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The effect of priming exercise on O2 uptake kinetics, muscle O2 delivery and utilization, muscle activity, and exercise tolerance in boys Alan R. Barker, Emily Trebilcock, Brynmor Breese, Andrew M. Jones, and Neil Armstrong

Abstract: This study used priming exercise in young boys to investigate (i) how muscle oxygen delivery and oxygen utilization, and muscle activity modulate oxygen uptake kinetics during exercise; and (ii) whether the accelerated oxygen uptake kinetics following priming exercise can improve exercise tolerance. Seven boys that were aged 11.3 ± 1.6 years completed either a single bout (bout 1) or repeated bouts with 6 min of recovery (bout 2) of very heavy-intensity cycling exercise. During the tests oxygen uptake, muscle oxygenation, muscle electrical activity and exercise tolerance were measured. Priming exercise most likely shortened the oxygen uptake mean response time (change, ±90% confidence limits; –8.0 s, ±3.0), possibly increased the phase II oxygen uptake amplitude (0.11 L·min−1, ±0.09) and very likely reduced the oxygen uptake slow component amplitude (–0.08 L·min−1, ±0.07). Priming resulted in a likely reduction in integrated electromyography (–24% baseline, ±21% and –25% baseline, ±19) and a very likely reduction in ⌬ deoxyhaemoglobin/⌬oxygen uptake (–0.16, ±0.11 and –0.09, ±0.05) over the phase II and slow component portions of the oxygen uptake response, respectively. A correlation was present between the change in tissue oxygenation index during bout 2 and the change in the phase II (r = –0.72, likely negative) and slow component (r = 0.72, likely positive) oxygen uptake amplitudes following priming exercise, but not for muscle activity. Exercise tolerance was likely reduced (change –177 s, ±180) following priming exercise. The altered phase II and slow component oxygen uptake amplitudes in boys following priming exercise are linked to an improved localised matching of muscle oxygen delivery to oxygen uptake and not muscle electrical activity. Despite more rapid oxygen uptake kinetics following priming exercise, exercise tolerance was not enhanced. Key words: oxidative metabolism, children, warm-up, muscle fibres. Résumé : Cette étude utilise l’exercice physique comme amorce chez de jeunes garçons pour examiner : (i) le mécanisme de la livraison d’oxygène, de l’utilisation de l’oxygène et de l’activité musculaire dans la modulation de la cinétique de la consommation d’oxygène au cours de l’exercice physique et pour vérifier si (ii) l’accélération de la cinétique de la consommation d’oxygène suivant l’amorce par l’exercice améliore la tolérance a` l’effort. Sept garçons âgés de 11,3 ± 1,6 ans effectuent un seul exercice (séance 1) ou une série d’exercices incorporant 6 min de récupération (séance 2); l’exercice consiste a` pédaler a` une intensité très élevée sur un vélo. Au cours de l’expérimentation, on évalue la consommation d’oxygène, l’oxygénation musculaire, l’activité myoélectrique et la tolérance a` l’effort. L’exercice d’amorce abrège vraisemblablement le temps moyen de réponse du consommation d’oxygène (modification, IC 90 % : –8,0 s, ±3,0), probablement par l’accroissement de l’amplitude du consommation d’oxygène durant la phase II (0,11 L·min–1, ±0,09) et fort probablement par la diminution de l’amplitude de la composante lente de la consommation d’oxygène (–0,08 L·min–1, ±0,07). L’amorce a vraisemblablement pour effet de diminuer l’iEMG (–24 %, ±21 % par rapport a` la référence, et –25 %, ±19 par rapport a` la référence) et de diminuer fort probablement ⌬ deoxyhaemoglobin/ ⌬ consommation d’oxygène (–0,16, ±0,11 et –0,09, ±0,05) durant la phase II et la composante lente de la réponse du consommation d’oxygène, respectivement. On observe une corrélation entre la variation de l’index d’oxygénation tissulaire au cours de la séance 2 et la variation de l’amplitude de la consommation d’oxygène durant la phase II (r = –0,72, vraisemblablement négative) et la phase lente (r = 0,72, vraisemblablement positive) suivant l’exercice d’amorce, mais pas en ce qui concerne l’activité musculaire. On observe vraisemblablement une diminution de la tolérance a` l’effort (variation de –177 s, ±180) a` la suite de l’exercice d’amorce. La modification chez les garçons de l’amplitude de la consommation d’oxygène durant la phase II et la composante lente suivant l’exercice d’amorce sont liées a` un meilleur appariement local entre la livraison musculaire de l’oxygène et le consommation d’oxygène, mais pas en ce qui concerne l’activité myoélectrique. Même en présence d’une cinétique de la consommation d’oxygène plus rapide a` la suite d’un exercice d’amorce, la tolérance a` l’effort n’est pas améliorée. [Traduit par la Rédaction] Mots-clés : métabolisme aérobie, enfants, échauffement, fibres musculaires.

Introduction The pulmonary oxygen uptake (V˙O2) kinetic response during exercise provides a noninvasive insight into muscle O2 uptake dynamics (Krustrup et al. 2009). Both cross-sectional and longitudinal studies have demonstrated growth and maturation to slow

V˙O2 kinetics during moderate (Fawkner et al. 2002; Breese et al. 2012), heavy (Fawkner and Armstrong 2004; Breese et al. 2010) and very heavy- (Breese et al. 2012) intensity exercise. These observations have been linked to age-related changes in intramuscular phosphate dynamics (Barker et al. 2008a), muscle O2 extraction

Received 26 April 2013. Accepted 6 September 2013. A.R. Barker, E. Trebilcock, B. Breese, A.M. Jones, and N. Armstrong. Children’s Health and Exercise Research Centre, Sport and Health Sciences, University of Exeter, Exeter EX1 2LU, UK. Corresponding author: Alan R. Barker (e-mail: [email protected]). Appl. Physiol. Nutr. Metab. 39: 308–317 (2014) dx.doi.org/10.1139/apnm-2013-0174

Published at www.nrcresearchpress.com/apnm on 24 September 2013.

