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Center for Sensory-Motor Interaction, Department of Health Science and Technology, Aalborg University, Aalborg, Denmark
Submitted 14 February 2005; accepted in final form 22 January 2006
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSREFERENCES |
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). In the lower extremity, the sensitivity of the central part of the stretch reflex arc has been studied during various cyclic motor tasks (i.e., walking, running, pedaling, and hopping) primarily in soleus by application of the H-reflex technique (Boorman et al. 1992; Crenna and Frigo 1987; Voigt et al. 1998). However, the behavior of the quadriceps H-reflex during cyclic movements has not been object of much attention, and to our knowledge, it has only been studied during the first part of the stance phase during walking (Dietz et al. 1990). The reason is most likely that the H-reflex is technically more difficult to evoke and to process in quadriceps than in the soleus muscle or the flexor carpi radialis muscle (Zehr et al. 2003). Searching for the optimal position and reliable fixation of the stimulating electrode during movements make studies of the quadriceps H-reflex nontrivial during movements. Furthermore, the quadriceps muscle is situated close to its motor neuron pool in the spinal cord and consequently, because of the short reflex delay, there is an overlap between the M- and the H-waves even at relatively low stimulation intensities. Therefore the quantification of the H-reflex magnitude may be contaminated by the M-wave, and a dedicated recording and analysis procedure should be applied to obtain reliable quadriceps recordings during movement.
Studies of the soleus H-reflex have focused on the description of the phase dependent modulation during different forms of motor tasks as indicated above and on the influences of speed of movement on the reflex level or gain (Edamura et al. 1991; Simonsen and Dyhre-Poulsen 1999). Furthermore, a task-dependent decrease in the reflex level or gain from tonic activation to movement has been reported in soleus in several studies (Capaday and Stein 1986; Morin et al.1982). Whether the behavior of the H-reflex in quadriceps during cyclic movements corresponds to that of the soleus H-reflex and whether the task- and speed-dependent influences shown for the soleus H-reflex are similar in quadriceps remain to be shown.
Consequently, this study has two aims: 1) to compare the basic behavior of the H-reflex in the quadriceps muscle such as phase-dependent reflex modulation and sensitivity to changes in movement speed and in motor task, respectively, with the behavior that previously has been shown for soleus during pedaling, and to achieve this, 2) to develop an optimized H-reflex recording and processing procedure for recording of quadriceps H-reflexes during movement.
During pedaling movements, the magnitude of the mechanical work generated by the quadriceps muscle, and consequently, the general quadriceps activation level is relatively high in comparison to the situation during walking (Broker and Gregor 1994; Eng and Winter 1995). Therefore from a functional point of view, we chose pedaling as a model for study of the behavior of the quadriceps H-reflex during rhythmical alternating leg movements. The pedaling test was repeated at two different movement speeds (pedaling frequencies) at a constant workload and motor recruitment level to assess possible speed-dependent influences on the quadriceps H-reflex. The kinematics and kinetics of the legs during the pedaling tasks was quantified to specify the movement properties of each task. Finally, the operationally defined H-reflex gain function was compared between pedaling and tonic muscle activation during sitting to evaluate a possible task related influence on the quadriceps H-reflex.
In accordance with previous results obtained from the soleus muscle (Brooke et al. 1992; Larsen and Voigt 2004), it was hypothesized that the quadriceps H-reflex gain would decrease with an increase in speed of movement and that there would be a task dependent decrease in the quadriceps H-reflex gain between the tonic condition during sitting and pedaling.
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METHODS |
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Sixteen healthy subjects participated in the study [12 male and 4 female; age between 21 and 43 yr; height 174 ± 9.1 (SD) cm; weight: 71 ± 10.1 (SD) kg]. All subjects gave their informed consent before participating in the experiments. The experiments were approved by the local ethical committee and conducted in conformity with the Declaration of Helsinki.
