Comparison of External Load Compensation During Rhythmic Arm Movements and Rhythmic Jaw Movements in Humans

J. H. Abbink,1 A. van der Bilt,1 F. Bosman,1 H. W. van der Glas,1 C. J. Erkelens,2 and M.F.H. Klaassen1

 1Department of Oral Pathophysiology, Faculty of Medicine, University of Utrecht; and  2Helmholtz Institute, Faculty of Physics and Astronomy, University of Utrecht, 3584 CC Utrecht, The Netherlands


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Abbink, J. H., A. van der Bilt, F. Bosman, H. W. van der Glas, C. J. Erkelens, and M.F.H. Klaassen. Comparison of External Load Compensation During Rhythmic Arm Movements and Rhythmic Jaw Movements in Humans. J. Neurophysiol. 82: 1209-1217, 1999. Experiments were performed on human elbow flexor and extensor muscles and jaw-opening and -closing muscles to observe the effect on rhythmic movements of sudden loading. The load was provided by an electromagnetic device, which simulated the appearance of a smoothly increasing spring-like load. The responses to this loading were compared in jaw and elbow movements and between expected and unexpected disturbances. All muscles showed electromyographic responses to unexpected perturbations, with latencies of ~65 ms in the arm muscles and 25 ms in the jaw. When loading was predictable, anticipatory responses started in arm muscles ~200 ms before and in jaw muscles 100 ms before the onset of loading. The reflex responses relative to the anticipatory responses were smaller for the arm muscles than for the jaw muscles. The reflex responses in the arm muscles were the same with unexpected and expected perturbations, whereas anticipation increased the reflex responses in the jaw muscles. Biceps brachii and triceps brachii showed similar sensory-induced responses and similar anticipatory responses. Jaw muscles differed, however, in that the reflex response was stronger in masseter than in digastric. It was concluded that reflex responses in the arm muscles cannot overcome the loading of the arm adequately, which is compensated by a large centrally programmed response when loading is predictable. The jaw muscles, particularly the jaw-closing muscles, tend to respond mainly through reflex loops, even when loading of the jaw is anticipated. The differences between the responses of the arm and the jaw muscles may be related to physical differences. For example, the jaw was decelerated more strongly by the load than the heavier arm. The jaw was decelerated strongly but briefly, <30 ms during jaw closing, indicating that muscle force increased before the onset of reflex activity. Apparently, the force-velocity properties of the jaw muscles have a stabilizing effect on the jaw and have this effect before sensory induced responses occur. The symmetrical responses in biceps and triceps indicate similar motor control of both arm muscles. The differences in reflex activity between masseter and digastric muscle indicate fundamental differences in sensory feedback to the jaw-closing muscle and jaw-opening muscle.


    INTRODUCTION
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

When jaw closing is counteracted by the appearance of a smoothly increasing spring-like load, the muscle activity developed to overcome this resistance has two components: preprogrammed muscle activity (when the resistance is anticipated) and reflex muscle activity (generated by a feedback loop) (Ottenhoff et al. 1992). These authors found that reflex activity was greater when the resistance (loading) was anticipated than when it was unexpected and was always greater than the preprogrammed activity. They concluded that the muscle activity needed to overcome resistance to jaw closure was generated by feedback loops rather than by preprogrammed activity in anticipation of the resistance.

Further studies showed there to be marked differences between the masseter muscle (jaw-closing muscle) and the digastric muscle (jaw-opening muscle) in the sensory-induced muscle activity needed to overcome the resistance to jaw closing and opening (Abbink et al. 1998). In both muscles, an initial reflex was observed ~25 ms after the onset of loading, but the second phase of sensory induced muscle activity started 75 ms earlier in the masseter muscle than in the digastric muscle. Furthermore the ratio between reflex activity and voluntary (background) activity, observed between 20 and 120 ms after loading, was on average four times higher in the masseter muscle than in the digastric muscle. This difference in sensory facilitation indicates that the masseter muscle is better equipped than the digastric muscle to overcome sudden disturbances of jaw movement and this may be related to the fact that the digastric muscle does not contain muscle spindles (Kubota and Masegi 1977; Voss 1956). The masseter muscle contains many spindles, which play an important role in peripheral feedback to this muscle. Slow, ramp-like stretching of human masseter muscle induces short- and long-latency reflexes that are probably due to spindle activity because blockade of the receptors around the teeth does not affect these reflexes (Poliakov and Miles 1994).