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Barker et al.

(Leclair et al. 2012), muscle O2 delivery (Leclair et al. 2012) and (or) muscle fibre recruitment patterns (Breese et al. 2012). However, such mechanisms have been studied in isolation despite knowledge that these factors interact to limit V˙O2 kinetics during exercise (Poole et al. 2008). Investigating the limiting factors of V˙O2 kinetics in children or adolescents offers an alternative approach to understanding why V˙O2 kinetics are altered during growth and maturation. In this regard, a recent study found a bout of “priming” (or prior) very heavy-intensity exercise in 9- to 13-year-old boys to reduce the V˙O2 mean response time (MRT), increase the phase II V˙O2 amplitude and reduce the V˙O2 slow component amplitude during subsequent very heavy cycling exercise (Barker et al. 2010). These observations were reasoned to result from an improved muscle O2 availability, as inferred from near infrared spectroscopy (NIRS)derived deoxyhaemoglobin (HHb) kinetics (Koga et al. 2012). However, this study did not examine the dynamic matching of muscle HHb relative to V˙O2 during the exercise transient, which may provide additional insights into the factors limiting oxidative metabolism. A study on healthy young men found that a bout of heavy-intensity priming exercise resulted in more rapid V˙O2 kinetics during subsequent moderate-intensity exercise and this was related to an improved muscle O2 delivery as evidenced by an abolished HHb/V˙O2 “overshoot” shortly after the onset of exercise (Murias et al. 2011a). An overshoot in the HHb/V˙O2 dynamics shortly after the onset of exercise is present in young adults with a phase II V˙O2 time constant (␶) >21 s, but not in those with more rapid phase II kinetics (Murias et al. 2011b), suggesting the hypothesised “tipping point” (Poole et al. 2008) for an O2 delivery dependency on V˙O2 kinetics may reside in this region. Interestingly, the group mean phase II V˙O2 ␶ in the priming study by Barker et al. (2010) was 22 ± 7 s for 9- to 13-year-old boys, which sits strikingly close to the proposed tipping point for an O2 delivery dependency on V˙O2 kinetics. It is, however, currently unknown whether children display a HHb/V˙O2 overshoot at the onset of exercise and if so, whether this can be abolished with priming exercise. In addition to altered muscle O2 delivery, muscle fibre type and motor unit recruitment strategies are known to impact V˙O2 kinetics during exercise (Barstow et al. 1996; Jones et al. 2011), and have been linked to the priming effect on V˙O2 kinetics in adults (Burnley et al. 2002; Layec et al. 2009). Changes in muscle activation have been used to explain, in part, the slowing of V˙O2 kinetics in youth following experimental manipulation of pedal rate (Breese et al. 2011) and baseline metabolic rate (Breese et al. 2012). It may be predicted, therefore, that the altered V˙O2 phase II and slow component amplitudes previously reported by Barker et al. (2010) following priming exercise in youth may be related, in part, to altered muscle activation strategies. This hypothesis, however, remains to be tested. As the faster V˙O2 kinetics following priming exercise is consistent with an improved oxidative contribution to energy turnover and a smaller O2 deficit, an enhanced exercise tolerance may be anticipated (Burnley and Jones 2007). However, a potential enhancement in exercise tolerance is dependent on the recovery of intramuscular high-energy phosphates and fatigue-inducing metabolites (e.g., Pi and H+) (Chidnok et al. 2013), which will be related to both the intensity of the priming bout and the recovery duration between bouts (Bailey et al. 2009). We are, however, not aware of any study that has investigated the potential for priming exercise to improve exercise tolerance in youth. The purpose of the present study was to use priming exercise to further our understanding of the limiting factors of V˙O2 kinetics in boys. Specifically, we were interested in establishing (i) how muscle O2 delivery and O2 utilization, and muscle activity may limit V˙O2 kinetics during very heavy exercise; and (ii) whether priming exercise can improve exercise tolerance. We hypothesised that (i) the altered phase II and slow component V˙O2 amplitudes following priming exercise will be related to an improved

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matching of muscle O2 delivery relative to V˙O2 and a blunted increase in muscle activity over time; and (ii) the priming-induced accelerated V˙O2 will enhance exercise tolerance.

Materials and methods Participants Seven male participants volunteered to take part in the study (age: 11.3 ± 1.6 years; stature: 1.50 ± 0.13 m and body mass: 42.0 ± 11.1 kg). All participants and their parent(s)/guardian(s) provided informed assent and consent respectively, to partake in the project, which was approved by the institutional ethics committee. The participants were healthy, recreationally active, and showed no contraindications to exercise to exhaustion. Experimental protocol Participants visited the laboratory on 4 separate occasions over a 3-week period, with at least 24 h of rest provided between visits. All participants arrived at the laboratory in a rested state and were requested to refrain from food and caffeine for at least 2 h prior to testing. The first laboratory session consisted of basic anthropometrical measures and an exercise test to determine maximal oxygen uptake (V˙O2max) and the gas exchange threshold (GET). During the subsequent 3 visits, the participants completed either a single bout or double bouts of very-heavy-intensity exercise. All tests were performed on an electronically braked cycle ergometer (Lode, Netherlands). Visit 1: Incremental exercise A combined ramp and supra-maximal exercise test to exhaustion was employed to determine V˙O2max and the GET (Barker et al. 2011b). The highest 15-s averaged V˙O2 during the ramp or supramaximal test was taken as V˙O2max. The V˙O2 at the GET was identified as a disproportionate increase in expired carbon dioxide (V˙CO2) relative to V˙O2 (Beaver et al. 1986) and verified using the ventilatory equivalents for V˙O2 and V˙CO2 (Wasserman et al. 2005). Visits 2– 4: Square-wave exercise Each participant completed, in a randomized order, 3 exercise protocols that consisted of a either a single or double bout of square-wave exercise: (i) 6 min of cycling at 10 W followed by a single 6-min exercise transition to a power output equivalent to 60% ⌬ (60% of the difference between the GET and V˙O2max); and (ii–iii) 6 min of cycling at 10 W followed by two 6-min exercise transitions to a power output equivalent to 60% ⌬, with 6 min of cycling at 10 W used as the recovery between the transitions. To provide a measure of exercise tolerance, the participants were asked to exercise until exhaustion in protocol 1 and during bout 2 in protocol 3. Experimental measures Breath by breath gas exchange and ventilation were determined using a metabolic cart (Metalyser 3B Cortex, Biophysik, Leipzig, Germany) that was calibrated prior to each test. Heart rate was recorded using short range radio telemetry (Polar Vantage NV, Polar Electro, Kempele, Finland). Changes in the concentrations of O2Hb and HHb of the left leg were measured noninvasively using a commercially available nearinfrared spectrometer (NIRO-300, Hamamatsu Photonics KK), as previously described (Barker et al. 2010). The emitter-detector probe was affixed over the vastus lateralis muscle, defined as the midway point between the greater trochanter and lateral epicondyle of the left leg, using double-sided adhesive tape and an elastic bandage to prevent movement during data collection. As the relative contribution of haemoglobin and myoglobin to the NIRS signal is currently unknown, the dynamics of O2Hb and HHb were considered to reflect changes in both haemoglobin and myoglobin concentrations. The HHb signal is considered to reflect the dynamic (im)balance between muscle O2 supply and O2 utilization Published by NRC Research Press