Experimental protocol
PEDALING. Nine subjects participated in this part of the experiment. After preparation of the subject, an H-reflex excitability curve was recorded from the quadriceps of the right leg during relaxed sitting in a chair. Before pedaling, handlebar and seat position on the bicycle ergometer were adjusted according to the comfort of each subject. Subsequently, the subjects performed the following two tests: pedaling at a speed of 40 rpm, crank load of 5.1 Nm— corresponding to an exercise intensity of 80 W; and pedaling at a speed of 80 rpm, crank load 2.6 Nm—corresponding to an exercise intensity of 80 W.
Before each series of H-reflex measurements was initiated, the subjects practiced 4–6 min to warm-up and to get accustomed to the specific movement speed and crank load. At the end of this period EMGs from vastus lateralis (VL) and medialis (VM), rectus femoris (RF), biceps femoris (BF), soleus (SOL), and tibialis anterior (TA), crank angle, pedal angles, and pedal reaction forces were recorded continuously over a period of 20 s for characterization of the specific movement situation with respect to muscle activation pattern, kinematics, and kinetics. Subsequently, the modulation of the quadriceps H-reflex was recorded. The sequence of the two pedaling tests was randomized by tossing a coin. About 20 min of constant pedaling was required in each test situation to record the H-reflex modulation, and an adequate rest period was allowed between tests to avoid fatigue during the experiment. To ensure constant pedaling frequency, the subjects were asked to follow the rhythm generated by an electronic metronome, and additionally, visual feedback on the pedaling frequency was presented. Finally, reflective markers were placed on trochanter major, epicondylus lateralis, malleolus lateralis, and the center of the crank, and a digital sagittal plane photo was taken of the subject sitting in a fixed position on the bicycle. The photo was used for measurement of the segment lengths, the foot angle in relation to pedal surface, and the position of the hip joint center in relation to the crank center of rotation.
SITTING. The excitability of the quadriceps H-reflex in relation to tonic muscle activation level during isometric conditions was additionally measured in seven subjects during sitting. H-reflex excitability curves were recorded simultaneously from the quadriceps heads (VL, VM, and RF), and recordings were repeated in random order at five different quadriceps activation levels between 10 and 50% maximum activation. Adequate rest periods were required in between tests to avoid muscle fatigue.
Instrumentation and recording procedures
BICYCLE ERGOMETER.
An instrumented Monark bicycle ergometer (model 90824E) was used on which the angular orientation of the crank arms and the pedal surfaces were measured with optical encoders. The pedals were instrumented with force transducers according to the guidelines presented by Broker and Gregor (1990) for measurement of the pedal reaction forces. The subjects wore bicycle shoes with a standard clip-less Shimano SPD foot-shoe interface for fixation of the feet to the pedals. For visual feedback concerning the pedaling frequency, a so-called bicycle computer (Cateye) was mounted on the ergometer.
EMG RECORDING PROCEDURES.
Pairs of surface electrodes (Neuroline, Medicotest 720-01-K, sensory area of 7 mm2) were used to record EMG of the selected muscles of the right leg. The electrodes of the three quadriceps heads were placed 2 cm apart according to the recommendations presented by Garland et al. (1994) regarding optimal mono- and bipolar registration of quadriceps H-reflexes. On BF and TA, the electrodes were placed 2 cm apart on the thickest part of the muscle belly with the line between the electrode centers parallel with the muscle fibers. On soleus, the electrodes were placed 2 cm apart vertically in the mid-dorsal line, 
4 cm distal to the point, where the two heads of m. gastrocnemius join the Achilles tendon. A reference electrode (PALS Flex 896230) was placed medially over the middle of tibia, and electrodes and cables were attached to the leg with tape and an elastic tube bandage. The EMG signals were preamplified (100 times) with custom build preamplifiers, led through long cables to an amplifier (Axon, CyberAmp 380), and amplified again (10 times;(total amplification, 1,000 times).