If the asymmetry in the presence of muscle spindles contributes to the asymmetry of the reflex response, then one would expect a more symmetric response in antagonistic muscle pairs that both contain muscle spindles. To investigate this, we examined the activity of two antagonist muscles in the arm, the main flexor and extensor muscles of the elbow joint. Stretching of these muscles, both of which contain muscle spindles, elicits spinal reflexes (biceps: Hammond 1960, Marsden et al. 1976; triceps: Tarkka 1986). These muscles also show anticipatory activity (Dietz et al. 1980; Lacquaniti and Maioli 1989). In many of these studies, the arm was held still during the experiment, and the perturbations were fairly strong, for example, caused by catching a ball dropped from a height or by landing from a forward fall. In experiments in which the perturbation occurred during movement of the arm, the movement rate was often high and the perturbations transient (Bennet 1993; Smeets et al. 1990).

The aim of this study was to investigate the response of the arm muscles to sudden loading during rhythmic movements. Because we wanted to compare the results for biceps/triceps with those for masseter/digastric, loading of the arm muscles had to resemble that of the jaw muscles. To this end, the flexion/extension movement of the arm was counteracted by a spring-like external load that depended on arm position in a similar way as the loading of the jaw muscles depended on the position of the jaw. The load was applied during relatively slow, rhythmic flexion-extension movements of the lower arm at the same rate, 1 Hz, as the opening-closing movements of the jaw. Biceps and triceps were loaded in separate experiments and in a symmetrical way, that is, the external load that counteracted flexion and extension had identical spring-like characteristics and magnitude but in opposite directions.


    METHODS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Arm experiments

Eight healthy human volunteers aged between 22 and 50 yr participated in this study, which was approved by the ethics committee of Utrecht University. The subject was seated upright alongside a table (Fig. 1, left). The upper part of the right arm was held parallel to the body, and the elbow was supported by a cushioned rest attached to the table. The lower part of the right arm was perpendicular to the upper arm, parallel to the surface of the table, and in the supine position, the palm of the hand pointing up. The wrist was strapped with adhesive tape to one end of a lever that allowed movement up and down by flexion and extension of the arm. The other side of the lever was connected to a coil that could move freely up and down in a permanent and uniform magnetic field. By varying the electrical current through the coil the force on the lever, and thus on the wrist of the subject, could be varied. The purpose of the lever was to amplify the movement range of the coil, ~4 cm, to 9 cm wrist movement, which is equivalent to a rotation about the elbow of ~20 degrees. Lever movement was confined by two rods rigidly connected to the table to ensure that the coil remained within the range of the uniform magnetic field. By generating a constant current through the coil, a force was applied that compensated the weight of the arm so that the lower arm could be kept floating horizontally without activity of the arm muscles. The magnet-coil system, which also was used in the experiments with the jaw, has been described in detail in a previous paper (Ottenhoff et al. 1994).



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Fig. 1. Experimental setups for loading of arm muscles (left) and jaw muscles (right). Same magnet-coil system was used in both set-ups.

An infrared light-emitting diode (LED) was attached to the lever so that it followed the movement of the wrist. A second, reference LED was attached to the table. The positions of the LEDs were recorded by means of an optical motion analysis system (Northern Digital Optotrak) that sampled the LEDs at 500 Hz. Wrist position was obtained by subtracting the information about the vertical position of the LEDs. The wrist position was used as a parameter in some movement cycles to control a time-varying, spring-like force counteracting wrist movement. Loading was adjusted between samples, so that the delay of the feedback loop between wrist position and the counteracting load was 2 ms.

The load counteracted movement in one direction only, i.e., only during flexion of the arm or only during extension of the arm. Figure 2A depicts the relationship between wrist position and a load that counteracts flexion of the arm. Loading started when the wrist reached a preset position, denoted as "start," in the early part of the flexion movement, ~2 cm away from the lower rod and increased smoothly until it reached a maximum, 30 N, at a second preset position, denoted as "stop," just before the lever reached the upper rod. Loading was applied in the form of a spring-like force, simulated by computer-controlled feedback. Between the start and stop wrist positions the load is described by the equation: external force = 30 × (position - start)/(stop - start) N. This means that a spring stiffness of 30/(stop - start) N/m was introduced when the wrist position reached the start level. The zero point of the spring was at the start level, so that no force transient occurred. After reaching the stop position, the maximum load was maintained for 120 ms and then was released smoothly during 60 ms while the arm was still flexed and before it started to extend. Similarly, a load could be applied to counteract extension of the arm. The start and stop levels then were reverse with respect to the central wrist position.



