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INTRODUCTION |
When we manipulate objects we preserve a stable grasp by parallel changes in the grip and load forces at the digit contact surfaces. For example, when we lift an object vertically from a support surface, the grip force (force normal to the gripped surfaces) rises in parallel with the developing load force (vertical force tangential to the gripped surfaces) (Edin et al. 1992
; Johansson and Westling 1984
, 1988a
; Westling and Johansson 1984
). This parallel fluctuation of grip and load force occurs when we accelerate and decelerate objects held aloft with the use of arm movements, walking and running, or jumping (Flanagan and Tresilian 1994
; Flanagan and Wing 1993
, 1995
; Kinoshita et al. 1996
), pull on elastic loads (Johansson and Westling 1984
), and pull or push on immovable objects (Johansson et al. 1992
). Indeed, the coupling between the grip and load forces at the fingertips is a defining characteristic of lifting objects with a precision grip and appears by the age of 2 yr in humans (Forssberg et al. 1991
). In theory, coupling the grip force with load forces reduces the degrees of freedom for controlling these forces, and may simplify the process of achieving coordinated fingertip forces.
We do not completely understand the mechanisms underlying this force coupling at the fingertips. It is likely that the grip force commands reflect the load forces expected to develop at the skin contact patches, on the basis of an internal model of the limb-object system (cf. Ghez et al. 1991
; Johansson and Cole 1992
; Johansson and Westling 1988b
; Lacquaniti et al. 1992
). This is consistent with observations that, during transport of grasped objects, the grip and load force change in parallel and without phase differences regardless of the grip style (e.g., 1- or 2-hand grip) or mode of transport (arm motion vs. jumping) (Flanagan and Tresilian 1994
; Flanagan and Wing 1993
, 1995
; Kinoshita et al. 1996
).
The mechanical arrangement of the extrinsic finger muscles seems likely to affect the process of coupling the grip and load forces (for grasps with the use of the fingertip pads) because these muscles cross the wrist. Activating the extrinsic finger flexors will produce a wrist flexion moment during grasp in addition to grip force (Brand 1985
; Bunnell 1944
; Snijders et al. 1987
). Thus recruiting the finger flexors to assist with a desired wrist action could contribute to force coupling at the fingertips if the wrist action increased fingertip load, for example, during wrist angular motion. However, this also opens the possibility that the grip force could vary independent of fingertip load.
The mechanics of the extrinsic finger muscles pose additional complications to grasping. The force-producing capacities of the extrinsic finger flexors change during wrist motion, as the muscles change their length and velocity. The extrinsic finger flexors can shorten several centimeters during wrist flexion (Brand 1985
). O'Driscoll et al. (1992)
reported that maximum grip strength occurred at ~35° wrist extension, with reductions of grip strength up to 73% at less favorable wrist positions. Thus during angular wrist motion a constant grip-load force ratio would require an appropriate modulation of the neural drive to hand muscles. Johansson and Westling (1984)
in an anecdotal report noted little variation in grip force for slow wrist rotation (<90°/s), indicating that appropriate adjustments occurred in the activation levels of hand muscles. Grip force increased substantially at faster speeds, but the rising inertial loads on the fingertips during hand motion could account for this observation.
In the present experiments we investigated how closely grip force corresponded to fingertip loads during wrist flexion/extension motion and during voluntary changes in wrist isometric force. We observed the grip force to increase during such voluntary wrist actions.
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METHODS |
Subjects and general procedure
A total of 25 healthy adults (20-28 yr) participated in these experiments. Informed consent was obtained from all subjects according to the Declaration of Helsinki.
In each experiment, subjects grasped an object (weight = 24 g) between the thumb and index finger. The three remaining fingers were extended. The gripped surfaces consisted of two parallel square plates (25 mm on a side) spaced ~20 mm apart and covered with sandpaper (#320 grit). Subjects held the test object such that the grip plates were always oriented vertically. A single load cell that was integral to the object transduced the "grip" force exerted between the finger and thumb normal to the plane of the gripped surfaces. The output of the load cell showed <1% deviation from linearity for full-scale deflection over the force range recorded during these experiments. Loads applied at different points to the grip plate yielded a maximum variation of 4% in the load cell's output from edge to edge.