DATA ACQUISITION. EMG, position, and force signals were acquired with a custom-made PC-based data acquisition system (Humaniac by Knud Larsen, SMI, using an Amplicon A/D-board PC226 and Labview). During the recording of EMGs and kinematic and kinetic movement profiles, all signals were sampled at 1 KHz. All post hoc data analysis procedures were performed using Matlab (Mathworks).
H-REFLEX RECORDINGS.
The H-reflex recording procedures were the same during pedaling and in sitting. The quadriceps H-reflexes were elicited by stimulating the femoral nerve in the femoral triangle using squared pulses of either 1- or 0.5-ms duration delivered with a constant current isolated stimulator (Axon Isolator-11). In addition to the bipolar EMG leads from the surface electrodes described above, a monopolar EMG lead from VL and RF muscles was recorded, because monopolar leads have proven to give the largest H-reflex EMG responses (Garland et al. 1994). However, during pedaling, the monopolar recordings were seriously contaminated with movement artifacts and background noise, and therefore we chose only to extract and present the H-reflexes from the signals recorded with the bipolar leads. To reduce the stimulus artifact, two large self-adhesive electrodes (PALS Flex 896230) were used as a pair of anodes and placed ventral and dorsal, respectively, in relation to the greater trochanter. A surface electrode (Neuroline, Medicotest 720-01-K) was used as a cathode for stimulation and placed over the femoral nerve and secured with tape in the femoral triangle. Before the cathode was mounted, the optimal site for stimulation was located by stimulating with a handheld electrode observing the EMG responses on a computer screen. The stimuli were always delivered with a minimum interval of 4 s, and the stimulus intensity was varied manually in a random fashion over the range of stimulus intensities, thereby eliciting responses between no visible M- and H-waves up to maximal M-wave (Mmax). A minimum of 30 stimuli was delivered to record each H-reflex excitability curve. During pedaling, H-reflex excitability curves were recorded at 10 equally spaced crank positions starting at zero degrees, corresponding to top-dead-center (TDC). The sequence of crank positions where the H-reflexes were recorded from was randomized. The PC-based data acquisition system (Humaniac) controlled the data acquisition and the timing of the stimuli in relation to the position of the crank triggered by a feedback pulse from the ergometer each time the right pedal passed TDC. All signals were sampled at 5 KHz.
Data analysis
KINEMATICS AND KINETICS.
The position signals from crank and pedals and the pedal force signals were low-pass filtered at 30 Hz (Butterworth 4th order digital filters with no phase lag). By assuming that the hip joint center was stationary during pedaling, the kinematics of the right lower extremity and the crank can be considered as a closed kinetic chain; therefore using the segment lengths and the recorded crank and pedal positions, the tangential forces on the crank arms and the corresponding crank moments could be derived and the ankle, knee, and hip net joint moments calculated by standard inverse dynamics methods (Hull and Jorge 1985; Winter 1991). Ankle, knee, and hip joint mechanical work was calculated by integrating the joint moments with respect to the joint angles.
EMG PROFILES AND MOTOR RECRUITMENT. The EMG signals obtained during pedaling without stimulation were high-pass filtered at 40 Hz and low-pass filtered at 500 Hz (Butterworth 4th order digital filters with no phase lag), full-wave rectified, and averaged over 10 consecutive pedal cycles. Mean EMG level during a revolution was calculated in VL, RF, and BF for each pedaling frequency. To obtain the motor recruitment levels in VL and RF, respectively, corresponding to the positions where the H-reflexes were recorded, the averaged and rectified EMGs were integrated by calculating mean EMG in 10 intervals of 18° of crank rotation, each interval starting at the angle where the stimulus was delivered. The magnitude of the integrated EMG in each interval was normalized to the Mmax obtained in the corresponding interval.
