proximal forearm and elbow stabilized in a padded trough. The hand was held in a vertical orientation, midway between full supination and pronation, by padded vertical posts placed in contact with the dorsal and palmar aspects of the hand. An additional narrow vertical post was placed just distal to the metacarpophalangel (MCP) joints to contact the volar surface of the proximal phalanges of digits 2–5 and served to hold the MCP joints in a neutral orientation. The proximal IP joints of each finger were maintained in slightly flexed configurations (about 30° flexed from full extension) by narrow leather bands around the middle phalanges of each digit that were attached to separate force transducers.
Force and electromyographic recording
Flexion forces of the digits were measured by four force transducers (model FT-10, range 0–5 N, sensitivity 780 mN/mV; Grass Instruments, Warwick, RI) mounted in a custom-built manipulandum. Each transducer was aligned with the direction of pull orthogonal to the long axis of the middle phalanges of each digit. Force signals were amplified (x1,000) (World Precision Instruments, Sarasota, FL) and displayed on an oscilloscope.
Single-unit electromyographic (EMG) activity was recorded with sterilized, lacquer-coated tungsten microelectrodes inserted percutaneously into the FDS muscle (1- to 5-µm-tip diameter, 5- to 10-µm uninsulated length, 250-µm shaft diameter, about 200-k
impedance at 1,000 Hz after insertion; FHC, Bowdoinham, ME). Surface electrodes (4 mm diameter Ag–AgCl) attached to the skin overlying the radial styloid served as reference electrodes for each intramuscular electrode. Two microelectrodes were inserted into FDS at different locations to record the activity of separate motor units on each electrode. In some trials, the two electrodes were placed into the same compartment, and in other trials the electrodes were placed in separate compartments. Weak electrical stimulation (1.0-ms pulses, 1 Hz, 0.2–6.0 mA) was used initially and between each trial to identify, based on the evoked force responses, the compartment location of each electrode and to verify microelectrode placement in FDS (Hockensmith et al. 2005; Keen and Fuglevand 2004b). Each microelectrode was adjusted in depth and angle until an individuated response of the proximal IP joint of the target digit was elicited on stimulation. Figure 1 depicts example force responses in each of the four fingers to such electrical stimulation in the index (Fig. 1A), middle (Fig. 1B), ring (Fig. 1C), and little (Fig. 1D) finger compartments of FDS.
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; Lemon et al. 1990). The intramuscular and surface EMG signals were amplified (x2,000), band-pass filtered (100–3,000 and 10–1,000 Hz, respectively; Grass Instruments), and displayed on oscilloscopes. Intramuscular EMG signals were also routed to a two-channel audio amplifier. Protocol
Subjects were instructed to perform low-force isometric flexion of all four digits primarily at the proximal IP joint to activate the FDS muscle. The microelectrodes were gently manipulated during the contraction until action potentials of motor units could be clearly identified on each electrode. Subjects were then instructed to sustain weak isometric flexion of all four fingers such that both units remained active. This instruction was the same regardless of the compartment locations of the microelectrodes. During the contractions, the forces exerted by individual fingers were not specified; rather, subjects were instructed to maintain a low rate of discharge of the two motor units while maintaining some degree of flexion force on each finger. Intramuscular EMG signals were recorded for 5 min or until the action potentials could no longer be clearly discriminated. Subjects received visual and audio feedback of the motor-unit discharges and 1–2 min of rest between trials. After each trial at least one of the two microelectrodes was adjusted until a presumed different motor unit was identified. Occasionally this required removal and reinsertion of the microelectrode into a new site, after which placement was verified with electrical stimulation as described above. Successive trials were performed for up to 2 h. Flexion force of each finger, surface EMG, and intramuscular EMG signals were digitally sampled at about 2.0, 2.5, and 12.5 kHz, respectively, using the Spike2 data-acquisition and data-analysis system [Cambridge Electronics Design (CED), Cambridge, UK].
