Subjects cycled for 2 h at their previously determined V T (approximately 65%-70% of maximal oxygen consumption). They pedaled on their own bicycles, which were set up on a cycle trainer (Kurt Kinetic Road Machine; Kurt Kinetic, Jordan, MN). Respiratory gas measurements were made periodically for 5 min, every 20 min of cycling. Workload was adjusted to maintain oxygen consumption. The Borg scale was used to assess RPE at each measurement period (2). Immediately after the gas measurements, the cyclists sprinted for 1 min, after which measurements of RPE for the sprint were obtained. HR was determined using a Polar Heart Rate Monitor (Polar CIC, Port Washington, NY). Water was provided at a rate of 1% of body weight each hour.
After cycling for 2 h, they performed a 3-km time trial. Subjects were allowed to perform a 5-min cool-down on thebike at self-selected low resistance. Within 10 min of finishing the time trial, strength testing with magnetic stimulation was repeated as described above.
Changes in metabolic parameters were analyzed with repeated-measures ANOVA. Voluntary (VOL) and stimulated (PMS) strength, voluntary contraction with superimposed magnetic stimulation (VOL + AUG), augmentation from superimposed magnetic stimulation (AUG), and CAR were compared within subjects using paired t-tests. Previous testing of PMS of the quadriceps in our laboratory (10) has shown that we can detect a force decrement of 19% with 80% power using 12 subjects with PMS of the femoral nerve. Fatigue has been shown to produce force decrements of 23.5% using similar techniques to those described above with endurance athletes (18). Post hoc power testing of the strength testing data (voluntary and elicited contractions) demonstrated 85%power to detect a significant difference at P < 0.05 with 11subjects.
Subjects' descriptions are listed in Table 1. The subjects ranged from well-trained triathletes to Category 2 competitive cyclists, with a mean age of 41 yr. Their mean peak oxygen consumption (V˙O2peak) of 55.7 mL·kg−1·min−1 was typical of well-trained recreational cyclists, and their V T occurred at 65% of their V˙O2peak.
Water was provided throughout exercise. Although there was a significant decline in body mass during cycling (P=0.003), it represented only 0.65 kg or 0.9% of initial mass. Oxygen consumption did not change during the prolonged cycling bout (effect of time, P = 0.22). However, during the 2-h period, RER declined from 0.93 to 0.85 (effect of time, P < 0.001). RPE while pedaling at their own V T increased during the 2-h period, from a mean of 11.4 at 20 min to 12.9 at 2 h (P = 0.001). RPE during the five 1-min sprints remained unchanged over time, ranging from 16.5 to 17.3 (effect of time, P = 0.3). HR increased over time, from a mean of 128 bpm at 20 min to 138 bpm at 2 h (P = 0.3).
Strength data (VOL, PMS, VOL + AUG, AUG, CAR) are shown in Table 2. After the cycling exercise, subjects showed a 22% loss in strength (P = 0.001). Absolute force elicited by PMS alone also showed a decrease (17%, P<0.001). PMS alone elicited 89.6 ± 9.6% MVC beforeexercise and 104.4 ± 18.0% MVC after exercise (P=0.184); alternately, expressed as a percentage of VOL+ AUG, PMS elicited contractions of 72 ± 6% before exercise and 66 ± 5% after exercise (P = 0.164). Voluntary strength augmented with PMS tended to decrease by 8% (VOL + AUG, P = 0.06) before to after exercise. The force augmentation with PMS increased after fatigue (AUG, P=0.035); CAR decreased 15% after the cycling protocol (P = 0.005).
The objective of this study was to characterize neuromuscular fatigue in knee extensor muscles after prolonged cycling exercise which mimicked racing demands using a novel PMS-based method. We found that our cycling protocol induced fatigue (22% decrease in VOL) and that this fatigue had both peripheral (17% decrease in PMS, nonsignificant 8% decrease in VOL + AUG) and central (15% decrease in CAR) components, in accordance with our hypothesis (representative data for one subject are shown in Fig. 2). Central fatigue has been well demonstrated in endurance running (16,18,19). Some (1,13,20) but not all (17) studies of cycling have shown evidence for central fatigue, but generally, these studies have used longer duration or more intense exercise protocols than the one presented here. This is the first study to our knowledge thathas used PMS for this application (for cycling or any other activity).
Most protocols designed to investigate the effect of exercise on fatigue during cycling have been performed at a constant workload (12,21). In this study, we used a protocol meant to more closely mimic the fatigue developed in "real-world" racing situations, where multiple sprints are interspersed with sustained, steady-state cycling, and where a maximal effort is exerted during the final stages of the ride. This protocol is similar to those used by others (e.g., Cureton et al. ) to induce fatigue.
Studies that have evaluated fatigue using TMS have largely been limited to muscles of the upper extremity (e.g., [3,7,26,27,29]). Although some works have examined fatigue in the lower extremity using TMS (8,11,23), these studies have usually been limited to examining electrical manifestations of fatigue via magnetic evoked potentials (MEP). The work of Ross et al. (24) is the only example of which we are currently aware which has used TMS to examine lower extremity fatigue after endurance exercise using force measurements of VA. This is because of the relative ease of activating the arm and hand musculature via cortical stimulation, as the regions of the cortex controlling these are superficial. TMS of the lower extremity is a much more difficult task because the portion of the motor cortex controlling the lower extremity is much deeper in the brain. Thus, we used PMS to elicit contraction of large muscle groups in the lower extremity.