The motor recruitment levels during tonic activation of the quadriceps muscle were obtained from the VL and RF EMG signals acquired during the H-reflex recordings. Each acquired sweep included 50 ms of EMG signal before the stimulus was delivered, and for each activation level, all sweeps were filtered, rectified, and averaged as explained above. The mean amplitude over the first 50 ms was determined as the motor recruitment level and normalized to Mmax recorded at the same level of activation.
H-REFLEXES. Reflex signals from VL and RF were analyzed. Because of overlap between M- and H-waves, implying that H-reflexes appeared at the hindmost flank of the M-wave, a post hoc signal processing procedure was developed. Graphical presentation of this procedure is shown in Fig. 1.
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1% of the RMS residual error of the linear fit. The H-reflex amplitude was extracted at a stimulus intensity corresponding to an M-wave of 15% Mmax from the fitted curves. In four subjects, however, the H-reflex excitability curves were shifted to the right in RF, and consequently, H-reflex amplitudes were measured at a higher stimulus intensity corresponding to 35% Mmax. Because of the inherent variability in pedaling velocity at any given pedaling frequency, only the H-reflexes recorded within ±2.5% SD of target crank angle were used for the construction of the reflex excitability curves. The operationally defined H-reflex gain function (Edamura et al. 1991) for pedaling and tonic activation during sitting was calculated by least-squares linear regression between the normalized EMG amplitude and the normalized H-reflex excitability level. Only data where the quadriceps muscle was active during pedaling were included in the calculations (Larsen and Voigt 2004), which corresponded to the data obtained at the first three crank positions after TDC and the last two crank positions before TDC during pedaling at 80 rpm. Differences in the modulation of the H-reflex and background EMG during a crank cycle was calculated as differences significantly different from zero between the mean normalized, averaged reflex and background EMG amplitudes across subjects at each crank position. The H-reflex latencies were determined as the interval between the time of the delivery of the stimulus and the onset of the H-reflex. The latter was determined by marking the assumed reflex deflection appearing at low stimulus intensities by a cursor followed by the observation that this deflection disappeared at maximal stimulus intensities.
Statistics
A one-way ANOVA for repeated measures was used for comparison of the kinetic, kinematic, EMG, and reflex data between pedaling situations. Except for comparisons of the difference in the modulation of the reflex and background EMG amplitude where Dunnett's test was used, the Student-Newman-Keuls method was used for pairwise multiple comparisons. The level of significance in all tests was P < 0.05. For comparisons between pedaling and isometric contractions in sitting, a one-way ANOVA was applied. Unless otherwise mentioned, the data are presented as mean ± SD across subjects.
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RESULTS |
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The general pedaling patterns observed in this study were not fundamentally changed between tests; EMG-profiles (Baum and Li 2003; Ryan and Gregor 1992), kinematics, and kinetics (Neptune et al. 1997) did not deviate from previous observations, just as the relative work distribution between the muscles around hip, knee, and ankle joints was unchanged between tests.
All subjects were able to maintain pedaling at a very constant speed in both tests (test A: 40.3 ± 0.4 rpm; test B: 80.8 ± 0.5 rpm).
Figure 2 shows a representative set of EMGs and kinematic and kinetic data recorded from one subject during pedaling at 40 and 80 rpm, respectively. The doubling of the crank load at 40 rpm caused an increase in the right crank torque during the downstroke (from 0 to 180°). At the same time, the negative crank torque during upstroke (from 180 to 360°) was almost unchanged (Fig. 2). The timing of the EMGs shifted forward in time, i.e., the EMG onsets and offsets advanced by 20–30° as a consequence of the increase in pedaling frequency. At 40 rpm, peak VL EMG occurred around TDC, and the EMG decreased gradually during the first two-thirds of the downstroke phase, whereas at 80 rpm, peak VL EMG shifted until later in downstroke, and the EMG activity was more abruptly shut off (Fig. 2). Especially at 80 rpm, EMGs of the biarticular RF and BF varied more between subjects than the EMGs of the monoarticular VL (Fig. 6). However, RF was activated before VL during the upstroke in all subjects, indicating its contribution to the hip flexion during upstroke. In BF, EMG activity peaked when VL and RF EMGs approached zero toward the last part of downstroke in all subjects in both tests, which indicates the contribution of the hamstring muscles to the extension of the hip during the last part of downstroke and the flexion of the knee during the following upstroke phase (Fig. 6). The activation level of the muscles around the knee joint did not change between tests except peak RF EMG, which decreased significantly at 80 rpm compared with 40 rpm (P = 0.04; Fig. 3).