Data analysis
The extent of common, last-order synaptic input was estimated from the level of short-term synchrony in the discharge times of simultaneously recorded pairs of motor units (Kirkwood and Sears 1978; Sears and Stagg 1976). Accordingly, in off-line analysis, motor-unit action potentials were discriminated from intramuscular recordings using a template-matching algorithm (Spike2, CED). Only sections of recordings during which both units remained tonically active were included in the analyses. Cross-correlation histograms (1-ms bins, ±100 ms) were constructed from the discharge times of the discriminated motor units recorded from separate electrodes. The central peak in the histogram was identified using the cumulative sum (cusum) procedure, which involves progressively summing the differences in the number of counts in each bin of the histogram from the mean bin count (Ellaway 1978). The baseline mean was calculated as the mean count in the first and last 60 ms of the histogram. A rise in the cusum near time 0 was used to delineate the central peak in the histogram. The boundaries of this peak were defined as the bins corresponding to 10 and 90% of the maximum cusum values (Schmied et al. 1993). The magnitudes of the central peaks in the cross-correlation histograms were quantified using a synchronization index, referred to as common input strength (CIS). The CIS was calculated as the number of counts within the peak above the baseline mean divided by the duration of the recording, which represents the rate of extra synchronous impulses (extra synch. imp./s) above that expected by chance (Nordstrom et al. 1992). This method for quantifying synchrony is identical to that used previously in similar studies of the other extrinsic multitendoned muscles ED (Keen and Fuglevand 2004b) and FDP (Winges and Santello 2004). In addition, we calculated the index k', which is the ratio of the mean number of counts in the cross-correlogram peak to the baseline mean (Ellaway and Murthy 1985) to enable comparisons between our study and those that have used k' as their synchrony index in studies of other multitendoned extrinsic finger muscles (Reilly et al. 2004).
When no clear peak was evident in the cross-correlation histogram, the technique described above for identifying the region of the histogram for which to calculate CIS or k' was unreliable. Therefore for cases of nonsignificant peaks in the histograms, CIS and k' were calculated for an 11-ms region of the histogram centered at time 0 (Semmler and Nordstrom 1995). For the histogram peak to be considered significant, the average count within the peak needed to be >3 SDs above the baseline mean (z score 1.96 associated with a significance level of P < 0.05). All CIS and k' values, regardless of the method used for calculation, were included in the analysis.
Spike-triggered averaging of the surface EMG based on the discharge times of the discriminated motor units was performed after each experimental session to verify that each motor-unit pair recorded was not duplicated in subsequent trials of the same experiment. The identity of motor units was based on visual inspection of amplitude and shape of the spike-triggered average potentials. Suspected duplicate motor-unit pairs were then dropped from further analysis.
Statistical analyses were based on CIS values only (k' values were calculated only to enable comparison with other studies). Trials in which both microelectrodes were situated within the same compartment of FDS are referred to as intracompartmental, whereas trials in which the microelectrodes were located in different compartments are referred to as extracompartmental. Overall, there were 10 possible compartment combinations: four intracompartmental (D2–D2, D3–D3, D4–D4, D5–D5) and six extracompartmental (D2–D3, D3–D4, D4–D5, D2–D4, D3–D5, D2–D5). A Kruskal–Wallis test was performed to determine whether intracompartmental CIS values varied across the four muscle compartments. Kruskal–Wallis is a nonparameteric test based on the sum of the ranks and is used to compare three or more unpaired groups with different sample sizes. In addition, a Kruskal–Wallis test was used to determine whether CIS values differed, depending on the extent of compartmental separation between the recorded motor unit pairs (i.e., same compartment, adjacent compartments, two compartments apart, three compartments apart). Values are reported as means ± SD with a probability of 0.05 selected as the level of statistical significance.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Figure 2A shows four examples of intracompartmental cross-correlograms for each compartment of FDS and their respective CIS values. The labels at the top indicate the compartments within which the microelectrodes were located. The mean (SD) intracompartmental CIS values for each compartment are shown in Fig. 2B. A total of 94 motor-unit pairs were recorded from within the same compartment. These had substantial mean CIS values of 0.43 ± 0.40 (n = 28), 0.34 ± 0.19 (n = 28), 0.45 ± 0.24 (n = 28), and 0.75 ± 0.23 (n = 10) for D2–D5 compartments, respectively (Table 1). A Kruskal–Wallis test revealed a significant difference (P = 0.004) between compartments in CIS values for intracompartmental pairs. Post hoc analysis using the Dunn’s method identified this difference to include only comparisons involving the D5 compartment (between D2 and D5 and between D3 and D5). No other intracompartmental comparisons of CIS were significantly different from one another. Furthermore, there were no significant differences in durations of the cross-correlogram peaks, firing rates, or CVs across the four intracompartmental combinations (Table 1).