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and was used to provide a description of muscle O2 extraction (Koga et al. 2012). In addition, the tissue oxidation index (TOI) was used to describe the oxygenation of the muscle during exercise. All NIRS variables were collected a 6 Hz, averaged into 1-s intervals and expressed as a change from baseline, taken after 10 min of seated rest on the cycle ergometer. The neuromuscular activity of the vastus lateralis muscle of the right leg was determined using a 4-channel surface electromyography (EMG) system (ME3000PB Muscle Tester, Mega Electronics), as previously described (Breese et al. 2012). Briefly, following site preparation, graphite snap electrodes (Unilect 40713, Unomedical, Stonehouse, UK) were adhered to the skin surface in a bipolar arrangement with an interelectode distance of 20 mm at the midway point between the greater trochanter and lateral epicondyle of the right leg. The ground electrode was placed on the rectus femoris muscle of the right leg. Additional experiments demonstrated that the use of the rectus femoris for the ground electrode produced a similar EMG profile during square-wave exercise when compared with the tibial head (data not presented). An elastic bandage was wrapped around each participant’s leg to prevent displacement of the electrodes during cycling. All EMG measurements were sampled at 1000 Hz, between a bandwith of 8–500 Hz with a common mode rejection ratio of 110 dB, gain of 305 and maximum noise of 1.6 ␮V. The raw EMG signals were amplified (amplifier input impedance > 1 M⍀), collected online and stored on a personal computer using MegaWin software (Mega Electronics) for subsequent analysis. Data analysis Breath by breath changes in V˙O2 for each square-wave exercise bout were analyzed using methodology previously described from our laboratory (e.g., Fawkner and Armstrong 2004; Barker et al. 2010; Breese et al. 2012). Following the removal of data lying greater than 3 SD from a local moving mean, the repeat squarewave exercise transitions for bout 1 and bout 2 were interpolated to 1 s and averaged into 5-s data bins. The averaged V˙O2 response for bout 1 and bout 2 were baseline corrected by subtracting the mean V˙O2 between –60 and –15 s from the exercise response. Following removal of phase I (cardio-dynamic) by omitting the initial 15 s of data (Hebestreit et al. 1998), the phase II portion of the V˙O2 response was characterised using the following nonlinear equation: (1)

V˙O2(t) ⫽ ⌬V˙O2A × [1 ⫺ e⫺(t⫺TD)/␶]

where V˙O2(t), V˙O2A, TD and ␶ represent the value of V˙O2 at a given time (t), the amplitude of V˙O2 from baseline to its asymptote, time delay and the time constant of the response, respectively. Following the methods of Rossiter et al. (2002), eq. 1 was initially fit up to the first 60 s of exercise and then increased iteratively by 5 s to end-exercise (LabView, version 6.1, National Instruments, Newbury, UK). The best fit curve for the phase II portion of the response was established using (i) a plot of the V˙O2 ␶ against time, to identify the point at which the influence of the V˙O2 slow component lengthened the estimated ␶ following an initial plateau; and (ii) deviation from an optimal fitting of the model as judged by a systematic departure of the model’s residuals. The phase II parameter estimates from eq. 1 were then resolved by least-squares non-linear regression (GraphPad Prism, GraphPad Software, San Diego, Calif., USA). The magnitude of the V˙O2 slow component was calculated as the difference between the mean of the final 30 s at 6 min of exercise and the phase II asymptote. The V˙O2 slow component amplitude was also expressed in relative terms using V˙O2 at 6 min of exercise. To provide a description of the overall kinetic response (mean response time: MRT), eq. 1 with TD constrained to 0 s, was fit from exercise onset to 6 min of exercise.