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H-reflexes
When the femoral nerve was stimulated in the femoral triangle, H-reflexes were elicited simultaneously in the three heads of the quadriceps muscle from which EMGs were recorded (VL, VM, and RF); however, in 2 of the 16 subjects, H-reflex amplitudes were very small and not quantifiable in RF. In three subjects, originally enlisted in the study, H-reflexes were not elicited in any of the quadriceps heads, and the three subjects were consequently excluded from the study. The modulation of the H-reflexes in the monoarticular heads of the muscle were expected to be modulated in parallel, and therefore only the H-reflexes recorded from VL and RF were analyzed and presented here.
Mean H-reflex latencies were 19.0 ± 2.7 ms in VL and 16.9 ± 1.6 ms in RF. Mean Mmax measured during sitting rest was similar in the pedaling and the isometric group [VL: 7.5 ± 2.5 mV (pedaling), 7.6 ± 4.5 mV (isometric), RF: 5.5 ± 2.0 mV (pedaling), 4.6 ± 1.7 mV (isometric)]. Hmax/Mmax ratio during sitting rest varied considerably between subjects in both groups [VL range: 6–57% Mmax (pedaling group), 5–28% Mmax (isometric group), RF range: 8–30% Mmax (pedaling group), 5–17% Mmax (isometric group)], and in several subjects, H-reflexes were not elicited except during muscle activation.
Quadriceps H-reflex modulation during pedaling
Figure 5 shows a representative set of the M- and H-wave excitability curves from one subject recorded from VL at 10 equally spaced positions over the crank cycle during pedaling at 40 rpm and 5.1 Nm crank load and during sitting rest. The stimulus-response curves show the typical pattern of changes in M- and H-waves with increasing stimulation intensities. The maximal M-wave varied during the movement cycle in all subjects but to a different extent. The excitability of the H-reflexes modulated considerably during a crank cycle with relatively high reflex amplitudes in the major part of the downstroke phase and reflex inhibition in the upstroke phase.
Figure 6 shows the mean modulation of the H-reflexes in VL and RF and the EMGs of the thigh muscles VL, RF, and BF across subjects during pedaling at 40 and 80 rpm at a constant workload. All data are normalized to maximal value during the crank cycle in each subject before averaging. The amplitudes of the H-reflex were high during power generation in downstroke and the reflex was inhibited during upstroke until the last measurements before TDC. Irrespective of pedaling frequency cessation of the EMG in both heads of the quadriceps, H-reflex inhibition and peak BF EMG appeared at the same crank position in the last part of downstroke, and this pattern of H-reflex inhibition and antagonistic reciprocal EMG activity was seen in all subjects.
There were no significant differences in the H-reflex modulation in relation to the background EMG in VL and RF at 80 rpm (Fig. 7B), whereas at 40 rpm, there was a significant difference in the modulation of the two at TDC and during the major part of downstroke in both VL and RF (P < 0.05; Fig. 7A), i.e., reflex amplitudes remained high despite a gradual derecruitment of the muscle in downstroke. Furthermore, in RF, the increase in H-reflex amplitudes (i.e., the slope of the curve) before TDC was significantly lower than the increase in background EMG (P < 0.05).
