Comfortable at just below your critical speed: how is blood flow distribution coupled to muscle fibre recruitment during exercise?

It is a common experience for every one of us that exercising at a fast yet comfortable pace, running, cycling or basically whatever exercise discipline, can be continued for a considerable duration without overt fatigue. However, if you just slightly increase the pace, the perceived effort is substantially enhanced and the tolerable duration of exercise is usually dramatically reduced. It is this exercise physiology phenomenon that has created the critical speed (CS), or power, concept (Jones et al. 2010), which together with gas exchange threshold, maximal oxygen consumption, and exercise efficiency dictates exercise performance or intolerance in health and disease. While both aerobic and anaerobic energy production pathways are important determinants of CS, another important determinant is the amount of blood flow supplying the working muscles with oxygen. This includes not only bulk blood flow per se, but in particular the distribution of blood flow that delivers oxygen to those muscle fibres that are actively engaged in exercise. This very topic was addressed by Copp et al. in a recent issue of The Journal of Physiology that in many ways advances our knowledge about the integrative physiology of what happens when exercise intensity is increased from comfortable to abruptly fatiguing intensity (Copp et al. 2010). Although blood flow to the limbs can be measured in humans, even during strenuous and complex exercise involving all upper and lower body musculature such as in cross-country skiing (Calbet et al. 2004), it tells us little about how blood flow is actually distributed to different muscles, or other tissues of the working limbs and trunk. In animals, microspheres can be utilized to study inter- and intramuscular blood flow distribution, as was first studied by Laughlin and Armstrong during the 1980s when they laid the basis for our understanding of the blood flow heterogeneities between different muscles, especially between slow-type red and fast-type white muscles in varying exercise intensities (Laughlin & Armstrong, 1985). Microspheres were also used in the technique that Copp et al. applied in running rats. In their study microspheres were injected into the aortic arch of the exercising animal to measure hindlimb blood flow. After having determined maximal oxygen consumption and the CS for each rat, rats performed running at two speeds, just below and just above the CS, during which total hindlimb blood flow as well as blood flow to each of the 28 muscle groups of the hindlimb was measured. The results indicate that during constant-speed exercise below CS, exercise of sustained duration (>45 min) could easily be continued. In contrast, during exercise at speeds just above CS, exhaustion ensues rapidly (within 5–10 min). Not surprisingly the authors also found that blood flow to the total hindlimb was significantly elevated during exercise above (∼220 ml min−1 (100 g)−1) versus below CS (∼160 ml min−1 (100 g)−1)), but even more importantly, blood flow was increased above CS in 15 of the 28 individual muscles or muscle parts compared to below CS. Specifically, their blood flow measurements indisputably demonstrated that muscles and muscle portions of all fibre types are indeed increasingly recruited above CS, but the regions that are most heavily recruited from below CS to above CS exercise intensity are composed of a majority of type IIb/d/x fibres, i.e. very fast and powerful white fibres. Thus, running above CS, relative to below CS, requires disproportionate blood flow increases predominantly in highly glycolytic muscle fibres, which are known to have higher recruitment thresholds compared to highly aerobic slow fibres. From the measurements of Copp et al. it can also be readily appreciated that a wide range of blood flows exists in different muscles of the hindlimb during whole body exercise, ranging from 73 ml min−1 (100 g)−1 to almost 600 ml min−1 (100 g)−1, the highest value being also much higher than the typical 70–80 ml min−1 (100 g)−1 average muscle blood flow value in fit but untrained healthy young men during maximal whole body exercise, such as cycling. It is well known from human studies that at or especially slightly above CS, oxygen consumption soon reaches its maximal value which is associated with exhaustion, even if the speed is less than true maximal speed measured in the ramp test. This rise in during constant-speed exercise has been named as the slow component, which may, among other factors, stem from (1) progressive recruitment of additional fibres as those that were initially recruited fatigue, and/or (2) progressively developing inefficiency of already contracting fibres. While it had been known for some time that the fatigue-resistant slow-type red fibres are recruited first during exercise, Copp et al. now convincingly showed that fast fibres are recruited to a disproportionally greater extent from just below CS exercise to just above CS exercise. Hence, it is likely that the rise in to its highest value can be explained largely by additional recruitment of these fast fibres. Fast muscle fibres are less efficient and consume more oxygen as compared to slow-type fibres. Therefore, this, in addition to progressive metabolic inefficiency of already contracting fibres (from the onset of exercise), probably made these untrained rats reach their of almost 90 ml min−1 kg−1, the value that only a few highly trained and (in the sense of endurance performance) genetically superior people have ever accomplished. When exercising below CS does not reach ; however, fatigue with overt exhaustion still ultimately develops. This may be due to the fact that running speeds below CS do not create a stimulus that recruits the fast fibres needed for high running speeds, so that the fatigue-resistant slow-type red fibres recruited early in exercise ultimately develop fatigue. In addition, a wide variety of other centrally and peripherally mediated mechanisms are also probably involved (Allen et al. 2008). As mentioned previously, apart from the bulk blood flow level, blood flow distribution and its heterogeneity within and among muscles plays an important role in matching nutrient and oxygen delivery to the local needs of the tissues. Blood flow heterogeneity has been associated with efficacy of oxygen and nutrient delivery and, ultimately, tissue oxygenation and is therefore a functionally essential parameter (Duling & Damon, 1987). Due to the methodological constraints, studying muscle blood flow distribution and heterogeneity in humans is challenging, but it is possible, however, with small muscle mass exercise such as one leg knee extension exercise. We, by using positron emission tomography (Heinonen et al. 2007, 2010), and others, by applying magnetic resonance imaging (Richardson et al. 2001), have studied the phenomenon. In excellent agreement with the results of Copp et al. these human data also suggest that when exercise intensity is increased, blood flow is directed to newly recruited muscle fibres rather than to fibres already engaged in exercise (Heinonen et al. 2007). Moreover, blood flow heterogeneity in the whole knee-extensor muscle group decreases with increasing workload, which can be explained by the decreased variability in mean blood flow values of the individual muscles of knee extensors with the increasing exercise intensity. However, out of the four individual heads of the knee extensors, intra-muscle blood flow heterogeneity decreased only in m. vastus lateralis, which was also proportionally activated the most. Thus, there are apparent intensity-dependent, muscle-specific characteristics of blood flow in humans that still warrant further investigations, but current evidence also shows that the often observed exercise-induced changes in capillary blood flow heterogeneity probably reflect true changes in nutritive flow linked to muscle fibre and vascular unit recruitment (Heinonen et al. 2010). One important aspect that still needs to be discussed to this end is that especially during low intensity exercise with small muscle mass, muscle is likely to be fairly luxuriously perfused (Fuglevand & Segal, 1997; Heinonen et al. 2010). This idea stems largely from the anatomical fact that microvascular units are not precisely matched to muscle motor units (Fuglevand & Segal, 1997) and vascular units are perfused rather abundantly compared to heterogeneously recruited muscle fibres during submaximal exercise. Low intensity knee extension exercise or forearm contractions are, however, the small muscle mass exercise models on which our thinking of muscle blood flow regulation in humans is almost solely based. Consequently, it is essential to extend our current studies to include limb muscle blood flow responses during natural whole body exercise (Calbet et al. 2004). However, while the methodological limitations may hamper studies into muscle-specific blood flow distribution in humans, the study by Copp et al. is an important integrative step forward to elucidate how muscle blood flow and fibre recruitment are activated in high intensity exercise, specifically in the peri-CS range during whole body exercise.