Wrist motion experiment
Six subjects (4 females, 2 males) produced wrist movement (dorsiflexion and palmar flexion) in the horizontal plane while holding the object (Fig. 1). The arm and forearm were elevated so that they were parallel to the floor. The forearm was stabilized midway between pronation and supination in a cast secured to a table. The ulnar side of the hand rested on a lightweight aluminum platform (8 × 3 × 0.5 cm) connected to an axle set in a bearing that allowed the wrist to rotate. The three extended fingers were positioned between upright supports to stabilize the hand for flexion and extension movements of the wrist. A potentiometer attached to the axle transduced the angular position of the wrist.

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| FIG. 1.
Apparatus used for wrist motion experiment. Low-mass object (28 gm) minimized centrifugal force on fingertips. Elastic load provided vertical force on fingertips that required moderate grip force to hold object. Elastic load was maintained at constant level by allowing it to rotate with wrist flexion-extension.
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Subjects grasped the test object such that the fingertips were placed at a level even with the object's center of mass. The object's tangential (vertical) force on the fingertips was increased by a spring (1.24 N/cm) that connected the object to a miniature load cell (Kulite BG-1000) on a second platform. The length of the spring was adjusted to yield ~3 N when subjects held the object with their upper limb placed in the apparatus. The test object and spring rotated synchronously with the wrist. The total weight of the two platforms, spring, and load cells was 150 g, which constituted the mass that the wrist had to accelerate in this experiment.
Subjects produced discrete flexion and extension movements. Vertical load force was displayed to the subjects on an oscilloscope and they were encouraged to maintain a constant load force. Their target force was established after a few practice trials and was between 3 and 4 N for all subjects. For the flexion trials, subjects began with the wrist extended ~50° from neutral and then moved the wrist to a position of ~50° flexion. Subjects maintained this final position for a few seconds before returning the wrist to the starting position. The experimenter supported the object after every five trials or so to allow the subject to rest. Extension trials were performed similarly except that the starting position of the wrist was ~50° flexion. Subjects were instructed to produce wrist motion at three different self-selected speeds: "slow," "medium," and "fast." They performed eight trials at each speed (5 trials for 2 subjects). Only data from medium and fast trials are reported in this paper. Wrist movements during slow trials occurred over several seconds in most subjects and were produced with erratic changes in wrist angular velocity. Across subjects the average peak angular velocity for medium speed trials was 245 ± 79°/s (mean ± SD) for flexion and 240 ± 88°/s for extension. For fast speed trials the velocities were 906 ± 198°/s for flexion and 842 ± 165°/s for extension.
Isometric wrist force
Nine subjects (8 females, 1 male) exerted isometric wrist flexion or extension forces at varying rates while holding the test object with a 200-g weight attached. Subjects sat with the right forearm rigidly restrained, as previously described, except that the hand touched only a flat, rigid bar that was oriented vertically. For flexion trials the palmar surface of the hand was placed against a the bar so that the bar did not overlie the long flexor tendons of the index finger. For extension trials the hand dorsum contacted the bar. Subjects produced target wrist forces of 10%, 25%, and 50% of their maximum voluntary contraction (MVC). Target forces were displayed to the subjects on an oscilloscope. Subjects were instructed to produce wrist force at slowly, over several seconds (slow trials) to the target force, and to hold that force for ~4 s. Three trials at each isometric target force were performed. Six of the nine subjects in the isometric wrist force experiment also produced the force rapidly (fast trials) for five trials each of 50% MVC flexion and extension.
In separate procedures subjects were instructed to exert a wrist force in the flexion or extension direction without increasing the grip force. Subjects viewed the target wrist force levels and the grip force on an oscilloscope. Subjects produced 10 trials of wrist force to either 25% or 50% MVC at a gradual rate. Six of the subjects also produced five trials of the wrist force as fast as possible to 50% MVC.
Isometric leg experiment
Ten subjects (5 males, 5 females) participated in an experiment involving isometric knee extension. Subjects held a 200-g test object and produced knee extension forces with the leg ipsilateral to the object. Subjects sat with the knee flexed ~30° (with 0 equal to alignment of the tibia and femur). The leg was positioned against a padded, horizontal steel bar at the distal aspect of the tibia. Each subject's MVC for leg extension was established. Isometric contractions consisted of 10% MVC at slow, medium, and fast rates; 25% MVC at a medium rate; and 50% MVC at slow, medium, and fast rates. These rates were decided by each subject. Eight trials of each condition were produced.