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Quadriceps H-reflex gain functions during pedaling
Linear regression fits showed a high positive correlation between background EMG and H-reflex amplitudes during pedaling at 80 rpm (test B; mean r = 0.7 in both VL and RF, range: 0.97–0.37 in VL and 0.98–0.20 in RF). Figure 8A shows reflex data and the fitted linear regressions lines for the relationship between H-reflex amplitude and EMG in VL in test B (mean slope 7.3 ± 3.4 and mean y-intercept 3.7 ± 2.4). In RF, mean slope was 0.60 ± 15.88 and mean y-intercept was 4.3 ± 4.7. The positive correlation between background EMG and H-reflex amplitudes at 40 rpm (test A) was relatively weak (r = 0.5; range: 0.90–0.06 in VL and r = 0.4 in RF; range, 0.81–0.05), and consequently, the operationally defined H-reflex gain function was not clearly expressed. No significant correlation was found between changes in reflex amplitudes and knee joint angular velocities or knee joint moment during the crank cycles.
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Figure 8B shows the H-reflex amplitudes in relation to the background EMG activity in VL including the linear regression lines obtained during tonic activation of VL. The motor recruitment level was in the same range as during pedaling in all but one subject (Fig. 8B, 
). With good approximation, the VL H-reflex amplitudes increased linearly (r = 0.7) with increasing background EMG activity in all but one subject (Fig. 8B, 
). The mean slope and y-intercept of the linear regression in VL (slope: 9.5 ± 10.5, y-intercept: 4.9 ± 7.0) was not significantly different from that during pedaling (P = 0.6). When data from the two subjects with low motor recruitment level and negative linear correlation were excluded, the mean slope during tonic contractions were similar to that during pedaling (r = 0.9, slope: 7.5 ± 3.1; P = 0.93) and the y-intercept was not significantly different from that during pedaling (y-intercept: 1.7 ± 3.3; P = 0.2). In RF, the results during isometric contractions were more scattered (linear correlation, r = 0.6), and no significant differences were found in either slope or y-intercept in relation to pedaling (slope 2.8 ± 2.8, y-intercept: 3.5 ± 3.3; P = 0.8).
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DISCUSSION |
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Methodological considerations
From a methodological point of view, the following precautions were made to ensure the reliability of the quadriceps H-reflex measurements.
1) Much attention was paid to find the optimal position of the stimulating electrode and a reliable fixation of the electrode. 2) H-reflex amplitudes were compared at the same relative M-wave (Simonsen et al. 1995), and full H-reflex recruitment curves were carried out in all measurement points (Zehr 2002). Uncertainty relating the interpretations of the H-wave potentials appears in earlier quadriceps studies because of the difficulties in distinguishing between the direct short latency motor response (M-wave) and the later H-potential. To counteract this uncertainty 1) the recommendations concerning optimal position of the EMG electrodes for mono- and bipolar measurements of quadriceps H-reflexes were followed and 2) the duration of the stimulation varied (Capaday 1997). Furthermore, a novel post hoc correction was applied which from the pattern of the excitability curves appeared to work satisfactorily. Three subjects originally enlisted in the study were excluded because H-reflexes were not elicited at tolerable stimulation intensities. Even though attention was paid that stimulation intensities were kept within an acceptable range in each subject, the stimulation intensities required may have caused inconvenience to some extent and therefore may have had an influence on the excitability of the H-reflex in some subjects (Motl et al. 2002).
However, we believe that by applying the methodological precautions as in this study, quadriceps H-reflexes can be quantified during locomotion in a reliable way.