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Fig. 2. A: flexion of the arm is counteracted by an external load. Top: position of the wrist as a function of time. At a particular position (dotted horizontal line labeled start) the load (middle) started and increased proportionally to the decrease in distance to another preset level (dotted line labeled stop) at which the load reached its maximum of 30 N. Load remained at 30 N for 120 ms, and it then decreased over 60 ms. Bottom: activity of biceps brachii. B: experimental protocol: sequences of nonloaded movements are alternated with sequences of loaded movements. Transitions between the sequences were recorded (dotted lines).

The subject was instructed to move the wrist rhythmically up and down, with flexion or extension being maximal, lever resting against the rod, before the opposite movement was started. The frequency of the movements was 50 flexion-extension cycles per minute, controlled by a metronome. In the first half of the session, loading was applied to counteract flexion. Sequences of nonloaded movement cycles were alternated with sequences of movements in which the load was applied (Fig. 2B). The number of movement cycles in each sequence varied randomly between 11 and 18. The aim was to prevent the subject from being able to predict when the changes between the sequences would occur. Although subjects were allowed to pause to relax the arm, most subjects could maintain the movement rate for 18-20 min making 900-1,000 consecutive flexion/extension cycles. Thirty changes were recorded in which the load appeared (Fig. 2B, I) and 30 in which it no longer appeared (Fig. 2B, II).

In the second half of the session, loading was adjusted to counteract extension of the arm. Again 900-1,000 consecutive flexion/extension cycles were made and the changes were recorded between the loaded and nonloaded sequences.

Jaw experiments

The jaw experiments have been described in detail earlier (Abbink et al. 1998). Only an outline of the method will be given here. Eight subjects participated in the jaw-closing experiments, four of whom also participated in the experiments with loading of jaw opening. In brief, the subjects opened and closed their jaws at a rate of 60 movement cycles per minute, controlled by a metronome. In the jaw-closing phase, or in the jaw-opening phase in the other experiments, a smoothly increasing external load could be applied that counteracted jaw movement. The load was supplied by the same computer-controlled magnet-coil system used in the arm experiments (Fig. 1, right). The coil was attached to the subject's mandible by means of a dental plate made of orthodontic acrylic resin (Vertex Orthoplast) that was fitted individually on the subject's teeth. A second dental plate connected the teeth of the upper jaw to an earth-fixed rod to prevent movement of the head. The residual space between the dental plates and the teeth was filled with dental impression material (Impregum) to create a vacuum that held the dental plate in place. When the jaw closed, the flat outer surfaces of the dental plates covering the lower and upper teeth made parallel contact at ~5 mm distance from maximum intercuspation, as measured at the first premolars.

The coil was connected to a vertical rod, which was connected at the lower end by a ball joint to a 12-cm-wide fork. This fork was attached to two round rods protruding sideways from the dental plate on the mandible at the first premolars. The purpose of this construction was to distribute the load over the left and right part of the mandible. The two rods formed an axis around which the lower jaw could rotate freely forward and backward to prevent torque round this axis.

The loading of the mandible was applied in the form of a smoothly increasing spring-like force, as it was in the arm experiments (Fig. 2A). The load counteracting jaw closing increased to 25 N, which could be overcome easily by all subjects. In the jaw-opening experiments the load increased to 10 N instead of 25 N, which reflects the relative weakness of the digastric muscle compared with the jaw-closing muscles. As in the arm experiments, sequences of loaded movement cycles were randomly alternated with sequences of nonloaded movements. The cycles around the changes between the sequences were recorded (Fig. 2B). Thirty changes were recorded during which the load appeared and 30 during which the load no longer appeared.

Electromyography

Electrical activity in the flexor muscle (biceps brachii, caput breve) and the extensor muscle (triceps brachii, caput laterale) was recorded by means of bipolar surface electrodes (diameter 12 mm and interelectrode distance 22 mm). An electrode on the back of the hand served as a reference. Similar electrodes were used to record the electrical activity of the jaw-closing muscles (masseter and temporalis) and the jaw-opening muscle (digastric). The signals were amplified (bandwidth 10-800 Hz), rectified, and smoothed (low-pass 35 Hz) by a linear-phase-shift Paynter filter (Gottlieb and Agarwal 1970). The electromyographic (EMG) signals, external load, and wrist position were all sampled at 500 Hz.

