Tension distribution to the five digits of the hand by neuromuscular compartments in the macaque flexor digitorum profundus

Abstract

The macaque flexor digitorum profundus (FDP) consists of a muscle belly with four neuromuscular regions and a complex insertion tendon that divides to serve all five digits of the hand. To determine the extent to which compartments within FDP act on single versus multiple digits, we stimulated the primary nerve branch innervating each neuromuscular region while recording the tension in all five distal insertion tendons. Stimulation of each primary nerve branch activated a distinct region of the muscle belly, so that each primary nerve branch and the muscle region innervated can be considered a neuromuscular compartment. Although each neuromuscular compartment provided a distinct distribution of tension across the five distal tendons, none acted on only one digital tendon. Most of the distribution of tension to multiple digits could be attributed to passive biomechanical interactions in the complex insertion tendon, although for the larger compartments a wider distribution resulted from the broad insertion of the muscle belly. Nerve ligations excluded contributions of spinal reflexes or distal axon reflexes to the distribution of tension to multiple digits. We conclude that the macaque FDP consists of four neuromuscular compartments, each of which provides a distinct distribution of tension to multiple digits.

Fig. 1.

Experimental setup. Each of the five digital tendons of FDP was tied to a separate, independently positioned tension transducer, served by its own signal conditioner channel. Tissues of the palm and carpal tunnel were not dissected so that biomechanical interconnections here would be as close as possible to those in the intact animal. Bone screws placed in the distal radius, distal ulna, and proximal ulna fixed the forearm to an underlying frame, and a horizontal bar supported the metacarpus against gravity. Superficial forearm flexor muscles were dissected and removed, exposing the belly of FDP and its nerve supply. A protective oil pool was constructed with the skin flaps. Each primary nerve branch in turn was then elevated into the oil pool on a bipolar hook electrode for stimulation.

Fig. 2.

Standard map of FDP. This drawing of the superficial aspect of FDP, as if dissected free from the rest of the right forearm and hand, indicates the four neuromuscular regions of the muscle: r, radial region, FDPr; u, ulnar region, FDPu; a, accessory region, FDPa;pu, proximal ulnar region, FDPpu. Whereas the first three regions are innervated by primary nerve branches arising from the median nerve trunk, the latter typically is innervated by a branch from the ulnar nerve. The course of each nerve branch after penetrating the muscle belly is indicated by a string of symbols: ♦, FDPr; ▪, FDPu; ▴, FDPa; and ●, FDPpu. The locations of electrodes inserted to record compound muscle action potentials are indicated by ★: rd, radial distal; ri, radial intermediate; rp, radial proximal; a, accessory; ud, ulnar distal; ui, ulnar intermediate; up, ulnar proximal. The proximal insertion aponeurosis is indicated by stippling, with longitudinal furrows in the aponeurosis shown as horizontal black lines. a–l indicate the locations at which suture loops were tied for passive loading. A bracketindicates the portion of the insertion tendon that lies in the carpal tunnel. The digital insertion tendons on the thumb through the little finger are labeled t1 through t5, respectively.

Fig. 3.

Electromyographic localization.A, Compound muscle action potentials recorded simultaneously by intramuscular electrodes at each of the seven locations (rd through up), as indicated in Figure 2, are shown after a single supramaximal stimulation pulse in a 1 Hz train delivered to each primary nerve branch in turn (FDPr, FDPu, FDPa, or FDPpu) in a single experiment. The amplification of each channel was constant throughout, and the vertical scale represents ±5 V for each channel. The stimulation pulse was delivered to each nerve branch at the time indicated by the arrows at thebottom. B, The amplitude of the compound muscle action potentials recorded by a given electrode during stimulation of each primary nerve branch was normalized from 0 to 1 in each experiment, and these normalized values were averaged across experiments. Lines connect the pointsrepresenting the mean ± SD normalized EMG responses recorded from each of the seven intramuscular electrodes during stimulation of a given nerve branch. Abbreviations for electrode locations are as described in the legend to Figure 2. Stimulation of each primary nerve branch evoked compound muscle action potentials localized to the appropriate region of the muscle. For most points, the SD error bars fell inside the symbol representing the mean. Normalized EMG amplitude was most variable near the ulnar proximal and ulnar intermediate electrodes, consistent with the variable innervation of region FDPpu found in these monkeys.

