In this article, I’m going to discuss a very interesting tactic that has emerged from the literature on how to increase aerobic adaptations to endurance training from performing targeted training sessions in a glycogen-depleted state, and with no carbs consumed prior to training. This paradigm has become known as “train low, compete high.”
Sound contrary to everything you were ever told about nutrition for endurance sports? Thought so. Let’s get into it. As always, allow me to indulge the inner geek – if you couldn’t care less about the mechanisms, skip the next section.
The primary endurance training adaptation is mitochondrial biogenesis (Jornayvaz & Schulman, 2010). This process, in which genetic expression in existing mitochondria (the “energy factories” of muscle cells) is upregulated, increases the number and content of mitochondria – in essence increasing the capacity of muscle cells to produce energy (Margolis & Pasiakos, 2013). Together with increased development of new capillaries, these adaptations increase the capacity to transport and utilise oxygen in working muscles (Knuiman, Hopman & Mensink, 2015).
The process of mitochondrial biogenesis is induced by a protein called peroxisome proliferator-activated receptor)-γ coactivator-1α, or PGC-1a (Jomayvaz & Schulman, 2010). PGC-1a is activated by signaling from two proteins, AMPK and p38MAPK (Margolis & Pasiasos, 2013). Both AMPK and p38MAPK are particularly sensitive to energy status (Jornayvaz & Schulman, 2010). Restricting dietary carb intake and being glycogen-depleted will both upregulate AMPK and p38MAPK signaling (Wojtaszewski et al., 2002). Mitochondrial biogenesis is also regulated by the protein p53, which is particularly sensitive to reductions in carbohydrate, and AMPK upregulation increases p53 signaling for mitochondrial biogenesis (Bartlett et al., 2013).
Ok, I get that the terms for those proteins reads like a list of submachine guns, so what does it mean for you practically? It means that increasing the number and content of your mitochondria makes you more efficient at producing energy, and that the mechanisms that control this are activated in response to low carbohydrate stores in muscle and restriction of dietary carb intake.
Carbohydrate intake is vital to endurance athletes in order to be successful in competition. But the traditional advice to maintain a constant, linear high carbohydrate intake before, during and after training has been questioned due to the ability of performing targeted training bouts in a low-carb state to increase subsequent performance (Impey et al., 2016).
A typical protocol that has been utilised in research to demonstrate this effect is to have subjects deplete muscle glycogen during 1-hour of low-moderate intensity cycling in the morning, then perform a high-intensity session in a glycogen-depleted state that afternoon (Hansen et al., 2005). In this type of protocol, subjects increased the activity of mitochondrial enzymes, and their performance in a time-to-exhaustion trial improved (Hansen et al., 2005).
Interestingly, however, the performance benefit has not always been observed. In a study using the same protocol outlined above, although cyclists increased mitochondrial enzymes and fat oxidation, no performance increases were observed (Yeo et al., 2008). A recent paper offered an explanation for why several studies observed increases in biomarkers of aerobic adaptation, but failed to observe a performance benefit: these studies used low-intensity training to deplete glycogen, then had subjects perform high intensity training while glycogen-depleted (Marquet et al., 2016). High intensity training relies on muscle glycogen, so having subjects performing HIT while glycogen depleted impaired their ability to train with intensity, and as a result the subjects were unable to increase performance (Ibid.). In this particular study, the reverse protocol was used: performing HIT first, while in a carbohydrate-fed state, followed by LIT the next morning, led to significant increases in performance and reductions in 10km time trial (Ibid.).
So it would appear that the increased aerobic adaptations do translate to improved performance, but it is clear that the structure of training sessions and manner in which carbohydrate intake is manipulated are key features of this paradigm.
There is an important qualification here: “train low” does not mean “train zero” (Bartlett, Hawley & Morton, 2014). We know that fatigue impairing performance happens before muscle glycogen is completely emptied (Schulman & Rothman, 2001). But to stimulate these increases in aerobic adaptations, you do need to lower your glycogen stores.
You can achieve this by withholding dietary carbs after a glycogen-depleting training session, or by fasting overnight. Depleting glycogen in the afternoon before a training session the following morning would be one strategy to increase aerobic adaptations (Pilegaard at al., 2002). Even restricting carbohydrate intake in the post-training period has been shown to increase adaptive responses, when measured 3-hours after training (Bartlett et al., 2013).
It is arguable that the adaptive response primarily occurs in the post-training recovery period. This means you want to maintain a low-carb intake after training, which may be the critical factor in driving the adaptive response (Pilegaard et al., 2002). For example, significant increases in biomarkers of aerobic adaptation have been seen where subjects consumed less than 50g of carbs after glycogen-depletion, then fasted overnight, avoided carb intake during HIT the following morning, and for 3-hours after the morning training (Bartlett et al., 2013).