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). Despite the slightly higher discharge variability for trials involving extracompartmental pairs, the associated CIS values were still appreciably lower than those obtained during trials involving intracompartmental pairs. Extracompartmental pairs were further categorized according to the respective locations of each recorded motor unit in the pair and the degree of separation between compartments. The adjacent group included the motor-unit pairs of D2–D3 (CIS = 0.26 ± 0.81, n = 35), D3–D4 (CIS = 0.27 ± 0.17, n = 39), and D4–D5 (CIS = 0.26 ± 0.18, n = 10) (Table 1). The two-apart group included the motor-unit pairs of D2–D4 (CIS = 0.16 ± 0.15, n = 31) and D3–D5 (CIS = 0.36 ± 0.28, n = 13). The three-apart group included the motor-unit pairs of D2–D5 (CIS = 0.10 ± 0.13, n = 12). Figure 3A shows four examples of cross-correlograms, one for an intracompartmental pair of motor units and three for each of the groups of extracompartmental pairs, with their respective CIS values. Figure 3B shows the mean (SD) CIS values for all pairs recorded within the same compartment (0.45 ± 0.30, n = 94), for pairs in adjacent compartments (0.26 ± 0.17, n = 84), for pairs two compartments apart (0.22 ± 0.21, n = 44), and for pairs three compartments apart (0.10 ± 0.13, n = 12). A Kruskal–Wallis test revealed a significant effect of compartment separation on CIS (P < 0.001). Post hoc analysis with Dunn’s method indicated all extracompartmental pair groups had significantly smaller CIS values than those of the intracompartment pairs (P < 0.05). Furthermore, the post hoc test showed that the CIS values for pairs of units located three compartments apart were significantly smaller than those for pairs in adjacent compartments (P < 0.05). There was no significant difference in CIS values for pairs of units in adjacent compartments compared with pairs two compartments apart. Likewise, although the mean (0.22) and median (0.18) CIS values for pairs of units two compartments apart were more than twofold that of pairs three compartments apart (mean = 0.10; median 0.06), there was no significant difference in CIS between these groups. This absence of difference here should be interpreted cautiously because of the modest number (12) of observations involving pairs three compartments apart.
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Figure 4 depicts the mean CIS values obtained for various extracompartment combinations of motor-unit pairs for the three extrinsic multitendoned finger muscles: FDP (Winges and Santello 2004), FDS (present study), and ED (Keen and Fuglevand 2004b). Insufficient or no data were available from ED for combinations of motor-unit pairs two and three compartments apart and therefore ED is not depicted for those combinations in Fig. 4. From Fig. 4, it can be seen that the average level of synchrony is greater in FDP (black bars) than in FDS (hatched bars) for all extracompartmental combinations of motor-unit pairs. For adjacent-compartment pairs (i.e., those "one apart"), the average level of synchrony tends to be higher in ED (open bars) than in the flexors for combinations involving ulnar compartments (D3–D4 and D4–D5), whereas ED synchrony appears to be somewhat less than that in the flexors for the most radially situated compartment combination (D2–D3). The functional implications of these apparent differences in synchrony across muscles are highlighted in the following discussion.
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DISCUSSION |
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; Häger-Ross and Schieber 2000; Kilbreath and Gandevia 1994; Zatsiorsky et al. 2000). Anatomical complexity of the FDS muscle
The FDS anatomy is unique when compared with the other multitendoned muscles of the hand, having a more complex arrangement of the digital compartments and greater variation and anomalies across subjects (Brand and Hollister 1999; Ohtani 1979; Wood Jones 1941). For instance, the deep layer of the muscle typically consists of a single proximal belly that gives rise distally to an intermediate tendon from which two muscle bellies emerge, one of which gives rise to the tendon inserting on the index finger and the other gives rise to the tendon inserting on the little finger. In the present experiments, we sampled primarily from the distal, single-digit compartments. Future work is needed to evaluate the organization of the intriguing proximal belly and how its activity is coordinated with that of its two daughter bellies.