Electromyographic procedures
Electrical activity was recorded from selected muscles during the wrist motion and isometric wrist force experiments. During the wrist motion experiment, surface electromyographic (EMG) signals were collected from first dorsal interosseous (1DO), flexor digitorum superficialis (FDS), flexor carpi radialis (FCR), and extensor carpi radialis (ECR). The FDS electrodes were placed distal on the forearm, typically within a few centimeters of the distal wrist crease, to minimize cross talk from wrist flexor muscles. During the isometric force experiments, fine wire electrodes (75-µm wire) in bipolar pairs (1-cm interelectrode distance) collected EMG signals from 1DO and FDS. Surface electrodes collected signals from flexor carpi ulnaris and ECR. Surface EMG signals were collected with the use of bipolar silver-silver chloride surface EMG electrodes filled with conducting jelly. Interelectrode distances were 1 cm for 1DO and FDS and 3 cm for FCR and ECR. The common-mode reference electrode for use with the differential preamplifiers was placed over the olecranon process. Muscle activity signals were filtered during amplification (30 Hz-2.5 kHz).
Data sampling and signal processing
All data were digitized at 12-bit resolution with a personal computer with the use of the "SC/ZOOM" system (Department of Physiology, University of Umeå, Umea, Sweden). Force and position signals were sampled at 400 Hz. EMG signals were sampled at 1,600 Hz for the wrist motion experiment and at 3,200 Hz for the isometric force experiment. These were full-wave rectified digitally. The beginning of force increases and motion were determined by visual inspection with the use of force rate or wrist angular velocity signals, which were calculated as a function of time with the use of a ±5-point numerical differentiation method. Wrist acceleration was computed with the use of this numerical differentiation method also.
The loads acting on the digits from motion of the grasped object during the wrist motion experiment were derived from the digitized wrist motion data. We accounted for these forces to determine whether any grip force changes occurred that were independent of the loads affecting grasp stability. The centrifugal force was calculated as
where m is object mass (0.024 kg), r is distance (m) from the object's center to the estimated center of wrist rotation in the flexion/extension plane (dorso/palmar), and w is wrist angular velocity (rad/s).
The reaction force on the finger or thumb pulp from linear acceleration/deceleration of the object will register as a change in grip force and must be calculated to avoid attributing these grip force changes directly to the neuromuscular system. This reaction force is termed the "inertial force" here and was calculated as
where m and r are as defined above, and a is angular acceleration (rad/s2).
The vectorial sum of the centrifugal and vertical tangential forces (gravitational and elastic) was calculated and termed the "total load." Change in total load during wrist motion was used to help determine whether changes in grip force were related to changes in fingertip loading. In particular, the ratio formed by the change in grip force during wrist movement divided by the change in total load was a dependent variable in some statistical tests.
Data analysis
Repeated-measures analysis of variance (ANOVA) was used for statistical analysis of data, unless otherwise noted. Post hoc comparisons were tested with a Tukey's Honestly Significant Difference Test. Values expressed in the text are means ± SD averaged across subjects, unless otherwise noted.
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RESULTS |
Effects of wrist motion
The grip force increased during wrist flexion or extension, and during fast wrist flexion in particular (Figs. 2-4). For both flexion and extension movements the grip force began to increase slightly before the start of wrist motion for fast movements (32 ± 44 ms; P < 0.0175) and about at wrist motion onset for medium speed movements (18 ± 147 ms after wrist motion onset; P < 0.65). Also, for both movement directions the increased grip force often was maintained after the movement ended.

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| FIG. 2.
Examples of signals obtained from 1 subject on single trial of "rapid" speed wrist flexion (left) and extension (right) movements. Centrifugal load was calculated with the use of angular velocity (see METHODS). Vertical load is force obtained from load cell in series with test object and spring. "Inertial" force is portion of grip force due to linear acceleration of object (see METHODS). Total load is sum of centrifugal and vertical loads. Shaded region depicts grip force that is in excess of total load. Baselines of grip force and total load signals were aligned before movement start. The 2 calibration bars adjacent to grip force and total load traces are for grip force (left bar) and total load (right bar). 1DO, 1st dorsal interosseus; FDS, flexor digitorum superficialis; FCR, flexor carpi radialis; ECR, extensor carpi radialis.