Signal averaging

For each subject, ensemble averages were computed for the 30 records of the changes in which loading appeared and for the 30 records in which loading no longer appeared. The position (arm or jaw) and EMG signals were averaged, taking in each cycle the load trigger point as the reference for synchronization. The load trigger point is the point during the movement cycle at which the position crossed the start level in the appropriate direction, triggering the load in about half of the cycles. The averaged signals were used to compute EMG parameters per muscle and per subject. For graphic presentation, group averages were computed.

Normalization of muscle activity

To be able to compare the results of different muscles and different subjects, the activity of each individual muscle was normalized against the activity in the last cycle (average of 30 records) in which the muscle was loaded, before the change to cycles in which the external load was no longer applied (Fig. 3). This cycle followed >= 10 cycles in which the muscle was loaded, during which the EMG of the muscle had stabilized to a constant pattern. In the averaged movement signal, the points were determined at which 5 and 95% of the distance had been covered in the movement phase in which the load was applied. The mean EMG amplitude in that interval was computed and the EMG signal was divided by this value.



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Fig. 3. Muscle activity was normalized using the results obtained at the end of series of movement cycles (>10) in which the muscle was loaded (middle). Example shows the results in 1 subject when flexion of the arm was counteracted (average of 30 records). Average electromyogram (EMG) of biceps during the middle 90% of the flexion movement () was used for normalization. Activity of triceps was normalized by using results from the experiments in which extension of the arm was counteracted.

Additional muscle activity

The muscle activity in the nonloaded cycle before loading appeared was regarded as the basal muscle activity needed for moving the arm or jaw. It was assumed that in this cycle the subject did not anticipate loading because this cycle followed >= 10 other nonloaded cycles. Additional muscle activity was generated when the load was applied or when the subject expected the load to be applied. To obtain the additional muscle activity, the basal muscle activity was subtracted point by point from the muscle activity in the other cycles using the load trigger point as the reference.


    RESULTS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Loading is applied

Figures 4 (arm) and 5 (jaw) show what happened when nonloaded movement cycles changed to loaded movement cycles. Each trace represents the average of eight subjects, 30 recordings per subject. The results for loading of the opposite movement are shown in the same plots to enable direct comparison of the movement trajectories and the additional muscle activity generated by antagonist muscles. In the jaw-closing experiments the activity of the right masseter muscle is shown; all jaw-closing muscles (left and right masseter and temporalis) showed similar patterns of muscle activity.



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Fig. 4. Arm movement was counteracted by loading. Thick lines: load against flexion of the arm, response of biceps. Thin lines: load against extension of the arm, response of triceps. Averaged results from 8 subjects, 30 recordings per subject. In the 1st cycle movement of the arm was still not loaded. In the following cycles loading was applied. Load trigger points are indicated by dashed vertical lines. Dotted vertical lines indicate 120 ms after loading. Top and middle: position and velocity of the wrist. Bottom: additional muscle activity generated to overcome the load.



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Fig. 5. Jaw movement was counteracted by loading. Averaged results from 8 subjects, 30 recordings per subject. Thick lines: load against jaw closing, response of masseter. Thin lines: load against jaw opening, response of digastric muscle. Same format as Fig. 4.

When the movements were not counteracted by loading, muscle activity stabilized to identical bursts of low activity. It was assumed that loading was not expected and that no anticipatory additional muscle activity was generated (Figs. 4 and 5, left). Peripherally induced additional muscle activity was not generated as the movement was not perturbed by loading. The muscle activity in this cycle was defined as the basal muscle activity needed for moving the arm or jaw.

In the next cycle suddenly the spring-like loading was applied (Figs. 4 and 5, middle). Movement of the wrist or the jaw was slowed down, indicated by inflection of the movement signals. In the arm experiments, the direction of arm movement was reversed temporarily with most subjects starting ~100 ms after the onset of loading. The response of the agonist arm muscle, that started 60-70 ms after the onset of the load, resulted in continuation of movement in the intended direction. In the experiments on the jaw, a fairly sharp inflection of jaw movement was observed after the onset of loading, but neither jaw closing nor jaw opening was halted. The velocity of the jaw dropped sharply, but stabilized within 30 ms after loading. Additional activity of the jaw muscle appeared after ~25 ms. In the masseter muscle, the reflex response, generated within 120 ms of loading, was stronger than in the digastric muscle (Fig. 5; Fig. 9, sensory-induced, force not expected).