In addition to the complex arrangement of the muscle-belly components, there is a surprisingly high proportion of anomalies associated with the FDS tendon to the little finger. Indeed, only 43% of our sample population had a functional FDS tendon to the little finger of the right hand. This is in agreement with the percentage (42%) reported by Stein and colleagues (1990) using more extensive clinical tests of FDS. It remains for future investigations to determine whether the absence of an FDS tendon to the little finger leads to detectable functional impairment in certain types of manipulative tasks. From a practical standpoint, this relatively low incidence of digit 5 tendons limited the number of trials we were able to record involving motor units in the little-finger compartment of FDS.
Functional consequences of extracompartment synchrony
When human subjects attempt to voluntarily flex an individual finger, significant motor unit activity is detected in compartments other than that associated with the targeted compartment in multitendoned flexor muscles (Butler et al. 2005; Kilbreath and Gandevia 1994). This inadvertent activity is particularly prominent in FDP compared with FDS (Butler et al. 2005; Kilbreath and Gandevia 1994). On this basis, Butler and colleagues (2005) suggested that descending pathways destined for the FDS motor nucleus might be more selective for subsets of motor neurons supplying individual compartments of FDS than the pathways that target the FDP motor nucleus. Consonant with this idea, we have shown here that the degree of extracompartment synchrony was less for FDS than that for FDP (Winges and Santello 2004) for every extracompartment combination of motor-unit pairs tested (Fig. 4). Because such extracompartment synchrony can be considered to reflect the extent of neural coupling across motor units acting on different digits, these results imply that FDS has the potential to exert more selective control over individual digits than FDP.
From a functional perspective, it would seem reasonable to suspect that multitendoned flexor muscles might possess a greater capacity for selective control over the digits compared with the multitendoned extensor muscle. One manifestation of such an enhanced capacity for digit individuation should be a lower degree of extracompartment synchrony for multitendoned flexors compared with the extensor. Although this seems to be the case for compartments inserting on digits 3 and 4, and on digits 4 and 5 (Fig. 4), the extensor muscle (ED) appears to exhibit less neural coupling (i.e., extracompartment synchrony) between digits 2 and 3 compared with either of the flexors (Fig. 4).
Interestingly, there is some evidence to indicate a parallel between those patterns of extracompartment synchrony and the relative independence of finger movements for flexion and extension (Robinson and Fuglevand 1999). In that study, subjects were instructed to attempt to flex or extend just one finger while movements of the instructed finger and noninstructed fingers were recorded (Robinson and Fuglevand 1999). The movement that exhibited the greatest independence was index-finger extension, whereas the least independent movement was ring-finger extension. Likewise, the lowest level of adjacent-compartment (i.e., "one apart") synchrony depicted in Fig. 4 is associated with the index-finger compartment of the extensor, ED, whereas the greatest extracompartment synchrony also involves the ED but when associated with the ring finger. Although the high degree of independence associated with index-finger extension could certainly arise from selective activation of the extensor indicis muscle, the behavioral results are nevertheless intriguingly consistent with the predicted patterns of finger independence based on the extent of extracompartment synchrony for different multitendoned muscles.
Finally, the pattern of extracompartment synchrony we found for FDS in which synchrony tended to be greatest for unit pairs in adjacent compartments and to decrease with increasing physical separation between units (Fig. 3) was consistent with previous observations in the ED and FDP (Bremner et al. 1991; Keen and Fuglevand 2004; Reilly et al. 2004; however, see Winges and Santello 2004). Likewise, Kilbreath and Gandevia (1994) and Butler et al. (2005) showed similar patterns of coactivation across compartments in multitendoned flexor muscles when subjects attempted to exert force with a single digit. Furthermore, behavioral studies also showed that the greatest degree of unintended force development (Reilly and Hammond 2000; Zatsiorsky et al. 2000) or digit movement (Aoki et al. 2003; Hager-Ross and Schieber 2000; Schieber 1991) occurs in the digits immediately adjacent to the digit subjects attempt to move in isolation. Although such inadvertent movements of neighboring digits during finger-individuation tasks might partly be related to biomechanical coupling between adjacent digits (e.g., Lang and Schieber 2004), it seems likely that divergence of descending inputs, particularly across submotor nuclei supplying neighboring muscle compartments, may also limit the ability to move the digits independently (Keen and Fuglevand 2004b; Kilbreath and Gandevia 1994).
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests and other correspondence: A. J. Fuglevand, Department of Physiology, College of Medicine, P.O. Box 210093, University of Arizona, Tucson, AZ 85721-0093 (E-mail: fuglevan{at}u.arizona.edu)
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