H-reflex modulation during pedaling
In line with H-reflexes in other upper and lower extremity muscles during rhythmically movements, the amplitude of the quadriceps H-reflex displayed considerable phase-dependent modulation during a crank cycle. H-reflex amplitudes were larger and reflexes more easily evoked in VL compared with RF in all subjects, possibly determined by the mutual anatomical position of the different branches of the femoral nerve in relation to the stimulating electrode (Sabbahi and Khalil 1990). This implied that the variability of the H-reflexes was relatively larger in RF compared with VL because of an aggravated signal to noise ratio in the smaller RF H-reflexes. However, the pattern of reflex modulation was similar in the two muscles, indicating that during stereotyped alternating leg movements like pedaling, the central control of the Ia afferent feedback is most likely identical in the mono- and biarticular heads of quadriceps.
The modulation of the quadriceps H-reflex during a crank cycle corresponds to that in soleus with peak reflex amplitude during power generation in downstroke and reflex inhibition in upstroke. However, the association between the excitability of the quadriceps H-reflex and the motor command was substantially altered with speed of movement, and it was most evident at 80 rpm, which is probably close to the preferred pedaling frequency in most subjects (Marsh and Martin 1993). In cats, phase-dependent changes in primary afferent depolarization (PAD) (Rossignol et al. 1998) and monosynaptic reflexes during movements (Duenas et al. 1990; Gossard 1996) have been associated with changes in presynaptic inhibition. Presynaptic inhibition is considered to influence the phase-dependent modulation of the human H-reflexes as well (Stein 1995), and therefore changes in presynaptic inhibition probably underlie the changes in the modulation of H-reflex amplitudes between the two pedaling tests, also. Previous H-reflex studies in soleus during muscle release after isotonic muscle activation have shown a fast H-reflex inhibition during derecruitment, indicating that an enhancement in presynaptic inhibition of the Ia afferents and thereby a blocking of the autogenetic excitation from Ia afferents to the motoneurons may be paramount to ensure cessation of motoneuron discharge (Schieppati et al. 1986). Gating of the ongoing Ia afferent input is probably not as critical when motoneurons are derecruited during shortening of the muscle fibers like in downstroke during pedaling movements. However, these results obtained during pedaling at 80 rpm correspond to earlier reports pointing at a fast increase in presynaptic inhibition during derecruitment. However, at 40 rpm, when motoneurons are gradually derecruited during muscle shortening, the quadriceps H-reflex is not correspondingly inhibited until complete cessation of activation. This change in reflex modulation at 40 rpm indicates that the onset of presynaptic inhibition is delayed during derecruitment at low movement speed by which the afferent contribution to muscle activation is still possible during power generation. Thus the Ia afferent input to the quadriceps muscle seems to be controlled much in parallel to the motor command when pedaling movements are executed close to the optimal speed or rhythm, with "ballistic"-type of movement patterns characterized with short quadriceps EMG bursts and short lasting high peak power generation. During slow and more "isokinetic"-like pedaling movements, however, the afferent input is controlled more independently of the motor command.
The muscles around the knee joint are reciprocally activated in downstroke in all subjects, causing peak EMG activity in BF at the time of quadriceps EMG offset and complete reflex inhibition. In soleus, the activation of TA influences the amplitude of the H-reflex at rest (Crone and Nielsen 1989) and during locomotion (Lavoie et al. 1997; Schneider et al. 2000), although it is probably not decisive to the modulation pattern (Yang and Whelan 1993). It is likely that the classical pattern of reciprocal inhibition between antagonist muscles influences the quadriceps H-reflex inhibition in downstroke during pedaling, also. However, it does not seem from these results that changes in reciprocal muscle activation determine the speed-dependent differences in the quadriceps H-reflex modulation pattern during pedaling.