The muscle HHb profiles were averaged into 5-s data bins, timealigned to exercise onset, and ensemble averaged to yield a single response for the control and primed exercise conditions. The HHb kinetics (primary and slow component phases) were modeled in a similar fashion to the procedures described for V˙O2 above, but with some slight modifications. The exponential-like increase in HHb after the onset of exercise occurred after a discernible delay. The time at which the exponential-like increase in HHb commenced was identified as the point of a 1 SD increase above baseline (DeLorey et al. 2003). Equation 1 was then applied to resolve the HHb TD and ␶ following removal of the data preceding the exponential-like increase. The HHb MRT was calculated by summing TD and ␶ to provide an overall description of the kinetics in the primary phase. Changes in TOI were described at baseline and 6 min of exercise. The ratio of HHb to V˙O2 was calculated using 2 different methods, as described by Murias et al. (2011a), to investigate the impact of priming exercise on the matching of O2 delivery to O2 utilization. First, the absolute ratio of HHb and V˙O2 (HHb/V˙O2) was calculated at baseline, the primary amplitude and at 6 min of exercise. Second, the ratio of the index of ⌬HHb to ⌬V˙O2 (⌬HHb/ ⌬V˙O2) was determined by normalizing the respective response profiles with 0% and 100% representing baseline and 6 min of exercise, respectively. The ⌬HHb and ⌬V˙O2 signals were timealigned by deleting the initial 15 s of the V˙O2 data to account for phase I. The mean ⌬HHb/⌬V˙O2 was calculated over the phase II and slow component phases of the V˙O2 kinetic response for each individual. At any given time a ⌬HHb/⌬V˙O2 ratio of 1.00 represents an equivalent matching between muscle O2 delivery and O2 utilization to that observed at 6 min of exercise. Conversely, a ⌬HHb/ ⌬V˙O2 ratio >1.00 or 50%) of the 90% CL lay between beneficial and harmful. Conversely, an effect was deemed unclear when the likelihood of a beneficial and harmful effect was >5%. Pearson’s correlation coefficients and their 90% CL were used to explore the relationship between changes in V˙O2 kinetics and mechanistically important variables (e.g., muscle TOI) following priming exercise. Probabilistic-based inferences for the smallest worthwhile correlation were calculated, as described above for the changes in means. Descriptive statistics were calculated using SPSS (version 19.0, Chicago, Ill., USA) and are presented as means ± SD.

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Fig. 1. Mean oxygen uptake (V˙O2) profile during bout 1 (open circles) and bout 2 (filled circles). The onset of exercise is illustrated by the vertical dotted line. Note the increased phase II V˙O2 amplitude and the reduced V˙O2 slow component amplitude in bout 2.

Results Ramp and supra-maximal exercise The group mean V˙O2max, maximal heart rate and peak power output was 2.12 ± 0.56 L·min−1, 192 ± 8 beats·min−1 and 170 ± 57 W, respectively. The GET occurred at a V˙O2 of 1.20 ± 0.28 L·min−1, which represented 59% ± 16% V˙O2max. The mean power output at 60% ⌬ was 124 ± 47 W. V˙O2 kinetics The group mean V˙O2 response during the control and primed cycling exercise bouts is shown in Fig. 1. Table 1 provides the inferential statistics for the V˙O2 kinetic response parameters. Baseline V˙O2 was possibly lower in bout 2 compared with bout 1 (effect size (ES) = –0.21). The influence of priming exercise on the phase II ␶ (ES = −0.35) and TD (ES = −0.17) was unclear but the phase II amplitude (ES = 0.23) and gain (ES = 0.74) were possibly and very likely higher, respectively, in bout 2 compared with bout 1. A slow component was manifest in all V˙O2 responses and was lower both in absolute (likely, ES = −0.92) and relative terms (very likely, ES = −1.17) in bout 2 compared with bout 1. The V˙O2 MRT was most likely reduced in bout 2 (ES = −1.07). Muscle oxygenation kinetics The group mean HHb and TOI response profiles during bout 1 and bout 2 are shown in Fig. 2 with the HHb kinetic parameters presented in Table 2. Bout 2 was associated with a very likely reduced HHb (ES = −0.62) and a very likely higher TOI (bout 1: 66.8 ± 2.9 vs. bout 2: 71.5 ± 3.7; change, ±90%CL: 4.7, ±2.4, ES = 1.23) at baseline. The HHb TD was very likely reduced in bout 2 (ES = −0.99), although priming exercise had an unclear effect on HHb ␶ (ES = 0.04) and MRT (ES = −0.44). The primary amplitude for HHb was likely higher (ES = 0.31) in bout 2 but priming exercise had an unclear effect on the HHb slow component (ES = 0.11). Endexercise HHb was possibly lower in bout 2 but the increase in HHb above baseline was possibly higher in bout 2 (bout 1: 8.2 ± 4.3 vs. bout 2: 9.4 ± 3.6; change: 1.3, ±1.1, ES = 0.28). End TOI (bout 1: 52.4 ± 4.5 vs. bout 2: 54.2 ± 4.5; change: 1.8, ±1.8, ES = 0.35) was likely higher in bout 2. Baseline TOI in bout 2 had a likely positive relationship with the change in the phase II V˙O2 amplitude following priming exercise (r = 0.57, ±0.54) but an unclear relationship with the change in the V˙O2 slow component amplitude (r = −0.47, ±0.59). The delta change in TOI from baseline to 6 min during bout 2 had a likely negative relationship with the change in the phase II V˙O2 amplitude (r = −0.72, ±0.43) and a likely positive relationship with the slow component (r = 0.72, ±0.43) amplitude, following priming exercise (Fig. 3). Matching of HHb to V˙O2 The magnitude of the absolute HHb/V˙O2 ratio was lower in bout 2 compared with bout 1 at baseline (very likely, ES = −0.74), the primary phase (likely, ES = −0.33) and 6 min (likely, ES = −0.29) of exercise (Table 2). The group mean normalized dynamics of ⌬HHb/⌬V˙O2 are shown in Fig. 4 and show a profoundly altered adjustment of ⌬HHb relative to ⌬V˙O2 in bout 1 (Fig. 4A) compared

