Introduction: Eccentric contractions induce muscle fiber damage that is associated with delayed-onset muscle soreness and an impaired ability of the muscle to generate voluntary force. Pain and pathophysiological changes within the damaged muscle can delay or inhibit neuromuscular responses at the injured site, which is expected to have an effect on reflex activity of the muscle.
Purpose: The aim of the study was to investigate the reflex activity of knee muscles to rapid destabilizing perturbations, before, immediately after, and 24 and 48 h after eccentric exercise.
Methods: Bipolar surface EMG signals were recorded from 10 healthy men with seven pairs of electrodes located on the knee extensor muscles (vastus medialis, rectus femoris, and vastus lateralis) and knee flexor muscles (the medial and lateral heads of the hamstring and the medial and lateral heads of gastrocnemius) of the right leg during rapid perturbations.
Results: The maximal voluntary contraction force decreased by 24% ± 4.9% immediately after exercise and remained reduced by 21.4% ± 4.1% at 24 h and by 21.6% ± 9.9% at 48 h after exercise with respect to baseline. During the postexercise postural perturbations, the EMG average rectified value of the knee extensor muscles was significantly lower than baseline (P < 0.001). Moreover, the decrease in average rectified value over time during postexercise sustained contractions was greatest compared with the session before exercise (P < 0.0001).
Conclusions: Reflex activity in leg muscles elicited by rapid destabilizing perturbations is reduced after exercise-induced muscle soreness.
1Centre for Sensory-Motor Interaction, Department of Health Science and Technology, Aalborg University, Aalborg, DENMARK; 2Pain Clinic, Center for Anesthesiology, Emergency and Intensive Care Medicine, University Hospital Göttingen, GERMANY; 3Department of Neurorehabilitation Engineering, Bernstein Center for Computational Neuroscience, University Medical Center Göttingen, Georg-August University, Göttingen, GERMANY
Address for correspondence: Deborah Falla, Ph.D., Department of Neurorehabilitation Engineering, Bernstein Center for Computational Neuroscience, University Medical Center Göttingen, Georg-August University, Von-Siebold-Str. 4, 37075 Göttingen, Germany; E-mail: email@example.com.
Submitted for publication August 2010.
Accepted for publication November 2010.
Maintenance of posture often requires reflex muscle activity to return a perturbed joint to its initial position. Reflex muscle responses to rapid perturbations play a significant role in the dynamic alignment and stability of musculoskeletal structures. For example, enhanced knee stability has been demonstrated by reflexive responses elicited in muscles surrounding the knee by mechanical stimulation of the medial ligament (21,27) and by a rapid valgus/varus movement of the knee (4).
Pain is common after a high-intensity eccentric exercise particularly in untrained individuals, most likely due to accumulation of metabolites and/or fiber injury within the skeletal muscle (26). The quadriceps femoris muscle is particularly susceptible to fiber damage due to its powerful action and frequent eccentric loading of the leg during sport and daily activities. Delayed-onset muscle soreness (DOMS) usually manifests 24 h after eccentric exercise and persists for prolonged periods of time (up to 72 h after exercise) due to pathophysiological changes in the muscle fibers. In the injured muscle, phagocyte cell infiltration results in progressive necrosis of the contractile elements and inflammation (1,26,37), which, in turn, sensitizes intramyofibril pain afferents (group IV) (37). The presence of pain within the quadriceps muscle may delay or inhibit neuromuscular responses at the injured site (13,14) because input from nociceptive afferents can inhibit the input of muscle spindles via presynaptic inhibition (5,42). Thus, when individuals with quadriceps pain are faced with demanding tasks that may challenge knee stability, the neuromuscular system may be incapable of appropriately activating muscles to stabilize the joint. Such altered muscle activity around the knee may expose structures of the knee joint to abnormal loading during exercise and may contribute to sport-related injuries (24,25).
Changes in motor control strategies induced by eccentric exercise are reflected in features of the surface EMG (28). Thus, the use of EMG during destabilizing perturbations that challenge knee stability may provide greater insight into the change in muscle activation patterns after eccentric exercise. This knowledge may be useful to understand the mechanisms underlying the development of knee disorders (e.g., patella, ligament and tendon injuries) after an unaccustomed exercise. In this study, it was hypothesized that muscle activity elicited by rapid destabilizing perturbation would be reduced after exercise-induced muscle soreness. Therefore, the purpose of this study was to assess the EMG activity of knee muscles during destabilizing perturbations performed before, immediately after, and 24 and 48 h after eccentric exercise.