In the next movement cycle (Figs. 4 and 5, right), loading was anticipated, and in all muscles additional muscle activity was observed before loading started. In all experiments, movement velocity was higher than in the preceding cycle. The movement of the arm was no longer reversed by the load.

Loading is removed

Figures 6 and 7 show what happened when loaded movement cycles changed to nonloaded movement cycles. Each trace is the average of eight subjects, 30 recordings per subject. The left columns show the muscle response when the movement was still counteracted by loading. Muscle activity had stabilized to identical bursts of increased activity compared with the activity of nonloaded movements. Note that the results in this cycle closely resemble the results when the load was applied for the second consecutive time (Figs. 4 and 5, right). The additional muscle activity consisted of anticipatory activity, which started before the onset of the load, and sensory-induced activity, which started after loading.



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Fig. 6. Load counteracting arm movement is unexpectedly no longer applied. In the 1st cycle, the arm was still loaded. Same format as Fig. 4.



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Fig. 7. Load counteracting jaw movement is unexpectedly no longer applied. Same format as Fig. 4.

When the load no longer appeared (Figs. 6 and 7, middle), the movement was no longer perturbed. Additional muscle activity was still generated, which indicates that loading was still expected. Biceps and triceps showed similar patterns of anticipatory additional muscle activity, which gradually increased until the mechanical stop was reached 120-130 ms after the load trigger point. Subsequently activity of the arm muscles decreased. The masseter and the digastric muscle also showed similar patterns of additional muscle activity. Clenching activity was observed in the masseter muscle after the dental plates made contact and were pressed together.

In the next cycle, the absence of loading was anticipated. The anticipatory muscle response had largely disappeared, and the normal "nonloaded" movement pattern was restored. Note that the muscle activity closely resembled that measured when movement was not loaded for eleven or more consecutive cycles (Figs. 4 and 5, left).

Sensory-induced and anticipatory responses

Figure 8 shows the anticipatory and sensory-induced responses in all four muscles during the change from loaded to nonloaded movements. In the cycle during which loading still occurred (Fig. 8, left), the muscle response consisted of anticipatory activity (hatched area), which started before loading, and sensory-induced activity (black area), which started after the onset of loading. The thin lines show the sensory-induced muscle activity obtained by subtracting the activity observed the next cycle, when the muscle was no longer loaded (Fig. 8, middle), from the activity in this cycle. This subtraction was based on the assumption that in the next cycle the same anticipatory EMG activity would be generated because loading was anticipated, whereas the sensory-induced EMG was absent because the movement was not loaded. The muscle responses to the external loading could only be evaluated <= 120 ms after the trigger point because thereafter the nonloaded movements, except jaw opening, reached the mechanical stop, resulting in brief, monosynaptic reflexes (not clearly visible in the averaged signals due to the lack of synchronization with respect to the load trigger that served as the reference for averaging). The sensory-induced responses before 120 ms after loading can be regarded as reflex activity. The latency of voluntary jaw muscle activity, for example, is ~120 ms (Ottenhoff et al. 1992).



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Fig. 8. Additional muscle activity (ama) generated by arm and jaw muscles during the change from loaded to nonloaded movements. Hatched areas indicate the anticipatory responses observed until 120 ms after the load trigger point. Black areas indicate reflex responses generated between 20 and 120 ms after loading.

Figure 9 shows the average muscle responses (anticipatory and sensory-induced) between 20 and 120 ms after loading. It also shows the sensory-induced muscle activity in that interval when loading was applied unexpectedly (Figs. 4 and 5, middle). Tables 1 and 2 list the muscle responses, each the average of 30 repetitions, recorded in individual subjects.



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Fig. 9. Anticipatory and sensory-induced responses of arm and jaw muscles, generated between 20 and 120 ms after loading. Each bar shows the average for 8 subjects and standard error of the mean.