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The increased grip force was not proportional to the motion-dependent change in fingertip loads, and often persisted after wrist motion ceased. This can be observed by comparing the difference in the change in grip force and the change in total load (see METHODS) on the fingertips (Figs. 2-4), and from inspection of the ratio formed by dividing the change in grip force with the change in total load (Fig. 3). The grip force that could be attributed to the reaction force from linear acceleration of the object also was small in relation to the increase in grip force (Figs. 2 and 4; inertial force).

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| FIG. 3.
Examples of signals from 2 subjects (top vs. bottom) performing 5 trials (superimposed) of wrist flexion (right) and wrist extension (left) movements. Bottom traces in each panel: ratio of grip force divided by total load.
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| FIG. 4.
Examples of signals obtained from single subject during single trials at "medium" speed for wrist flexion (right) and wrist extension (left) movements. Calibration bars for total load are located at right of each total load trace.
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The size of the increase in grip-load ratio depended on the speed and direction of wrist movement. This increase was quantified by measuring the change in grip-load ratio between the start of the rise in ratio and the peak ratio. The average increase in the ratio was 1.43 ± 0.34 (SD) for fast flexion, 0.85 ± 0.30 for fast extension, 0.67 ± 0.37 for medium flexion, and 0.41 ± 0.21 for medium extension. A 2 × 2 repeated-measures ANOVA for speed (medium/fast) and direction (flexion/extension) confirmed that the ratio increase was significantly greater for fast wrist movements [F(1,6) = 85.8, P < 0.0001 main effect for speed] and for flexion movements [F(1,6) = 14.0, P < 0.009 main effect for direction]. In contrast, on some trials the ratio change during wrist extension was quite small even for fast extension movements (e.g., Fig. 3, subject 4); this never occurred for fast wrist flexion in any subject.
The disproportional increases in grip force relative to the total tangential load (vertical plus centrifugal) may have been required for a stable grasp if slippery conditions existed at the digit-object contact patches (because force of friction = grip force × coefficient of static friction). This did not seem to be the case. All subjects but one were able to hold the test object (before wrist motion) with the use of load/grip ratios of
1.0 (mean = 1.6). This indicates that adequate frictional forces could be produced during centrifugal loading with grip force responses that were smaller than those observed.
There were characteristic patterns of grip force increase and hand muscle activity. These patterns depended in part on the direction of wrist movement. Two prominent peaks characterized the grip force during fast wrist flexion (Figs. 2 and 3) and these peaks coincided with peaks in wrist acceleration (Fig. 2). The first peak occurred early in wrist movement, typically coinciding with the first peak in acceleration. A rapid reduction in grip force followed this initial peak that eventually approached the premotion grip force. The second peak occurred after the target wrist position was achieved. The wrist angular position demonstrated a slightly underdamped behavior, and the second peak coincided with the second peak in wrist acceleration. During fast wrist extension some subjects exhibited a two-peak pattern in grip force similar to that used during flexion movements, whereas in other subjects the first peak was small or absent (Figs. 2 and 3).
Myoelectric activity increased during wrist flexion in FDS (an extrinsic hand muscle, which crosses the wrist) and 1DO (an intrinsic hand muscle, which does not contribute to wrist torque; Figs. 2 and 4). These muscles remained active after the wrist stopped moving, while it was held in flexion. By contrast, substantially smaller increases in hand muscle activity occurred during wrist extension. In some cases myoelectric activity decreased substantially in finger muscles during wrist extension, and while the wrist was held in extension.
Effects of isometric wrist force and force rate
All subjects increased the grip force when they flexed or extended their wrists isometrically against a rigid bar while holding the test object (Fig. 5). In this experiment the object's total tangential load on the fingertips remained constant at 200 g of weight (see METHODS). The additional grip force was associated with increased activity of FDS and 1DO.

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| FIG. 5.
Examples of signals obtained from single subject producing "fast" isometric wrist flexion (right) and extension (left).