MATERIALS AND METHODS
Experimental design and approach.
This experiment analyzed reflex activity of the knee muscles after eccentric exercise. Reflex activity was elicited in knee muscles by rapid destabilizing perturbations. Surface EMG signals were recorded from the quadriceps, hamstrings, and gastrocnemius simultaneously during the destabilizing movements before, immediately after, and 24 and 48 h after eccentric exercise.
Ten healthy men (mean ± SD; age = 23.2 ± 3.1 yr, body mass = 75.5 ± 10.4 kg, height = 1.78 ± 0.06 m) participated in the study. All subjects were right leg dominant and were not involved in regular exercise of their knee extensor muscles for at least 6 months before the experiment. The study was conducted in accordance with the Declaration of Helsinki and approved by the local ethics committee (No. 20070019). Subjects provided informed written consent before participation in the study. The number of participants was based on previous studies examining the effects of eccentric exercise on muscle activity, which showed that 10 volunteers were sufficient to show a difference (14,15).
Time to task failure for a sustained isometric contraction at 50% of maximal force and EMG variables during both the sustained contraction and destabilizing perturbations were recorded, before, immediately after, and 24 and 48 h after exercise. Moreover, maximal voluntary contraction (MVC) force, subjective pain intensity ratings, and muscle circumference were measured before and after the exercise sessions. The exercise protocol was performed with a KinCom Isokinetic Dynamometer (Chattanooga, TN) and consisted of four bouts of 25 maximum voluntary eccentric knee extension contractions at a speed of 60°·s−1 between 90° and 170° of knee extension, with 3 min of rest between each set (8,13-15). During the exercise, the subject was provided with visual feedback of the force produced and was verbally encouraged to generate a maximal force during the eccentric phase, whereas during the concentric phase, the movement was assisted by the dynamometer.
Maximal voluntary contraction.
Maximal voluntary isometric contraction force was measured using the KinCom Dynamometer. The subject was seated on the adjustable chair of the KinCom with the hip in 90° flexion. The chair position was modified until the knee axis of rotation (tibiofemoral joint) was aligned with the axis of rotation of the dynamometer's attachment arm. The subject was fixed with straps secured across the chest and hips. The right leg was secured to the attachment arm in 90° knee flexion with a Velcro strap. Visual feedback of force was provided on a screen positioned in front of the subject. The subject was asked to perform three maximal isometric knee extensions (3-5 s in duration) in 90° knee flexion, with 2 min of rest between and verbal encouragement to exceed the previous force level. The highest MVC value was used as a reference for the definition of the submaximal force level. The submaximal forces were relative to the MVC measured on the same day of the test. Thigh circumference was measured using a tape measure around the distal portion of the thigh at 10% of the distance between superior border of the patella and anterior superior iliac spine.
A 10-cm visual analog scale, labeled with end points on the left (no pain) and right (worst pain imaginable), was used to assess the perceived pain intensity 24 and 48 h after exercise. The subjects were asked to rate the average pain intensity in the quadriceps during their regular activities of daily living (e.g., climbing stairs) since their last visit to the laboratory (during the past 24 h).
Seven pairs of circular Ag-AgCl surface electrodes (Ambu Neuroline, Ambu A/S, Ballerup, Denmark; conductive area = 28 mm2) were placed in bipolar configuration (interelectrode distance = 2 cm) over the quadriceps, hamstring, and gastrocnemius muscles. Electrodes were placed over the quadriceps at 10% of the distance between medial border (vastus medialis; VM), superior border (rectus femoris; RF), and lateral border (vastus lateralis; VL) of the patella and anterior superior iliac spine. The position of electrodes on hamstring muscle was determined by palpation of the most distal portion of the medial (biceps femoris; BF) and lateral (semitendinosus; ST and semimembranosus; SM) belly of the hamstrings during light isometric contractions with the subject in a prone position. For the gastrocnemius muscle electrode pairs were placed on the lateral and medial head of gastrocnemius (LG and MG, respectively) at one-fourth the distance from the popliteal fossa to the insertion of the Achilles tendon. Before electrode placement, the skin was shaved and lightly abraded at the selected locations. Surface EMG signals were amplified (EMG amplifier (EMG-128; LISiN-OT Bioelettronica, Turin, Italy) with a bandwidth of 10-500 Hz), sampled at 2048 Hz, and stored after 12-bit A/D conversion.