                              
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Table 1. Responses in biceps and triceps 20-120 ms after the onset of loading


                              
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Table 2. Responses in masseter and digastric muscle 20-120 ms after the onset of loading

Both arm muscles showed similar patterns of anticipatory and sensory-induced muscle activity (Fig. 8, rows 1 and 2). Reflex activity was generated in the arm muscles ~60-70 ms after loading, and its magnitude was similar to that recorded after unexpected loading (Fig. 9; Table 1). A large anticipatory response was generated in the arm muscles, starting ~200 ms before loading. The strong anticipatory arm-muscle response was observed in all subjects.

The sensory induced responses recorded in the jaw muscles started ~25 ms after loading. Reflex activity, generated between 20 and 120 ms after loading, was larger when loading was anticipated than when it was unexpected (Fig. 8, rows 3 and 4; Fig. 9, Table 2). The sensory-induced response of the jaw muscles consisted of two phases, as compared with one phase in the arm muscles, and the patterns were not symmetrical. In the masseter muscle, the initial reflex burst of muscle activity was shorter and steeper and the subsequent increase in muscle activity appeared sooner in the masseter muscle than in the digastric muscle (Abbink et al. 1998). Anticipatory additional activity of the jaw muscles started ~100 ms before the loading. The anticipatory responses in the jaw muscles varied strongly between subjects. In some subjects, the anticipatory response exceeded the reflex response, in others there was no anticipatory response.


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The results showed that arm and jaw muscles respond differently to loading. In the arm muscles, there was little reflex activity but a large anticipatory response. In the jaw muscles, stronger reflex responses were observed than in the arm muscles particularly in the jaw-closing masseter muscle. Biceps and triceps showed symmetrical responses, of anticipatory as well as of sensory origin, to external loading. Masseter and digastric muscle, however, showed different patterns of sensory-induced muscle activity. These differences may be related to physical and functional differences between the arm and the jaw.

Sensory-induced responses

Identical patterns of sensory-induced muscle activity were observed in biceps and triceps, starting 60-70 ms after loading. The short-latency reflex, 20-30 ms, described by Hammond (1960) and Dietz et al. (1981) was absent. They suggested that the sensory-induced response of arm muscles depended on the motor task and also on the kind of disturbance imposed on the muscle. In the experiments of Hammond (1960) on the stretch response of biceps brachii, the speed of the imposed length change was ~80°/s angular velocity of the elbow joint, and the stretch reflex was small in comparison with the late response. Dietz et al. (1981) investigated the stretch reflex in triceps brachii during landing from forward falls with angular velocities of the elbow joint that were ten times higher, <= 800°/s, and observed stretch responses that were large in comparison with the late response. In these studies, the arms were held still until the perturbation stretched the muscles. In our experiments, the muscle was loaded when it was shortening. The arm muscles were stretched only when loading occurred unexpectedly, and even then the arm decelerated slowly and muscle stretch started only 100 ms after loading. By this time, sensory-induced muscle activity, latency 60-70 ms, already had started.

A reflex with a latency of 25 ms can occur in biceps even when loading does not stretch the muscle but only slows its shortening. This has been shown in experiments with imposed position errors during voluntary flexion of the arm (Bennet et al. 1993), in which the arm was slowed at >50 rad/s2 angular deceleration of the elbow joint, ~20 ms after the onset of the perturbation. In our experiments, the perturbation of arm movement was fairly weak. This is shown in Fig. 10, in which the perturbation of arm flexion is compared with that of jaw closing. The movement signals have been transformed into muscle shortening in centimeters using a scale factor. For biceps, this factor was estimated as 0.2, assuming that the distance of the elbow rotation axis to the tendon insertion on the radius is 5-6 cm, and ~28 cm to the wrist. The perturbation of triceps was analogous to that of biceps, as the flexion and extension movements were symmetrical. After the external load started to counteract flexion of the arm, the velocity of biceps shortening (Fig. 10, row 2) decreased gradually until ~150 ms after loading. The maximum deceleration, ~60 cm/s2 (Fig. 10, row 3), corresponds to ~12 rad/s2 angular deceleration of the elbow joint and was reached only 80 ms after loading. This is a weaker perturbation than the 50 rad/s2 reached at 20 ms in the experiments of Bennet et al. (1993) that resulted in a short-latency reflex. The absence of the short-latency reflex in our arm experiments probably is related to insufficient excitation of arm-muscle spindles by the relatively small deceleration of arm-muscle shortening. The same sensory-induced response was observed with expected and unexpected loading. This suggests that, under our experimental conditions with small deceleration of arm movement by the external loading, anticipation of loading did not alter peripheral feedback to the arm muscles.