Effects on metabolic parameters
We controlled V˙O2 during the 2-h period to maintain energy expenditure at the V T. Despite this control, HR increased over time. This "cardiac drift" may be attributable to the slight (0.8%) loss in body mass and due to cumulative thermoregulatory stresses (31). The subjects did rate their effort as greater as cycling progressed, as would be expected with fatigue.
Strength loss and central fatigue
We noted a 22% decrease in voluntary strength after prolonged exercise, consistent with the reports of others (6,12,13,16-18,20,21). Using PMS, we were able to demonstrate significant central and peripheral components to this strength loss. Force elicited by PMS alone decreased by 17%. This is largely an indicator of peripheral fatigue, as stimulation alone bypasses the central drive from the motor cortex. This decrease may also reflect changes in the motor threshold of the femoral nerve (30). The 13% decrease in CAR from 0.84 to 0.73 is largely indicative of central fatigue. Whereas a significant component of central fatigue in knee extensors has been found after an ultramarathon race (16,18), Millet et al. (17) did not detect central fatigue after a cycling race using electrical twitch interpolation. Our results using PMS demonstrate significant peripheral and central components of fatigue after prolonged cycling that simulated racing conditions.
We feel that this PMS-based technique is superior for evaluating fatigue and CAR for several reasons. Many authors (12,13,16) investigate fatigue using a single- or double-twitch interpolation technique. Although this has long been used (originally proposed by Merton ), this technique often leads to data with large variability (13). Miller et al. (15) found stimulus trains better able than single pulses in augmenting voluntary contractions of the quadriceps and recommended their use in determining central activation failure. Some (1,14,18,20,21) have used trains of stimuli superimposed on voluntary contractions. Although we agree that this approach will likely lead to greater augmentation, electrical stimulation at this intensity is often painful to subjects, with this pain being the limiting factor of the intensity/frequency of stimulation. PMS is much better tolerated than electrical stimulation (10,12), which should allow for greater intensity/frequency of stimulation and less variable data as the stimulus is more likely to be supramaximal. In fact, Ross et al. (24) used PMS of the peroneal nerve to achieve supramaximal stimulation of the tibialis anterior (as documented by MEP recruitment curves) before and after a treadmill marathon. Polkey et al. (22) also demonstrated supramaximal activation of the quadriceps via PMS of the femoral nerve. We were able to induce contractions of greater than 90% MVC in the prefatigued state and greater than MVC after fatigue; expressed as a percentage of VOL + AUG rather than MVC (as subjects demonstrated incomplete activation), PMS was able to induce contractions of 72% before fatigue and 66% after fatigue. All of these exceed the recommendation of at least 65% MVC proposed by Kent-Braun (9).
The initial CAR of 0.84 indicates that these cyclists did not maximally activate their knee extensor muscles before fatigue. Similar results have been reported elsewhere (16,24) in endurance runners. This is perhaps not surprising given the unfamiliar nature of the task (maximal isometric contraction) and unusual posture (slightly reclined in hip extension) for subjects whose usual training modality is endurance cycling, which by nature is very submaximal and is performed in an upright posture with the hip flexed.
This PMS-based technique lends itself to exploration of many different facets of fatigue. For example, women have been shown to be more resistant to fatigue than men (6,9), although the mechanisms responsible for this difference are unclear. Magnetic stimulation of superficial nerves may be a useful technique to clarify if this difference is of peripheral or central origin. Magnetic stimulation may also be used to explore the mechanism of known ergogenic aids such as caffeine and carbohydrates. For example, Kalmar and Cafarelli (7,8) have used TMS to demonstrate that caffeine increases central excitability. PMS, however, is not without limitations. Its usefulness depends on the accessibility of a superficial nerve, and better contractions may be induced in lean subjects than in those with a significant amount of subcutaneous fat. The cost of the equipment is also substantially greater than the traditionally used electrical stimulation units. On the basis of measurements of magnetically elicited force as a percentage of VOL + AUG (72% and 66% before and after exercise, respectively), our technique did not provide supramaximal stimulation, so quantification of peripheral fatigue may be limited. In addition, our protocol was limited in that neither did we provide exogenous carbohydrate nor did we measure blood glucose levels. Nybo (20) demonstrated centrally mediated fatigue after 3 h of cycling with no carbohydrate supplementation. Although this could have contributed to the fatigue our subjects experienced, none reported any symptoms associated with low blood sugar (e.g., shakiness, dizziness, confusion, difficulty speaking). We plan to investigate the effect of carbohydrate supplementation in future studies.
In conclusion, these results clearly demonstrate that trained male cyclists experience significant central fatigue during prolonged cycling. PMS may be a better technique for identifying central fatigue than the traditionally used interpolated twitch technique. Used in combination with TMS, PMS can be used to pinpoint the locus of fatigue. Further work in this area should explore this technique to examine differences in fatigue between men and women and to examine central versus peripheral effects of ergogenic aids.
No outside funding was received for this work. The results of this study do not constitute endorsement by ACSM.
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Keywords:©2009The American College of Sports Medicine
ENDURANCE; EXERCISE; MUSCLE; CENTRAL ACTIVATION