with bout 2 (Fig. 4B). This was captured in the normalized ⌬HHb/ ⌬V˙O2 response (Fig. 4C). The mean normalized ⌬HHb/⌬V˙O2 response was likely higher (overshoot, ES = 0.88) than unity in bout 1 and very likely lower than unity (“undershoot”, ES = −1.33) in bout 2 over the phase II V˙O2 region. At 6 min of exercise, the normalized ⌬HHb/⌬V˙O2 ratio remained likely higher than unity for bout 1 (1.02 ± 0.02, ES = 0.81) but was unclear for bout 2 (1.00 ± 0.02, ES = −0.18). The mean normalized ⌬HHb/⌬V˙O2 was very likely reduced in bout 2 compared with bout 1 over both the phase II (bout 1: 1.08 ± 0.11 vs. bout 2: 0.92 ± 0.07; change: –0.16, ±0.11, ES = −1.47) and slow component (bout 1: 1.05 ± 0.04 vs. bout 2: 0.96 ± 0.05; change: –0.09, ±0.05, ES = −1.64) phases. iEMG The group mean iEMG response during bout 1 and bout 2 is presented in Fig. 5. The mean iEMG response in bout 2 was likely reduced at baseline (bout 1: 100% ± 0% vs. bout 2: 82% ± 24%; change: –18, ±18, ES = –0.91), up until the onset of the V˙O2 slow component (bout 1: 253% ± 55% vs. bout 2: 229% ± 79%; change: –24, ±21, ES = –0.30) and from the onset of the V˙O2 slow component to 6 min of exercise (bout 1: 251% ± 60% vs. bout 2: 227% ± 80%; change: –25, ±19, ES = –0.31). The appearance of a linear slope for iEMG over the V˙O2 slow component portion of the response was unclear for bout 1 (0.07 ± 0.17, ES = 0.34) and bout 2 (–0.03 ± 0.08, ES = –0.28). Likewise, the linear iEMG slope from the onset of the V˙O2 slow component to 6 min of exercise was unclear between bouts (bout 1: 0.07 ± 0.17 vs. bout 2: –0.03% ± 0.08%; change: –0.09, ±0.14, ES = –0.61). The relationship between the V˙O2 slow component and the change in iEMG over the slow component region was unclear for bout 1 (r = –0.31, ±0.64) and bout 2 (r = 0.02, ±0.68). The change in the iEMG amplitude between bout 1 and 2 shared an unclear relationship with the change in the phase II (r = 0.22, ±0.66) and slow component (r = –0.16, ±0.67) V˙O2 amplitudes. Exercise tolerance Priming exercise resulted in a likely reduction in exercise tolerance (bout 1: 739 ± 248 s vs. bout 2: 562 ± 181 s; change: –177, ±180, ES = –0.71), with an impaired exercise tolerance observed in all but 1 participant. Published by NRC Research Press

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Table 1. Oxygen uptake kinetics during bout 1 and bout 2. Variable

Bout 1 (mean ± SD)

Bout 2 (mean ± SD)

Change, ±90% CL

Inference

Baseline V˙O2 (L·min−1) Phase II ␶ (s) Phase II TD (s) Phase II V˙O2 amplitude (L·min−1) Phase II gain (mL·min−1·W−1) V˙O2 slow component onset (s) V˙O2 slow component amplitude (L·min−1) V˙O2 slow component relative amplitude (%) End-exercise V˙O2 (L·min−1) End-exercise V˙O2 gain (mL·min−1·W−1) V˙O2 mean response time (s)

0.74±0.09 25.5±2.2 9.8±2.9 0.93±0.34 9.2±0.9 159±60 0.12±0.10 6.3±3.4 1.80±0.49 10.3±1.0 45.1±7.4

0.72±0.10 23.5±6.4 9.3±2.0 1.04±0.45 10.1±1.2 187±40 0.05±0.02 2.8±1.3 1.81±0.50 10.6±1.3 37.1±5.4

−1.9, ±3.5 −0.5, ±1.7 0.11, ±0.09 0.9, ±0.6 29, ±36 −0.08, ±0.07 −3.5, ±2.6 0.01, ±0.04 0.3, ±0.3 −8.0, ±3.0

Unclear Unclear Possibly higher Very likely higher Likely higher Likely lower Very likely lower Trivial Possibly higher Most likely faster

Note: Effect represents the magnitude of the change by subtracting bout 2 from bout 1. 90% CL represents the uncertainty of the observed effect. The 90% CL of the true effect can be established by adding and subtracting the 90% CL to the effect. Inference represents the probabilistic inference that the magnitude of the observed effect is different from the smallest worthwhile change using Cohen’s standardized effect of 0.2 (see methods for details). CL, confidence limit; V˙O2, oxygen uptake; TD, time delay.

Fig. 2. Mean deoxyhaemoglobin (HHb) (A) and TOI (B) dynamics during bout 1 (open circles) and bout 2 (filled circles). The vertical dotted line signifies the onset of exercise. Note that in bout 2 the tissue oxidation index (TOI) is elevated at baseline and throughout the exercise transition.

Discussion In agreement with our earlier study (Barker et al. 2010), priming exercise resulted in a speeding of the V˙O2 MRT because of an increase in the phase II V˙O2 amplitude and a reduced V˙O2 slow

component. Changes in the phase II V˙O2 ␶ were unclear. However, the present study has revealed the following novel findings in young boys: (i) priming exercise increased baseline muscle TOI and caused subtle adjustments to the dynamics of HHb by reducing the HHb TD; changes in the HHb primary ␶ and MRT were unclear; (ii) priming exercise reduced the normalized ⌬HHb/⌬V˙O2 ratio by abolishing the overshoot that was present in bout 1 and causing an undershoot in bout 2; (iii) priming exercise reduced muscle activity as inferred by a lower iEMG amplitude in bout 2 compared with bout 1; (iv) large relationships between indices of enhanced muscle O2 availability (e.g., baseline TOI, ⌬ TOI) during bout 2 and the change in the V˙O2 phase II and slow component amplitudes following priming exercise were found. In contrast, changes in iEMG following priming exercise did not correlate with the altered V˙O2 response; and (v) exercise tolerance was reduced by ⬃24% on average following priming exercise. Collectively, these findings suggest that localized changes in both muscle O2 delivery and muscle O2 utilization, and not muscle activity, play an important role in limiting V˙O2 kinetics during very heavy exercise in youth. However, despite the more rapid adjustment of oxidative metabolism brought about by priming exercise, this did not improve exercise tolerance. Poole et al. (2008) have proposed that a “tipping point” may exist with regard to the dependence of the phase II V˙O2 ␶ on muscle O2 delivery. In this regard, it has been suggested that when the phase II V˙O2 ␶ is greater than 21 s, the V˙O2 kinetic response becomes, in part, muscle O2 delivery-dependent (Murias et al. 2011a, 2011b). This is based on the finding that the normalized ⌬HHb/⌬V˙O2 ratio demonstrated an overshoot in adult participants with a phase II V˙O2 ␶ greater than 21 s, suggesting a greater rate of change in fractional O2 extraction relative to V˙O2, possibly because of a reduced microvascular O2 delivery (Murias et al. 2011b). It is therefore interesting that in bout 1 of the current study the mean phase II V˙O2 ␶ was 25.5 s and an overshoot in the normalized ⌬HHb/⌬V˙O2 ratio (1.08) was observed over the phase II V˙O2 region. This overshoot is identical to (1.08) that previously reported in young adults with similar phase II kinetics (Murias et al. 2011a) and may suggest that the phase II V˙O2 ␶ is, in part, limited by muscle O2 delivery in young people. In support of this reasoning is evidence of a slowed phase II V˙O2 ␶ in children during cycling exercise during hypoxia (15% O2) (Springer et al. 1991). However, evidence of a speeding of the phase II V˙O2 ␶ during conditions when muscle O2 delivery is elevated is needed to fully support the view that muscle O2 availability limits V˙O2 kinetics in youth. In the current study the priming intervention elevated muscle O2 availability during bout 2, as evidenced by the increased TOI at baseline and throughout exercise. In addition, as recently shown in young healthy adults (Murias et al. 2011a), priming exercise Published by NRC Research Press