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Fig. 10. Muscle shortening, velocity and acceleration of muscle shortening observed in biceps brachii and masseter after application of a load to flexion of the arm and jaw closing. Bottom: responses of these muscles to overcome the load.

In contrast to the arm muscles, the jaw muscles showed a short-latency reflex, which started 20-25 ms after loading, followed by a longer latency reflex. The important role of reflex activity in the control of jaw movement is underlined by the increase in reflex activity when loading was anticipated as compared with when it was not expected (Fig. 9). This increase could not be explained by the increase in background activity and probably was caused in part by an increase in the gain of the reflex loops (Abbink et al. 1998). The presence of the short-latency response in the jaw muscles may be related to the relatively strong deceleration of jaw movement. Figure 10 shows the perturbation of the masseter muscle. The movement signals have been transformed into muscle shortening using a scale factor of 0.5, assuming that the insertion of the masseter on the mandible is approximately halfway the premolars and the mandibular joint. After loading, the velocity of masseter shortening decreased rapidly but briefly. The masseter muscle was not stretched. The maximum deceleration of masseter shortening, ~150 cm/s2, was three times higher than in biceps and lasted only for ~30 ms, whereas the deceleration of biceps shortening lasted until 150 ms.

The responses of the jaw-closing and jaw-opening muscles were not symmetrical as they were in the arm muscles. In the masseter, the initial reflex burst was shorter and steeper and the second, continuous increase occurred sooner in the masseter muscle than in the digastric muscle (Abbink et al. 1998). Reflex activity, relative to the anticipatory response, was much greater in the masseter muscle than in the digastric muscle (Fig. 9). Also the changes in the jaw-closing and jaw-opening movements were not as symmetric as in the arm experiments. The maximum deceleration of the jaw-opening movement (measured at the first premolars) was approximately the same as when jaw closing was perturbed, but it was reached later, 25 ms after loading, compared with 15 ms in the jaw-closing experiments. However, despite the 2.5-times greater load counteracting jaw closing, the duration of jaw deceleration was shorter in the jaw-closing experiments than in the jaw-opening experiments and the decrease in jaw velocity (Fig. 5, middle, and 3; Fig. 7, left) was smaller. The jaw appears to be more resistant to forces counteracting jaw closing than to forces counteracting jaw opening, which probably reflects the greater strength of the jaw-closing muscles and the greater sensitivity of these muscles to perturbation of the jaw-closing movement. These results indicate that the control of muscle activity is fundamentally different in the masseter muscle and the digastric muscle: the masseter appears better able to generate additional muscle activity through short-latency feedback loops. This difference may be related to the fact that the digastric muscle does not contain muscle spindles whereas the masseter muscle contains many spindles.

Poliakov and Miles (1994) showed that slow, ramp-like stretches of the masseter evoked a brief short-latency excitation with a latency of ~10-12 ms, followed by a longer-latency response at 35-40 ms. The reflexes that they observed probably were mediated by muscle spindles because blockade of activation of mechanoreceptors around the teeth hardly affected the responses. In our experiments, the latency of the reflex in the masseter was 20-25 ms. The 10- to 15-ms difference was not an artifact caused by the low-pass filtering because such filtering preserved the leading edges of the EMG bursts. In earlier experiments at our department in which a brief and transient load pulse was superimposed on a gradually increasing load, a monosynaptic jaw-jerk reflex was observed in the masseter muscle 10 ms after the onset of the load pulse (van der Bilt et al. 1997). In our jaw-closing experiments with only the gradually increasing load, the perturbation was probably too weak to induce the monosynaptic jaw-jerk reflex. Nevertheless, it may well be that the reflexes in the masseter that we observed were mediated by spindles despite the fact that the muscle was not stretched. Because of alpha -gamma coactivation, the muscle spindles shorten together with the extrafusal muscle, allowing spindle firing during shortening of the muscle and enhancement of spindle firing when muscle shortening is slowed down (Murphy and Martin 1993; Taylor and Appenteng 1981). Studies in which the mechanoreceptors around the teeth are blocked may give more insight into this matter.