Speed-dependent influences on the H-reflex gain were previously showed in soleus during walking and running (Capaday and Stein 1987b), and an approximately linear relationship has been reported between soleus H-reflex inhibition and speed of movement during pedaling (McIlroy et al. 1992). In a previous study, we showed that the speed-dependent decrease in the excitability of the soleus H-reflex from pedaling at 40 to 80 rpm at constant workload appears as a decrease in the gain of the operational H-reflex gain function whereas reflex threshold is not influenced by speed of movement (Larsen and Voigt 2004). A similar comparison of speed-dependent changes in the operationally defined H-reflex gain function during pedaling was not possible in quadriceps. However, these changes in reflex modulation pattern at 40 rpm, which resulted in a relative high excitability of the reflex in relation to the motor activation in downstroke in general, support the findings in soleus, suggesting a decrease in the excitability of the H-reflex with increased pedaling frequency, just as the strong trend toward an increase in VL H-reflex/EMG ratio at peak H-reflex at 40 rpm does. It has been suggested that a decrease in reflex gain at high speed of movements may ensure that the net motor output does not saturate at high movement speeds (Capaday and Stein 1987b). Also, a decrease in the reflex gain may ensure that movements are not inappropriately disrupted by a sudden increase in afferent discharge caused by the time lag between receptor activation and the increase in muscle stiffness. Whereas at low speed of movement, a high reflex gain during power generation allows that irregularities in the propulsion of the crank during pedaling are corrected by the afferent discharge. The significance of speed-dependent changes in the H-reflex is uncertain; however, these results confirm a decrease in the spinal sensitivity of the Ia afferent discharge at high speed of movement.
Quadriceps H-reflex during tonic muscle activation
These results did not show a task-dependent modulation of the quadriceps H-reflex gain function between tonic conditions and pedaling movements. Mean slope (an expression of the reflex gain) and y-intercept (an expression of the reflex threshold) of the linear relation between quadriceps H-reflex amplitudes and background EMG measured in the same range of motor recruitment were not significantly different during sitting and pedaling.
Task-dependent changes in the soleus H-reflex have been shown at a constant background EMG activity from tonic activation in standing to walking. By application of the H-reflex gain function, Capaday and Stein (1986) found a decrease in both the soleus H-reflex gain and threshold from standing to walking. From simulation studies and reflex studies on cats, they later argued that the shown changes in reflex gain and threshold were controlled by presynaptic mechanisms (Capaday and Stein 1987a, 1989). Task-dependent changes in the amplitude of the soleus H-reflex have been reported from sitting to pedaling, also. However, it seems that the task-dependent differences in reflex amplitudes are most prominent during soleus inactivation in upstroke, whereas during soleus activation in downstroke, the movement-specific modulation of the reflex at matched background EMG levels seems harder to identify (Pyndt and Nielsen 2003; Zehr et al. 2001).
In contrast to most reports on the soleus H-reflex (Loscher et al. 1996), the excitability of the quadriceps H-reflex during rest and at low contraction levels in sitting was low in all but one subject in this study. It has been shown in animal preparations (Burke 1968; Messina and Cotrufo 1976) as well as in humans (Awiszus and Feistner 1993; Buchthal and Schmalbruch 1970) that the responsiveness of Ia afferent inputs are larger in slow twitch muscle fibers compared with fast twitch fibers, although some differences may exist in upper limb muscles (Buller et al. 1980; Mazzocchio et al. 1995). Therefore it is likely that H-reflexes are more readily evoked and reflex amplitudes are larger at low contraction levels in distinct postural muscles with a relative high content of slow-twitch fibers such as soleus in comparison with the quadriceps muscle with a more even distribution of fiber types (Saltin and Gollnick 1983). Although both muscles are considered as postural muscles, the fact that soleus generates higher torque compared with the quadriceps during standing possibly influences the control of the muscles in general.
These results showed no significant differences in the H-reflex gain function elaborated during pedaling and tonic muscle activation in sitting. Thus the concept of task-dependent reflex modulation, which has mainly been studied at the ankle joint, may not generalize to other joints. Further work on a variety of tasks and joints is required to test this important concept.
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FOOTNOTES |
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Address for reprint requests and other correspondence: B. Larsen, Fredrik Bajers Vej 7-D3, 9220 Aalborg, Denmark (E-mail: BL{at}Neurodan.dk)
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REFERENCES |
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