EMG during sustained contractions.
Surface EMG signals were recorded from the VM, VL, and RF during an isometric knee extension contraction at 50% MVC, which was sustained until task failure. The sustained contraction was performed on the KinCom Dynamometer with the subject in the same position as in the maximal voluntary contractions, i.e., with the knee and hip in 90° of flexion. Task failure was defined as a drop in force greater than 5% MVC for more than 5 s after strong verbal encouragement to the subject to maintain the target force.
The average rectified value (ARV) was estimated from the EMG signals for epochs of 1 s. The values obtained from 1-s-long epochs in intervals of 10% of the time to task failure were averaged to obtain one representative value for each 10% interval. This allows for comparison of data with different times to task failure. To compare changes across testing sessions, the percent change in ARV over time was calculated by subtracting the final value from the initial value of ARV and dividing by the initial value.
EMG during postural perturbations.
Subjects stood with their feet shoulder width apart and their right limb on a movable platform. A positioning actuator (41) translated the platform 6 cm frontally (forward and backward direction) for 150 ms. The subject's left foot was positioned on the ground, and an oscilloscope was positioned in front of the subject to monitor weight bearing. To restrict hip joint motion, a strap was secured around the pelvis and bolted firmly to the wall. The subject stood comfortably with equal weight on each limb using the visual feedback. Four 3-s trials were collected in which the plate was triggered to move at a random interval within the 3 s. Subjects were unaware of when the plate would be triggered to move. Surface EMG was recorded from the quadriceps, hamstring, and gastrocnemius of the right limb.
To assess the amplitude of muscle reflex activity, the ARV of individual muscles was calculated over a fixed window, which was 175 ms after the onset of plate movement. This time window reflects the muscle response that occurs after the monosynaptic stretch reflex, which is thought to be mediated subconsciously, with afferent commands being sent to the cerebellum and brainstem (40). The ARV obtained from the 175-ms epochs in four trials were averaged to obtain a representative value. A reference electrode was placed around the right ankle. The positions of the electrodes were marked on the skin during the first session (day 1) so that the locations could be replicated 24 and 48 h after exercise.
A one-way repeated-measures ANOVA was applied to analyze MVC, time to task failure, and thigh circumference across testing days. Two-way repeated-measures ANOVA was used to assess the percent change of ARV across the sustained contraction at 50% MVC (percent change from the first to the last epoch), with day and muscle as dependent factors. To assess changes in the amplitude of reflex muscle activity during the perturbations, a three-way ANOVA was applied to the change of ARV value from baseline (day 1) to the ARV value after exercise (immediately after and 24 and 48 h after), with muscle and perturbation direction (backward and forward) as dependent factors. Pairwise comparisons were performed with the Student-Newman-Keuls post hoc test when ANOVA was significant. The significance level was set at P < 0.05 for all statistical procedures. Results are reported as mean and SD in the text and SE in the figures.
Functional properties and pain assessment.
Significant reductions in maximum voluntary force (F3 = 9.1, P < 0.0001) and time to task failure (F3 = 9.5, P < 0.0001) were observed immediately after and 24 and 48 h after exercise compared to baseline (Table 1). MVC and time to task failure were not significantly different between the three postexercise sessions (immediately after and 24 and 48 h after, P > 0.05). Thigh circumference measured immediately after and 24 and 48 h after exercise was larger than that in the measure before exercise (P < 0.001; Table 1). The average reported pain intensity was 5.8 ± 0.9 and 6.2 ± 0.8 at 24 and 48 h after exercise, respectively.
The ARV of the EMG decreased during the sustained isometric contraction. The percent decrease of ARV over time (in the final epoch with respect to the initial epoch) depended on the session (F3 = 118, P < 0.0001) and the interaction between session and muscle (F6 = 3.3, P < 0.05), with a greater reduction identified for the postexercise sessions (immediately after and 24 and 48 h after) with respect to the session before exercise, and a larger reduction identified for the VM muscle at the postexercise sessions compared with RF and VL muscles (Fig. 1).
Rapid destabilizing perturbation.