An important factor contributing to the difference in muscle activity in response to loading between the arm and the jaw is the fact that the arm/lever/coil system has more mass than the jaw/dental plate/coil system. A larger load would be needed to decelerate arm-muscle shortening to a similar extent as jaw-muscle shortening. However, despite the relatively smaller load, the arm movement eventually was perturbed more than the jaw movement. When loading was unexpected, arm movement was even reversed. The short duration of jaw deceleration, particularly during jaw closing (<30 ms), indicates that jaw-muscle force increased before reflex activity started (±25 ms). Apparently, properties of the jaw muscles that are not detected by EMG play a role in the development of muscle force to resist loading. The force-velocity properties of muscle, for example, predict that muscle activation results in more muscle force at lower shortening velocities. This may result in an increase in jaw-muscle force when shortening of the muscles is slowed down by the external loading. Experiments with sudden unloading of the jaw muscles during clenching showed a similar phenomenon: muscle force decreased so rapidly that it could not be the result of neural control and can only be explained by the force-velocity properties of the jaw muscles (Nagashima et al. 1997; Slager et al. 1997).

Anticipatory responses

When the load could be expected, because it had appeared in the preceding cycle, the arm muscles showed an anticipatory response that started ~200 ms before loading. When loading suddenly did not occur, after 11-18 loaded movements, the arm muscles still showed this anticipatory response, which was sustained during the entire movement despite the lack of loading (Fig. 8). Apparently the response was under open-loop control, preprogrammed by the CNS based on knowledge about the anticipated load. The strong anticipatory arm-muscle response was observed in all subjects. This indicates that sensory-induced responses could not overcome the load adequately. Only a preprogrammed response, starting before expected loading, could avoid the strong perturbation of arm movement observed when loading occurred unexpectedly.

Centrally programmed, anticipatory responses also were observed in the jaw muscles, but they started later, ~100 ms before anticipated loading. Contrary to what was observed in the arm muscles, the anticipatory jaw-muscle responses were not large compared with the sensory-induced responses. In some subjects, no anticipatory jaw-muscle response was observed at all. This indicates that the jaw muscles tend to overcome loading through sensory-induced muscle responses rather than through preprogrammed muscle responses.

Flexion or extension of the arm, when it is loaded by the appearance of a smoothly increasing spring-like force as applied in our experiments, cannot be stabilized as well as opening or closing of the jaw, counteracted by a similar spring-like load. This may be because there was no early reflex component in arm-muscle activity. Because of the relatively large mass of the arm compared with that of the jaw, loading of the arm may be too slow to excite enough muscle spindles needed to generate short-latency reflex activity. Consequently, when loading is anticipated, the arm muscles adopt a strategy to overcome the load in a largely feedforward manner. Motor control appears to be symmetrical in biceps and triceps, reflecting the symmetrical distribution of proprioceptors and the symmetry between the muscles in physical size, position and attachment with respect to the elbow joint.

In the experiments on the jaw, loading resulted in faster perturbations than in the arm experiments because the jaw is lighter than the arm. Sensory-induced activity of the jaw muscles has a shorter latency (20-25 vs. 60-70 ms in the arm) and, relative to the anticipatory response, more reflex activity is generated than in the arm muscles. The combination of small mass and strong muscles means that the muscle response to overcome resistance of jaw movements, especially jaw closing, is controlled for a large part by short-latency reflexes. The force-velocity properties of the jaw muscles probably have a stabilizing effect on the jaw and have this effect before sensory induced responses occur. The patterns of sensory-induced activity in the masseter and digastric muscle were not symmetric, indicating fundamental differences in motor control. This difference reflects the asymmetry in the presence of proprioceptors between jaw-closing and -opening muscles. It also reflects the physical and functional differences between the two muscle groups. The jaw-closing muscles are stronger than the jaw-opening muscles because they are specialized in overcoming the resistance of food during chewing.


    ACKNOWLEDGMENTS

This work was supported by the Faculty of Medicine of the Utrecht University and the Netherlands Institute for Dental Sciences.


    FOOTNOTES

Address for reprint requests: J. H. Abbink, Dept. of Oral Pathophysiology, PO Box 80.037, 3508 TA Utrecht, The Netherlands.

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received 6 July 1998; accepted in final form 17 May 1999.


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ABSTRACT
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0022-3077/99 $5.00 Copyright © 1999 The American Physiological Society