There is another vital point to make at this juncture: you don’t need to be following a low-carb diet overall. You just need to get timing right, make sure you’re glycogen-depleted and don’t spoil it by sipping on a Powerade before your targeted session. Let’s compare two studies each using the same carb intake of 5g per kg bodyweight a day. In one, subjects simply fasted for 2 hours before training and then 2 hours after, but no increases in aerobic adaptations was observed (Cox et al., 2010). Was it the carb intake? No, it was more likely the fact that they weren’t glycogen-depleted.
Another study using the exact same daily carb intake simply manipulated timing. In this study, all carbs were consumed during the day, allowing HIT to be performed in the evening with maximal intensity; carbs were then restricted during and after the HIT session, with subjects going to sleep after consuming a liquid protein-only shake and performing LIT in the fasted state the following morning (Marquet et al., 2016). This protocol, which has become known as “sleep low”, resulted in significant performance increases (Ibid.).
This effect can still be achieved doing twice-daily sessions (as many of you triathletes do): after a breakfast containing 540g carbs eaten 2-hours before a glycogen-depletion training session, withholding glucose intake after the session before performing a second daily session while glycogen-depleted led to increased aerobic adaptations (Cox et al., 2010).
So it’s not the intake per se, it’s how that intake is manipulated to deplete glycogen and restrict exogenous carbs in the post-training period, in order to perform a lower intensity session while in a low-glycogen state. The restriction of carbs during is an important variable. For example, in subjects already glycogen-depleted, glucose intake during subsequent training negated any aerobic adaptations, which suggests that glucose availability is a factor regulating these adaptations, not low glycogen levels alone (Morton et al., 2009).
Glycogen-depletion paired with restricting exogenous carb intake is the key boosting your aerobic capacity through this strategy.
An important consideration is that training in a low glycogen state can result in muscle protein breakdown, so supplementation with protein after aerobic training is as important as it is after resistance training to stimulate muscle protein and synthesis and return to positive protein balance (Howarth et al., 2010). Interestingly, increasing amino acids may supplement aerobic adaptations by stimulating mitochondrial biogenesis, but more work needs to be done in this area (Margolis & Pasiakos, 2013). You also don’t need to worry about any potential negative effect of restricting carbs post-training on muscle protein synthesis, as additional carbs do not have any further stimulating effect on MPS once sufficient amino acids are ingested (Koopman et al., 2007).
Ok, what have we learnt so far. We know that to increase performance, we should perform higher intensity sessions in a glycogen-replete, carbohydrate-fed state (Marquet et al., 2015). We also know that to increase aerobic adaptations, we want to withhold carb intake in the post-training period, and perform a lower intensity training session while glycogen-depleted and without exogenous glucose availability (Bartlett et al., 2013; Morton et al., 2009; Marquet et al., 2016). Currently, there are three different methods which the evidence supports for manipulating carb intake and glycogen storage to achieve this:
For example, you could schedule a high intensity training session for the evening, then restrict carb intake afterward and “sleep low”, performing a low intensity session the following morning while fasted (Bartlett et al., 2013; Marquet et al., 2016). In this set-up, you want to maximize muscle protein synthesis by consuming a protein supplement with 10g essential amino acids, of which 1.8-2g is leucine, after training (Reidy & Rasmussen, 2016). A high protein, casein-based snack before bed like Greek yogurt or cottage cheese would be a good addition to maintain MPS throughout the night (Res et al., 2012).
You would then schedule a lower intensity session for the following morning, after your glycogen-depleting workout the night before and an overnight fast. But remember to resist the Powerade ad and avoid consuming any carbs prior to or during this session, which would mitigate the adaptive response (Morton et al., 2009).
For twice-per day training, the same set-up broadly applies: HIT first for glycogen depletion, followed by LIT later in the day. In this set up, you can have a high carb breakfast to fuel your HIT, but then want to restrict carbs post-training leading up to your LIT session later that day (Cochran et al., 2015).
Important points to remember:
Bartlett, J., Louhelainen, J., Iqbal, Z., Cochran, A., Gibala, M., Gregson, W., Close, G., Drust, B. and Morton, J. (2013). Reduced carbohydrate availability enhances exercise-induced p53 signaling in human skeletal muscle: implications for mitochondrial biogenesis. AJP: Regulatory, Integrative and Comparative Physiology, 304(6), pp.R450-R458.