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Table 2. Muscle oxygenation kinetics during bout 1 and bout 2 cycling conditions. Variable

Bout 1 (mean ± SD)

Bout 2 (mean ± SD)

Change, ±90% CL

Inference

HHb baseline (a.u.) HHb primary TD (s) HHb primary ␶ (s) HHb primary MRT (s) HHb primary amplitude (a.u.) HHb slow component amplitude (a.u.) HHb slow component amplitude (%) HHb at 6 min (a.u.) HHb/V˙O2 baseline (a.u./L·min−1) HHb/V˙O2 primary (a.u./L·min−1) HHb/V˙O2 at 6 min (a.u./L·min−1)

−4.6±2.8 9.0±2.8 14.7±6.1 23.7±6.1 7.0±2.9 1.2±1.6 9.0±16.6 3.6±3.7 −6.07±3.23 1.47±1.57 2.06±1.95

−6.9±3.5 6.2±2.1 15.0±3.1 21.2±3.7 8.1±3.3 1.3±0.5 14.8±7.2 2.6±3.6 −9.23±4.11 0.75±2.19 1.36±2.24

−2.2, ±0.9 −2.8, ±1.6 0.2, ±3.9 −2.6, ±3.9 1.1, ±0.9 0.1, ±1.1 5.9, ±15.7 −1.0, ±0.9 −3.16, ±1.24 −0.72, ±0.58 −0.70, ±0.47

Very likely lower Very likely lower Unclear Unclear Likely higher Unclear Unclear Possibly lower Very likely lower Likely lower Likely lower

Note: Effect represents the magnitude of the change by subtracting bout 2 from bout 1. 90% CL represents the uncertainty of the observed effect. The 90% CL of the true effect can be established by adding and subtracting the 90% CL to the effect. Inference represents the probabilistic inference that the magnitude of the observed effect is different from the smallest worthwhile change using Cohen’s standardized effect of 0.2 (see Materials and methods section for details). CL, confidence limit; HHb, deoxyhaemoglobin; TD, time delay; MRT, mean response time; V˙O2, oxygen uptake.

Fig. 3. The relationship between the change in tissue oxidation index (TOI) from baseline to 6 min of exercise in bout 2 to the change in the phase II (A) and slow component (B) oxygen uptake (V˙O2) amplitudes following priming exercise.

reduced the normalized ⌬HHb/⌬V˙O2 ratio during phase II V˙O2 to 0.92 on average, suggesting a better matching of localized muscle O2 delivery to O2 utilization during the exercise transient, implying that a reduced rate of O2 extraction was required to meet the increased V˙O2. However, despite this elevated muscle O2 availability in bout 2, an unclear effect for priming exercise on the phase II

V˙O2 ␶ was found, which is in agreement with an earlier study from our laboratory using the same priming intervention in 9- to 13-year-old boys (Barker et al. 2010). This finding therefore supports the notion that the phase II V˙O2 ␶ in young boys is principally limited by intramuscular metabolic factors, likely related to the creatine kinase mediated splitting of muscle phosphocreatine (PCr) and (or) the activity of rate limiting oxidative enzymes (Meyer 1988; Kindig et al. 2005; Poole et al. 2008). Such a conclusion is indirectly supported by the similar kinetics for phase II V˙O2 and muscle PCr at the onset and offset of exercise in young people (Barker et al. 2008b). An interesting finding in the current study was the presence of a reduced HHb TD following priming exercise. This is likely to reflect an earlier mismatch between muscle O2 delivery and utilization during bout 2, suggesting an enhanced O2 extraction early (initial ⬃ 5 s) in the exercise transient. This occurred despite an elevated muscle O2 availability during the baseline of bout 2, and may reflect a more rapid activation of oxidative metabolism, possibly because of an increased activity of rate-limiting oxidative enzymes, such as pyruvate dehydrogenase (Gurd et al. 2009), and (or) activation of the mitochondrial electron transport chain (Gandra et al. 2012). Following the HHb TD, however, HHb rose with exponential-like kinetics but the resulting HHb ␶ and MRT (TD + ␶) was found to have an unclear effect following priming exercise, suggesting the overall dynamic balance between muscle O2 delivery and O2 utilization during the primary phase was unaltered by priming exercise. While this finding agrees with previous studies in adults (DeLorey et al. 2007; Murias et al. 2011a), it contrasts the recent work form our laboratory showing no changes in the HHb profile (TD, ␶ or MRT) following priming exercise in young boys (Barker et al. 2010). Such inter-study differences in HHb dynamics have also been reported across similar adult studies (DeLorey et al. 2007; Gurd et al. 2009; Murias et al. 2011a), and may be explained by the heterogeneity in the HHb response dynamics that is observed across the quadriceps muscle (Koga et al. 2007). In agreement with earlier investigations in children and adults (Burnley et al. 2001, 2002; Bailey et al. 2009; Barker et al. 2010), the phase II V˙O2 amplitude was elevated following priming exercise, resulting in an increase in the V˙O2 phase II gain. As shown previously in adults (Burnley et al. 2001), this was independent of an elevated baseline metabolic rate, as baseline V˙O2 during bout 2 had returned to, and was possibly lower than bout 1. Based on unchanged HHb (muscle O2 extraction) dynamics and an increase in bulk blood flow, we recently interpreted this to be caused by an improved muscle O2 delivery (Barker et al. 2010). The current study extends this interpretation as the change in the phase II V˙O2 amplitude following priming exercise was positively correlated Published by NRC Research Press