Figure 2 presents representative surface EMG data detected from the distal portion of the right vastus medialis muscle of one subject during the destabilizing perturbations at baseline, immediately after, and 24 and 48 h after exercise. During the rapid destabilizing perturbations, ARV depended on the perturbation direction (F1 = 4.8, P < 0.05), session (F3 = 5.8, P < 0.001), muscle (F2 = 19.1, P < 0.0001), and the interaction between session and muscle (F3 = 3.7, P < 0.05). The ARV value (average over all muscles) was larger for the backward perturbations compared with the forward direction (P < 0.05). ARV values were smaller in the postexercise sessions (immediately after and 24 and 48 h after) with respect to the preexercise session (P < 0.001), and among the knee extensor muscles, VL and VM had greater values of ARV compared with the RF muscle (P < 0.001). Moreover, VL and VM showed a higher decrease in ARV during the postexercise sessions for the backward perturbation (immediately after and 24 and 48 h after) with respect to the preexercise session (P < 0.05) than the RF muscle (Fig. 3). For the knee flexor muscles (MH, LH, MG, and LG), ARV values for the postexercise sessions (immediately after and 24 and 48 h after) were not significantly different from baseline (F3 = 2.2, P > 0.05).
This study demonstrated lower EMG activity of the DOMS-affected quadriceps muscle during rapid destabilizing perturbations immediately after and 24 and 48 h after eccentric exercise. Moreover, a greater reduction of muscle activity was observed during sustained contractions of the quadriceps muscle for the postexercise sessions with respect to the preexercise session. The results suggest that eccentric exercise contributes to a reduced ability of the quadriceps to stabilize the knee joint during a destabilizing event, indicating that care should be taken to prevent knee injury when training programs include a large number of heavily loaded eccentric contractions.
Maximal voluntary force and time to task failure in the DOMS-affected quadriceps muscle were significantly decreased immediately after eccentric exercise and persisted at 24 and 48 h after exercise, which is in agreement with previous studies on the same muscle (13,14). A significant reduction in maximal isometric force and time to task failure observed after exercise indirectly suggests that the eccentric exercise used in this study contributed to muscle damage and thus to the reduced muscle power and physical work capacity. A force deficit after an eccentric task can be explained by a failure in signal transmission from higher motor centers to the muscle fiber (30) and/or failure in signal conduction at the muscle fiber membrane (15), most likely because of fatigue, fiber disruption, and pain (23,25). After high-intensity eccentric exercise, an increase in extracellular potassium, accumulation of metabolites (e.g., acid lactate, inorganic phosphate), and/or fiber membrane disruption would decrease muscle fiber excitability (15) and sensitize intramyofibril group III and IV afferents (18), contributing to decreased maximal force generation capacity. The presence of pain within the injured muscle can also inhibit motor neurons at spinal and supraspinal levels, which, in turn, results in reduced motor unit recruitment and discharge rate (18) and, consequently, reduced maximal isometric force. The subjects reported soreness in the quadriceps muscle 24 and 48 h after exercise, which may be related to damage of the contractile elements and connective tissue (26).
A greater decrease in EMG amplitude over time was also observed during the postexercise sustained contraction with respect to the preexercise session. Previous studies have also demonstrated a greater EMG amplitude rate of reduction over time during sustained contraction after eccentric exercise (13,28). A larger reduction of ARV after eccentric exercise may be related to the inhibitory effect mediated by nociception both at the cortical and spinal levels (23), which, in turn, reduces motor unit discharge rate (11) and, consequently, results in a decreased drive to the muscle fibers (13). The decreased ARV can be also explained by a failure in motor unit recruitment required to compensate for contractile failure caused by fatigue (22).
After eccentric exercise, pain manifested and the EMG activity of knee extensor muscles (affected by DOMS) decreased during the potentially destabilizing perturbations, with respect to baseline. However, in the knee flexor muscles (not affected by DOMS), EMG activity was not significantly different from baseline. This result indicates that the level of coactivation between the knee extensors and flexors is altered after eccentric exercise, which likely contributes to reduced knee joint stiffness during rapid destabilizing movements. Altered coactivation could result in joint instability or laxity, imposing an abnormal load on the structures of the knee, thus leaving them more susceptible to injury.