Cochran, A., Myslik, F., MacInnis, M., Percival, M., Bishop, D., Tarnopolsky, M. and Gibala, M. (2015). Manipulating Carbohydrate Availability Between Twice-Daily Sessions of High-Intensity Interval Training Over 2 Weeks Improves Time-Trial Performance. IJSNEM, 25(5), pp.463-470.
Cox, G., Clark, S., Cox, A., Halson, S., Hargreaves, M., Hawley, J., Jeacocke, N., Snow, R., Yeo, W. and Burke, L. (2010). Daily training with high carbohydrate availability increases exogenous carbohydrate oxidation during endurance cycling. Journal of Applied Physiology, 109(1), pp.126-134.
Hansen, A., Fischer, C., Plomgaard, P., Andersen, J., Saltin, B. and Pedersen, B. (2005). Skeletal muscle adaptation: training twice every second day versus training once daily. Scand J Med Sci Sports, 15(1), pp.65-66.
Howarth, K., Moreau, N., Phillips, S. and Gibala, M. (2009). Coingestion of protein with carbohydrate during recovery from endurance exercise stimulates skeletal muscle protein synthesis in humans. Journal of Applied Physiology, 106(4), pp.1394-1402.
Howarth, K., Phillips, S., MacDonald, M., Richards, D., Moreau, N. and Gibala, M. (2010). Effect of glycogen availability on human skeletal muscle protein turnover during exercise and recovery. Journal of Applied Physiology, 109(2), pp.431-438.
Impey, S., Hammond, K., Shepherd, S., Sharples, A., Stewart, C., Limb, M., Smith, K., Philp, A., Jeromson, S., Hamilton, D., Cloce athletes. PHY2, 4(10), p.e12803.
Jornayvaz, F. and Shulman, G. (2010). Regulation of mitochondrial biogenesis. Essays In Biochemistry, 47, pp.69-84.
Knuiman, P., Hopman, M. and Mensink, M. (2015). Glycogen availability and skeletal muscle adaptations with endurance and resistance exercise. Nutrition & Metabolism, 12(1).
Koopman, R., Beelen, M., Stellingwerff, T., Pennings, B., Saris, W., Kies, A., Kuipers, H. and van Loon, L. (2007). Coingestion of carbohydrate with protein does not further augment postexercise muscle protein synthesis. AJP: Endocrinology and Metabolism, 293(3), pp.E833-E842.
Margolis, L. and Pasiakos, S. (2013). Optimizing Intramuscular Adaptations to Aerobic Exercise: Effects of Carbohydrate Restriction and Protein Supplementation on Mitochondrial Biogenesis. Advances in Nutrition: An International Review Journal, 4(6), pp.657-664.
Marquet, L., Brisswalter, J., Louis, J., Tiollier, E., Burke, L., Hawley, J. and Hausswirth, C. (2016). Enhanced Endurance Performance by Periodization of Carbohydrate Intake. Medicine & Science in Sports & Exercise, 48(4), pp.663-672.
Morton, J., Croft, L., Bartlett, J., MacLaren, D., Reilly, T., Evans, L., McArdle, A. and Drust, B. (2009). Reduced carbohydrate availability does not modulate training-induced heat shock protein adaptations but does upregulate oxidative enzyme activity in human skeletal muscle. Journal of Applied Physiology, 106(5), pp.1513-1521.
Pilegaard, H., Keller, C., Steensberg, A., Wulff Helge, J., Klarlund Pedersen, B., Saltin, B. and Neufer, P. (2002). Influence of pre-exercise muscle glycogen content on exercise-induced transcriptional regulation of metabolic genes. The Journal of Physiology, 541(1), pp.261-271.
Reidy, P. and Rasmussen, B. (2016). Role of Ingested Amino Acids and Protein in the Promotion of Resistance Exercise-Induced Muscle Protein Anabolism. Journal of Nutrition, 146(2), pp.155-183.
Res, P., Groen, B., Pennings, B., Beelen, M., Wallis, G., Gijsen, A., Senden, J. and Van Loon, L. (2012). Protein Ingestion before Sleep Improves Postexercise Overnight Recovery. Medicine & Science in Sports & Exercise, 44(8), pp.1560-1569.
Shulman, R. and Rothman, D. (2001). The “glycogen shunt” in exercising muscle: A role for glycogen in muscle energetics and fatigue. Proceedings of the National Academy of Sciences, 98(2), pp.457-461.
Wojtaszewski, J., MacDonald, C., Nielsen, J., Hellsten, Y., Hardie, D., Kemp, B., Kiens, B. and Richter, E. (2002). Regulation of 5â€²AMP-activated protein kinase activity and substrate utilization in exercising human skeletal muscle. American Journal of Physiology – Endocrinology And Metabolism, 284(4), pp.E813-E822.