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The initial grip force increase was a force pulse whose timing and size depended strongly on the development of wrist force. Grip force began increasing at about the same time as the wrist force, and the peak grip force rate occurred at about the same time as the peak wrist force rate (Fig. 6). The time at which peak grip force and peak wrist force occurred (relative to the onset of wrist force) also were related. For each subject the latency to peak grip was regressed linearly against the time to maximum wrist force. Regressions included all trials, regardless of direction, speed of action, or final wrist force. Across subjects the correlation coefficients ranged from 0.62 to 0.93 (mean = 0.84) with slopes ranging from 0.52 to 0.89 (mean = 0.70).

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| FIG. 6.
Wrist force and grip force signals along with their 1st derivatives from single subject producing 3 trials (superimposed) of isometric wrist extension at rapid rates (right) vs. slightly slower wrist force rates (left). All trials are aligned with start of wrist force production.
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The size of the grip force pulse depended on the rate of wrist force increase (Fig. 6). The increase in grip force was greater for trials with fast wrist force rates than for slow wrist force rates [F(1,5) = 6.94, P < 0.04, main effect for speed]. The increase at peak grip force averaged 0.9 N (77%) and 2.2 N (159%) for slow and fast flexion, respectively, at the 50% MVC wrist force target, and 0.5 N (54%) and 1.8 N (158%) for slow and fast extension, respectively. Peak wrist force rates ranged from 3 to 106 N/s (mean = 29 ± 20 N/s) for slow trials and from 58 to 305 N/s(mean = 149 ± 62 N/s) for fast trials, at the target force of 50% MVC. The peak wrist force rates for slow and fast trials did not overlap within any subject.
The increased grip force persisted during the time that the wrist force target was maintained. The additional grip force that existed at the time that the wrist force target was reached was larger for greater wrist force targets [F(1,26) = 7.81, P < 0.002, main effect for force level] and for flexion versus extension [F(1,13) = 9.16, P < 0.01, main effect for direction]. The increase in grip force across subjects for slow isometric flexion at 10, 25, and 50% MVC averaged 0.5 N (31%), 0.85 N (40%), and 0.92 N (76%), respectively; increases for slow extension at 10%, 25%, and 50% MVC averaged 0.36 N (15%), 0.37 N (23%), and 0.62 N (42%), respectively.
No subject could prevent the grip force from increasing when isometric wrist flexion or extension force was produced rapidly. Subjects could not suppress the initial dynamic portion of the grip force increase, but could completely suppress the added grip force once the wrist force reached its target level (Fig. 7). Subjects were better able to prevent the grip force from increasing much, if at all, when the isometric wrist force was produced slowly.

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| FIG. 7.
Wrist force and grip force signals from repeated trials of rapid isometric wrist flexion during (A) no visual feedback of grip force and no instructions to subject to suppress grip force increase, and (B) visual feedback of grip force, and instructions to subject to attempt to suppress grip force increase.
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Effects of isometric leg contractions on the grip force
We were interested in whether the grip force increases that were observed in the previous experiments could arise from a generalized motor facilitation (i.e., a Jendrassik effect). Subjects produced isometric contractions of the quadriceps muscles while holding an object with a precision grip. Compared with the upper limb experiments, only small increases in grip force occurred during isometric leg extension (5, 7, and 15.7% change for 10, 25, and 50% MVC at slow rates of force production. Moreover, the grip force did not depend on the rate of knee extension force (Fig. 8). The grip force increased slowly, even on trials with rapid knee extension, and reached a maximum at variable times well after peak knee extension. Only 1 of the 10 subjects showed a grip force that increased with the rate of isometric leg contraction.

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| FIG. 8.
Examples of signals obtained during knee extension from 1 subject. A: slow extension. B: fast extension. Note that grip force does not depend on knee force rate.
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DISCUSSION |
One purpose of these experiments was to examine how well the commands for precision grip force account for the muscle length and velocity changes that occur during wrist angular motion, and also for the moment that the extrinsic finger muscles produce at the wrist. Subjects did not maintain a constant grip force either in flexion or extension directions. This finding is consistent with a report from Johansson and Westling (1984)
, who described increases in grip force for rapid wrist rotations, but not for slow rotations(<90°/s). Furthermore, the present results indicate that the increased grip force exceeded the added tangential fingertip loads from hand and object motion. The failure to regulate the grip-load ratio was demonstrated also when grip force rose while subjects voluntarily produced isometric forces at the wrist. These data indicate that the production of voluntary wrist forces can affect the coupling between the grip force and tangential fingertip load.