The current study is the first study in which muscle activation is measured during perturbations after eccentric exercise-induced DOMS. Previously, it has been demonstrated that higher background muscle activity yields increased reflexive joint stiffness, potentially providing greater joint stability (35). Therefore, lower background muscle activity observed in the DOMS-affected quadriceps muscle after eccentric exercise could result in reduced reflexive joint stiffness through decreased muscle stiffness. The reduced reflex muscle activation immediately after exercise could be explained by fatigue-induced changes within the muscle. The strenuous fatiguing exercise used in this study could have altered muscle fiber properties (19,20). Fatigue alters the behavior of intrafusal chain and static bag fibers, which, in turn, results in a reduction in Ia afferent inflow from muscle spindles. Fatigue could also change force-feedback mediated by the Golgi tendon organ and thus contribute to the inhibition of spinal motor neurons (3). Moreover, myofibrillar ATPase activity is reduced after fatigue because of metabolic accumulation, which would likely reduce the detachment rate of cross bridges and muscle contraction.
The observed change in reflex muscle activation after exercise may be related to disturbance in the γ-motoneuron system involved in regulating muscle stiffness. The γ-motoneuron system controls muscle stiffness through sensory information from muscles, ligaments, the joint capsule, and skin. This afferent input has a strong effect on the γ-motoneuron system that provides continuous preparatory adjustments to muscle stiffness (17,36). In the injured muscle, articular and periarticular afferent input is likely to be altered as a result of muscle inflammation and/or increased tension in the joint capsule (6,33,37), and this may result in a reduced capacity of the γ-motoneuron system to control muscle activity.
There are several different mechanisms by which pathophysiological changes within the skeletal muscle may contribute to decreased reflex muscle activity. For example, decreased reflex muscle activity after eccentric exercise can be explained by alterations in nociceptive sensitization of the painful muscle. Altered nociceptor sensitization associated with tissue injury can influence primary afferents of muscle spindles in the superficial layers of the dorsal horn of the spinal cord after eccentric exercise (42). Input from nociceptive afferents inhibits the input of muscle spindles by presynaptic inhibition (5) and, consequently, leads to decreased motor unit discharge rate (11) and muscle activity (13). It has been reported that pain by itself may lead to instability of a joint (7,10) by inhibition of the motor system excitability both at the cortical and the spinal levels (23). Reflex inhibition has also been demonstrated in the presence of pain induced by infusion of fluid into knee extensor muscles during isometric (9) and isokinetic contractions (2). In addition, when the quadriceps is injured, there is an arthrogenic reflex inhibition that contributes to a decreased ability of this muscle to achieve full voluntary activation (39). Pain induced by experimental infusion has also been reported to reduce the H reflex (the monosynaptic reflex, motor response to electrical stimulation of spindle afferent fibers) in the quadriceps muscle at rest (38) and against a background of muscle activity (16). The decreased H reflex has been attributed to the reduced excitation level of the quadriceps' anterior horn cells (34).
The reduction in reflex muscle activity after an eccentric exercise may also be due to the tonic descending inhibition process. There is a supraspinal loop by which noxious stimuli dynamically activate the descending inhibition of multireceptive dorsal horn cells, which is tonic in nature (12). There is evidence that, after muscle injury, pain and inflammation (26,37) increase the amount of tonic descending inhibition (33), resulting in decreased afferent input from regions of the inflamed knee (6) and, consequently, reduced muscle activity. The increased tonic descending inhibition mediated by nociceptive afferents has been considered to contribute to protection of the injured tissue from further insult (29).
The vastus lateralis and vastus medialis muscles showed a greater decrease in muscle activity during the postexercise destabilizing perturbation. This may be related to a more extensive damage of these regions, most likely due to high force production in these areas to stabilize the patella during eccentric exercise (31).
The amplitude of the EMG can be influenced by several physiological (e.g., motor unit synchronization, muscle fiber conduction velocity) and nonphysiological (e.g., electrode orientation) factors. Although care was taken to place the electrodes in the same locations when the subjects returned to the laboratory 24 and 48 h after exercise, some factors may vary from session to session, which can increase the variability of the results.
Maximal eccentric knee extension exercise resulted in reduced activity of the quadriceps muscle in response to rapid destabilizing perturbations, most probably due to muscle fiber disruption and pain. This finding suggests that eccentric exercise can impair reflex activity in the quadriceps and may compromise knee stability, therefore leaving structures of the knee more vulnerable to injury.
Funding was not received for this work from the National Institutes of Health, Wellcome Trust, Howard Hughes Medical Institute, or others. The authors declare no conflict of interest. The authors thank Prof. Dario Farina for his useful comments on the text. The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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Keywords:©2011The American College of Sports Medicine
REFLEX; PERTURBATION; DOMS; ECCENTRIC EXERCISE