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Fig. 4. Group mean normalised deoxyhaemoglobin (HHb) (open circles) and oxygen uptake (V˙O2) (filled circles) dynamics during bout 1 (A) and bout 2 (B). Panel C expresses these changes as a ratio (⌬HHb/⌬V˙O2) for bout 1 (open squares) and bout 2 (filled squares). Note that a ⌬HHb/⌬V˙O2 “overshoot” is present in bout 1, but this is abolished to an “undershoot” in bout 2.

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Fig. 5. Mean integrated electromyography (iEMG) during bout 1 (open circles) and bout 2 (filled circles). The vertical dotted line signifies the onset of exercise.

with bout 2 baseline TOI (r = 0.57) and negatively with the delta change in TOI during bout 2 (r = –0.72). However, in addition to a potential role for muscle O2 delivery, the elevated phase II V˙O2 amplitude following priming exercise has been linked to an increase in muscle activation (Burnley et al. 2002; Layec et al. 2009). For example, Burnley et al. (2002) reported an elevated iEMG during heavy-intensity cycling following priming exercise, which was proportional to the rise in the phase II V˙O2 amplitude. In the current study, however, we observed a reduced iEMG amplitude during the phase II V˙O2 portion of the response, which according to previous interpretations in adults (Burnley et al. 2002; Bailey et al. 2009; Layec et al. 2009), suggests a reduction in motor unit recruitment. Unlike indices in muscle O2 availability, however, the reduction in iEMG did not correlate with the increase in the phase II V˙O2 amplitude following priming exercise. This finding does not support a mechanistic role for muscle activation in altering the phase II V˙O2 amplitude in young boys following priming exercise, which is in agreement with the adult data of Scheuermann et al. (2001). Rather, coupled with the elevated muscle O2 availability at the onset of exercise, priming exercise may have increased the distribution of O2 to the active muscle fibres, with the outcome being an elevated phase II V˙O2 amplitude. An alternative explanation for the increased phase II V˙O2 amplitude in the current study could relate to the possibility that muscle efficiency was reduced following priming exercise. For example, Sahlin et al. (2005) reported an elevated phase II V˙O2 amplitude following high-intensity priming exercise under conditions of elevated muscle and blood lactate and reduced muscle PCr, which remained until end exercise (10 min). These authors and others (Jones et al. 2008) have suggested that residual muscle fatigue from the initial priming bout may reduce muscle efficiency. However, not all data support this notion (Layec et al. 2009), and it is pertinent to note that the increased O2 cost of exercise in the present study was abolished by 6 min of exercise (see Fig. 1), suggesting that if exercise efficiency was altered in the present study, it was confined to the earlier portion of the bout. Over 80% of the V˙O2 slow component during high-intensity exercise has been shown to originate from the exercising limbs (Poole et al. 1991) with the progressive recruitment of muscle fibres, specifically high-order type II fibres, considered to be the main mechanism (Barstow et al. 1996; Krustrup et al. 2004; Endo et al. 2007). In this context it is pertinent to note that during bout 1 or bout 2 we did not observe a meaningful linear rise in iEMG over Published by NRC Research Press

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Barker et al.

time over the V˙O2 slow component region. Furthermore, while priming exercise reduced both the relative (56%) and absolute (58%) V˙O2 slow component amplitude in the current study, this was not correlated with iEMG, despite the reduced iEMG amplitude in bout 2. This lack of an association between changes in iEMG and the V˙O2 slow component corroborates some (Scheuermann et al. 2001) but not all (Burnley et al. 2002; Bailey et al. 2009) previous adult work, and provides support for the notion that the progressive recruitment of muscle fibres per se, is not mechanistically linked to the development of the V˙O2 slow component in young boys. Our study cannot, however, discount the possibility that the metabolic cost associated with the recovery of previously active muscle fibres (e.g., Vanhatalo et al. 2011) plays an important role in the development of the V˙O2 slow component in young people. An alternative explanation for the reduced V˙O2 slow component amplitude in the current study may be related to an elevated bulk O2 delivery and (or) the matching of muscle O2 availability to O2 utilization (DeLorey et al. 2007; Gurd et al. 2009; Murias et al. 2011a). We recently reported in young boys that a reduced V˙O2 slow component following priming exercise was observed with an elevated cardiac output (bulk blood flow) to V˙O2 ratio, although it could not be concluded that the elevated bulk blood flow resulted in an increased muscle O2 availability (Barker et al. 2010). The present study extends this work and provides evidence that an increase in muscle O2 availability was related to the reduction in the V˙O2 slow component amplitude. First, we observed a correlation between the change in the V˙O2 slow component following priming exercise and TOI at baseline of bout 2 (r = –0.47) and the change in TOI from baseline to 6 min of exercise in bout 2 (r = 0.72). Second, the mean normalized ratio of ⌬HHb/⌬V˙O2 over the slow component region was markedly reduced from 1.05 to 0.96 with priming exercise, suggesting a better matching of localized muscle O2 delivery to V˙O2. It has been proposed that the enhanced muscle O2 availability afforded by priming exercise reduces the rate of fatigue development, presumably by reducing the muscle metabolic perturbation (e.g., fall in PCr and increase in Pi and H+) (Hogan et al. 1999), and the requirement to recruit additional (high-order) muscle fibres during high-intensity exercise (Jones et al. 2011). This may account for the reduced iEMG amplitude reported following priming exercise in the present study, but as mentioned earlier, no meaningful correlation was observed between changes in iEMG and the V˙O2 kinetic response. Despite observing faster overall V˙O2 kinetics, and presumably a reduction in the muscle O2 deficit following priming exercise, we observed a 24% reduction in time to exhaustion (likely reduced), with 6 out of the 7 participants having a reduced exercise tolerance. This finding agrees with some previous adult studies that have reported an impaired exercise tolerance following very heavy intensity priming exercise (Carter et al. 2005; Ferguson et al. 2007). However, others have reported either an unchanged (Koppo and Bouckaert 2002) or enhanced exercise tolerance (Bailey et al. 2009) following priming exercise. It is well established that the tolerable duration of high-intensity exercise is well described by a hyperbolic function of time, the asymptote of which is termed critical power (CP), and the curvature constant (W=), which describes a finite amount of work that can be completed above CP (Jones et al. 2010). In adults (Poole et al. 1988), but not children (Barker et al. 2011a), constant work-rate exercise above CP until exhaustion occurs with the attainment of V˙O2max because of the presence of the V˙O2 slow component. Consequently, the kinetics of V˙O2, V˙O2max, CP and W= all have the potential to determine exercise tolerance during high-intensity exercise (Burnley and Jones 2007). However, as priming exercise does not alter CP or V˙O2max (Ferguson et al. 2007; Vanhatalo and Jones 2009), and the V˙O2 slow component was attenuated following priming exercise in the current study, our observed reduction in exercise tolerance is likely explained by an altered W=. Indeed, a recent study has suggested that the res-