Fig. 4.

Effects of stimulation frequency.A, An original recording shows tension in each FDP tendon during stimulation of an FDPr primary nerve branch at 1, 5, 10, 20, and 40 Hz. The vertical scale representing 0–1500 gm is the same for each digital tendon, t1 through t5.B, Mean tension (over 1 sec) in each tendon has been plotted as a function of stimulation frequency. Data are from the record shown in A. C, SEL and OPI indexes calculated from the same data are plotted against one another for each stimulus frequency to demonstrate that the distribution of tension among the five tendons of FDP did not vary with stimulation frequency.

Fig. 5.

Tension distribution by the different regions of FDP. A, Plots of the tension exerted on each digital tendon during 20 Hz stimulation of each primary nerve branch. Values are the average across subjects with SD error bars. B, The SEL and OPI indexes calculated for the tension distribution produced by 20 Hz stimulation of each primary nerve branch in each experiment have been plotted against one another. (Note that, because of atypical innervation in one animal, only 4 points were available for FDPpu. Only 4 points were available for FDPu because stimulation of this nerve branch inadvertently was omitted at this stage in one experiment.) The same plot shows SEL versus OPI for passive loading at each location tested on the proximal insertion aponeurosis (Fig.7).

Fig. 6.

Passive loading of the proximal insertion aponeurosis. A, An original record shows the simultaneous tension in all five distal tendons as a 1 kg weight was lowered (↓) and raised (↑) by hand, alternately applying and removing a proximally directed load to the proximal insertion aponeurosis of FDP at point l in Figure 2. The vertical scale represents 0–400 gm for each tendon. B, The data from A have been plotted as a function of the instantaneous total tension in all five tendons. The linear relationships indicate that a constant fraction of the total passive load on the proximal insertion aponeurosis was distributed to each distal insertion tendon.

Fig. 7.

Tension distributions from passive loading versus active contraction. A, The distribution of tension, normalized such that the total on all five digits equals 1, has been plotted for each passive loading site. The SEL and OPI indexes for each of these distributions are shown in Figure 5B (+).B, As the site of passive loading gradually shifted from more ulnar (a) to more radial (l), the OPI appropriately shifted from more ulnar (positive) to more radial (negative) values. C, The normalized tension distributions from stimulation of each primary nerve branch in each experiment have been plotted for comparison with the normalized tension distributions from passive loading inA. The underlying data are the same as for Figure 5. Note that these distributions for active contraction of regions FDPr (⋄) and FDPu (■) are broader (less selective) than those for any point under passive load, as also indicated by the low SEL values in Figure 5B.

Fig. 8.

Tension distributions after eliminating spinal reflexes. A, Plots of the tension exerted on each tendon during 20 Hz stimulation of each primary nerve branch after cutting the median and ulnar nerve trunks in the upper arm. Values are the average across subjects (n = 3) with SD error bars.B, The SEL and OPI indexes calculated for the tension distribution produced by 20 Hz stimulation of each primary nerve branch in each experiment have been plotted against one another. (Note that, because FDPpu received atypical innervation in 1 of the 3 monkeys studied here, only 2 points were available for this region.)

Fig. 9.

Tension distributions after eliminating axon reflexes. A, Plots of the tension exerted on each tendon during 20 Hz stimulation of each primary nerve branch after cutting the branch off its nerve trunk. Values are the average across subjects (n = 3) with SD error bars. B, The SEL and OPI indexes calculated for the tension distribution produced by 20 Hz stimulation of each primary nerve branch in each experiment have been plotted against one another. (Note that, because FDPpu received atypical innervation in 1 of the 3 monkeys studied here, and in another the FDPpu nerve branch failed to conduct after being cutoff the ulnar nerve trunk, only 1 point was available for this region.)