The mechanisms underlying the increased grip force differed somewhat for wrist flexion motion versus extension. During rapid wrist flexion the hand closing muscles that we monitored (FDS and 1DO) increased their myoelectric activity, paralleling the activity of the FCR, a primary wrist flexor. This increased drive to the hand muscles more than offset the decline in grip force that occurred from the shortening of the extrinsic finger flexors during wrist flexion, and produced substantial increases in the grip force. In contrast, the grip force increases during wrist extension (which were smaller than those during flexion) occurred without substantial increases in hand muscle EMG. Thus the increased grip force must have occurred from eccentric (lengthening) contraction of the extrinsic finger flexors, because they were active to maintain a grip force. To prevent this rise in grip force the drive to hand closing muscles must be reduced during wrist extension. Reduced activity of 1DO and FDS during wrist extension occurred in only some subjects, and these reductions were not sufficient to offset the grip force increases from extrinsic finger flexor muscle lengthening. This reasoning assumes that the other extrinsic flexor (flexor digitorum profundus) did not markedly increase its activity in relation to FDS. This assumption seems reasonable on the basis of previous studies of muscle action during finger flexion movement and pinch (Darling et al. 1994
; Maier and Hepp-Reymond 1995a
).
The increased finger flexion force should have been matched by opposing increases in thumb forces for grip force to increase while static equilibrium was maintained. We did not measure digit or object motion, but such motion would have been small to have escaped our observation. It is likely, therefore, that thumb muscle myoelectric activity increased. During pulp pinch, myoelectric activity of many intrinsic finger and thumb muscles, and extrinsic flexor muscles, varies in proportion to changes in pinch force (Johansson and Westling 1988b
; Kilbreath and Gandevia 1993
; Long 1970; Maier and Hepp-Reymond 1995a
,b
).
It is likely that a high-level controller is responsible for most of the process of coupling the grip force to the load forces (Flanagan and Wing 1995
; Johansson 1996
). This interpretation is favored because grip force is modulated automatically in anticipation of fingertip loads (Johansson and Westling 1988a
), and the function describing grip-load coupling can be independently controlled with regard to its gain and offset (Flanagan and Wing 1995
). A high-level controller may have generated the rise in grip force during wrist motion to generate the frictional force needed to offset the rising centrifugal loads on the fingertip. Recent experiments demonstrate that, compared with holding an object motionless, the motor system adopts a more conservative strategy (i.e., a higher grip-load ratio) during intended object acceleration (Flanagan and Tresilian 1994
; Flanagan and Wing 1995
) and when responding automatically to unexpected object acceleration (Cole and Johansson 1993
). This strategy may be especially useful to avoid slips during wrist angular motion, when predictions of grip force are further complicated by the changing lengths and velocities of the extrinsic finger flexors.
However, several characteristics of the present data indicate that the disproportionate increases in grip force during wrist flexion occurred also because the extrinsic finger flexors were recruited to assist in wrist force production. During wrist flexion movement the initial peak in grip force coincided roughly with peak wrist acceleration, rather than the peak total load, which occurred later. Likewise, the second peak in grip force coincided with a second peak in wrist acceleration, which occurs after the load forces had returned to near-baseline levels. On the basis of this reasoning, the second peak in grip force may be associated with attempts to clamp the wrist at the desired final position. The second peak was not from lengthening contractions of finger flexors, because the second rise in grip force occurred after any terminal oscillation of wrist position. Finally, the grip force and finger muscle activity remained elevated while the wrist was held motionless in extreme flexion and inertial loads from wrist motion were absent. We presume that the extrinsic finger flexors acted in this way to assist other wrist flexors in maintaining wrist position against the limb's elastic forces from soft tissues. This is consistent with the grip force increases observed during isometric wrist flexion in the second experiment. Similar to the finger's extrinsic flexors, the flexor pollicis longus and abductor pollicis longus have moment arms for wrist flexion (Brand 1985
). These thumb muscles, if recruited as discussed previously, could contribute to the dual tasks of contributing to wrist flexion torque and pinch force.