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toration of muscle metabolic status (e.g., PCr, H+) towards baseline levels is likely to be of importance in determining exercise tolerance above CP (Bailey et al. 2009), and has recently been confirmed experimentally in humans (Chidnok et al. 2013). In the context of the present study it is likely that the 6 min recovery duration employed was insufficient for sufficient recovery of W= (related to restoration of muscle PCr and H+) prior to the second bout of exercise. Therefore, although children are reportedly characterized with a more rapid muscle metabolic recovery following highintensity exercise compared with adults (Ratel et al. 2006), the 6-min recovery duration used between the exercise bouts in the current study is unlikely to have been sufficient to restore muscle PCr and H+ back to baseline prior to the second bout of exercise. A recovery period of ≥6 min is therefore likely to be needed to realize an enhancement in high-intensity exercise tolerance following priming exercise of an intensity (60% ⌬) and duration (6 min) used in the current study. Considerations and limitations The findings in the present study should be viewed in relation to the following considerations. First, the normalized ⌬HHb/⌬V˙O2 ratio is typically expressed relative to the steady-state responses achieved during moderate intensity exercise (Murias et al. 2011a; 2011b). As a steady-state is not observed during very heavy exercise (i.e., >CP) in youth, the normalized ⌬HHb/⌬V˙O2 ratio was expressed relative to the amplitudes obtained at 6 min of exercise. Despite this different approach, the magnitude of the overshoot in normalized ⌬HHb/⌬V˙O2 over the phase II region was similar to that previously reported in young adults (Murias et al. 2011b), and was meaningfully blunted following priming exercise, which is also consistent with previous adult work during moderate exercise (Murias et al. 2011a; De Roia et al. 2012). Second, similar to previous studies documenting changes in HHb relative to V˙O2 (DeLorey et al. 2007; Murias et al. 2011b; De Roia et al. 2012), we obtained the HHb signal from a single probe positioned over the vastus lateralis muscle. As large variations in the HHb response dynamics, and by inference the matching of muscle O2 delivery to utilization, exist both within and between the quadriceps muscle (Koga et al. 2007, 2011), this may limit the fidelity in relating HHb dynamics to whole-body V˙O2. Finally, muscle activity in the present study was quantified using surface iEMG over the vastus lateralis muscle, which is in accord with previous adult research in this area (Scheuermann et al. 2001; Bailey et al. 2009). Although the vastus lateralis muscle is progressively recruited throughout very heavy exercise, at least in adults (Endo et al. 2007), it cannot be discounted that the use of a single site iEMG measure in the current study may have resulted in an incomplete picture with regard to changes in muscle activity following priming exercise. For example, some adult studies have undertaken a more comprehensive measure of muscle activity (gluteus maximus, vastus lateralis, vastus medialis) following priming exercise and observed an increase in iEMG amplitude over the phase II V˙O2 portion of the response (Burnley et al. 2002). However, it should be noted that the iEMG data in the current study are consistent with a recent study documenting an increase in iEMG over the V˙O2 slow component region in men but not boys (Breese et al. 2012).

Conclusions The present study employed simultaneous measurements of muscle O2 delivery, O2 utilization and muscle activity following priming exercise to better understand the factors limiting V˙O2 kinetics and high-intensity exercise tolerance in youth. Priming exercise resulted in more rapid overall V˙O2 kinetics with the V˙O2 response returning closer to mono-exponentiality because of an increased phase II V˙O2 amplitude and a reduction in the V˙O2 slow component. Mechanistically these changes were related to an improvement in the matching of muscle O2 delivery to V˙O2 as evidenced by a reduction in ⌬HHb/⌬V˙O2 and an association with an Published by NRC Research Press

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elevated TOI before and during the second bout of exercise. While muscle activity, as measured using iEMG, was reduced following priming exercise, this did not correlate with the altered V˙O2 kinetics. Finally, despite the enhanced aerobic energy provision following the priming intervention, exercise tolerance was reduced by 24% on average, possibly because of an insufficient recovery period between exercise bouts that did not permit adequate recovery of the muscle metabolic status towards baseline.

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Acknowledgements We thank the participants for their time and commitment to this project. We also acknowledge the laboratory support provided by Mr. David Childs and Mr. Owen Tomlinson.

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