The coactivation of 1DO (an intrinsic hand muscle) with FDS during wrist flexion may have occurred to maintain static equilibrium, given that nearly all hand muscles have moment arms at more than one joint, and around two or more axes at each joint (Brand 1985
). We expect that intrinsic thumb muscles likewise increased their activity, assuming that extrinsic thumb muscles increased their activity during grip force increases, as discussed previously. This general muscle coactivation during grasp is consistent with previous studies of muscle function during pulp pinch (Johansson and Westling 1988b
; Kilbreath and Gandevia 1993
; Long 1970; Maier and Hepp-Reymond 1995a
,b
; Smith 1981
).
The increased grip force during isometric wrist flexion provides further evidence that the extrinsic finger flexors were recruited to assist other wrist flexors. The close relationship between the timing and amplitude of the initial pulse of isometric wrist and grip force is consistent with the coactivation of the extrinsic finger flexors and other wrist flexors. The difficulty in suppressing the initial rise in grip force during isometric wrist actions may indicate that the extrinsic finger flexors routinely serve wrist motor goals. Our data from wrist flexion tasks are consistent with a report that tensile force, measured directly from human extrinsic finger flexor tendons during surgery, increased up to 0.3 kg during voluntary wrist flexion even though subjects were instructed to keep their fingers "relaxed" (Schuind et al. 1992
).
Our observation that the grip force increased during isometric wrist extension is difficult to explain on a functional basis because the rising grip force indicates an increasing wrist flexor moment, which would oppose the isometric wrist extension action. Nor does there appear to be any advantage to coactivating the finger flexors or increasing the grip-load ratio during this isometric task. Instead, the increased finger flexor activation may reflect a Jendrassik-like general motor facilitation of finger flexors when other muscles of the forearm are activated. Voluntary contractions of specific muscle groups influence alpha motoneuron excitability of remote muscles (Clarke 1967
; Delwaide and Toulouse 1981
; Hagbarth et al. 1975
; Watanabe et al. 1994
). This type of remote muscle facilitation may be responsible for the weak grip force increases that occurred during isometric leg contractions, and for at least some of the increased grip force during wrist muscle activation. For example, the easily suppressed static phase of the grip force increase may reflect a Jendrassik effect. It is debatable whether the grasp force pulse that developed during wrist muscle activation results from a general motor facilitation. On knee extension the grip force did not depend on knee force rate, in contrast to the grip force pulses that arose during wrist actions. However, these contrasting findings may reflect differences in the proximity of motoneuronal pools or premotoneuronal pools used for knee extension versus wrist action. If so, a general motor facilitation also may account for the coactivation of finger flexors and other wrist flexors that we observed during wrist flexion.
Flanagan and Wing (1995)
suggest that a portion of the grip-load coupling they observed when subjects moved grasped objects with the upper limb may result from an obligatory or "low-level" mechanism. In one of those experiments subjects grasped and lifted a test object with a large voluntary grip force and then moved the object back and forth in the horizontal plane. Flanagan and Wing observed that the grip force modulated in parallel with the fingertip tangential loads even though the grip force that they employed before starting the horizontal object motion was large enough to maintain a stable grasp without further increases in grip force. This seemingly obligatory coupling of the grip and load forces may reflect a low-level coupling of the grip force with tangential fingertip loads, as suggested by Flanagan and Wing (1995)
, and it also may reflect the more general coactivation of finger flexors with other wrist muscles, as observed in the present experiments.
One advantage of recruiting the hand closing muscles (extrinsic and intrinsic) in parallel with other wrist muscles while lifting or transporting rigid objects is that the resulting grip force will occur synchronously with the tangential load at the fingertips. The inertial or resistive loads that develop at the wrist during lifting or transporting objects must be opposed by wrist muscle activity to prevent wrist motion. Unrestrained limb movement from shoulder and/or elbow motion causes phasic activation of the muscles around the wrist (Koshland and Hasan 1994
; Koshland et al. 1991
), apparently to stabilize the wrist. The resulting coactivation of hand closing muscles with wrist muscles will contribute partially to coupling the grip and tangential load forces at the fingertips. However, our observations indicate that the potential contribution to grip-load coupling from these mechanisms will weaken considerably for some movements. The task of coupling the grip forces to the fingertip loads may fall exclusively to the "higher-level" mechanisms suggested by Flanagan and Wing (1995)
and Johansson (1996)
for slow movements, or whenever small muscle forces at the wrist can be used to maintain a stable wrist position. This may be advantageous for tasks that are best performed with minimal grip-load ratios, for example when manipulating delicate objects or when dexterity must be maximized.