Podcast, Science and Physiology

Neuromuscular fatigue – mechanisms and applications with Callum Brownstein, PhD | EP#355

 September 12, 2022

By  Bernardo Gonçalves

LISTEN TO THE EPISODE HERE:

Callum Brownstein - That Triathlon Show

Callum Brownstein, PhD, is a lecturer in exercise physiology at Newcastle University. Callum has conducted extensive research in fatigability, and the mechanisms of neuromuscular fatigue in (among others) endurance exercise. In this interview, we dive deep into the mechanisms and applications of neuromuscular fatigue in an endurance sports context. 

In this episode you'll learn about:

  • What is fatigue?
  • Differentiating between impairments in contractile function ("peripheral fatigue") and voluntary activation ("central fatigue")
  • How can fatigue and its underlying mechanisms be measured?
  • Different fatigue mechanisms in cycling vs. running
  • Differences in magnitude of fatigue and fatigue mechanisms between the different intensity domains
  • The impact of exercise duration on fatigue
  • Practical applications for triathletes and endurance athletes

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Shownotes

Callum's background

02:46 -

  • Technically, I am still a post-doctoral researcher at Jean Monnet University in Etienne, France. 
  • I have now left France because I will now take a job as an exercise physiology lecturer at Newcastle University.
  • I did my PhD at Northumbria University.
  • My research interest is in acute exercise responses, focusing on neuromuscular fatigue. (the transient impairments in muscle function we experience)
  • I am interested in this topic from an integral perspective: neuromuscular fatigue manifests everything occurring within and upstream of the muscle. So, it can depend on factors inside the muscle, the cardiovascular capacity to bring oxygen to the muscle, which could depend on environmental conditions, characteristics of the exercise we perform and the population in question.

Carbohydrate recommendations

Pre-Race

05:11 -

  • Typically, amateur athletes start their races early. So, we need to consider what to recommend to them.
  • For example, Vuelta is taking place. Races start at 13h, which is much later than for some amateur races.
  • On the day, the aim is to fill up both glycogen stores: liver and muscle.
  • It is essential to distinguish between liver and muscle stores because we will not use muscle glycogen stores at night.
  • However, the brain and vital organs are working, so we can reduce liver glycogen stores overnight.
  • The morning nutrition is to replenish liver glycogen stores.
  • We have done a study in which we gave the same breakfast concerning quantities but different types of carbohydrates. (glucose or glucose and fructose)
  • This difference is because fructose first needs to go to the liver.
  • As it goes first to the liver, it takes care of those liver glycogen stores. We found out that time to exhaustion was higher for people that ate glucose and fructose.
  • In practical terms, it means something like rice or porridge oats with some sources of fructose (honey, jam, juice or anything like this)
  • The next topic is the type of carbohydrates (complex or simple)
  • If we start early, there is not much time to digest the food properly.
  • We want "easy-to-digest" foods (low fibre, low fat).
  • For example, rice is better than porridge oats.
  • On the other hand, if you start at 13h, gastrointestinal comfort will not be a problem; porridge oats can also be a good choice.
  • Porridge has more fibre and fat, so the release of carbohydrates will be slower, but you will not be as hungry in the morning as you would with rice.
  • The addition of protein and fat will depend on the race. If it is a one-day race, carbs are the only thing that matters in the morning.
  • We want protein for multiple-day stage races because we need to think about recovery and are not fresh in the morning.

Neuromuscular fatigue

04:53 -

  • If you asked ten researchers to define fatigue, you might get different answers. We research fatigue in different contexts.
  • In sports, fatigue is the inability to maintain a specific speed/power output. 
  • Neuromuscular fatigue occurs before task failure occurs. If you perform moderate/severe intense exercise, your maximum muscle capacity reduces quickly, but it does not mean you cannot sustain the task.
  • Fatigue got the definition as a reduction in maximal performance.
  • I am interested in muscle function and the neuromuscular mechanisms contributing to fatigue.
  • Recently, there was an effort to define "fatigue" universally. 
  • Therefore, fatigue is a sensation of tiredness, weakness or lethargy, and exercise is a potent stimulus for that. The muscle function impairments we see can be a significant factor in that sensation of fatigue.

Fatigue while exercising in the heavy domain

07:10 -

  • At the beginning of exercise, you might see increases in the perception of fatigue that stabilises quite early.
  • Often, you see an increase in fatigue compared to baseline and an impairment of the capacity of the muscle to produce force, but they are tightly linked. (it will depend on the intensity and type of exercise)

Different types of fatigue related to endurance exercise

08:15 -

  • I would say there is only one fatigue: sensation, which depends on many factors.
  • All apparent fatigue types (Muscle fatigue, neuromuscular fatigue, central fatigue, peripheral fatigue) refer to transient impairments in function at different steps of the neuromuscular pathway.
  • Neuromuscular fatigue refers to a reduction of the maximum force generated by the muscle measured during isometric contractions.
  • Muscle force reduces because of two causes. The first is that the activation signal from the nervous system to the muscle can reduce its strength. (the voluntary activation of the muscle reduces - "Central fatigue")
  • The second is on the muscle capacity to respond to a neural impulse lowering.
  • It means that when the signal arrives at the muscle, it can not respond with the same magnitude. (peripheral fatigue)
  • These factors can contribute to fatigue, but other perceptional values contribute to the perception of fatigue. Their importance will depend on the characteristics of exercise or environmental conditions.
  • If you exercise in high temperatures, you perceive heat stress. So, if I ask you to rate your fatigue, the perception of heat stress will be part of your sensation of fatigue.
  • Another factor is breathlessness because if I ask you to rate your fatigue during severe intense exercise, breathlessness will be part of that equation,
  • Thus, you have neuromuscular and perception elements that contribute to fatigue.

Research methods to evaluate fatigue

12:19 -

  • If we are talking about neuromuscular changes during exercise, we measure this in isometric contractions. For example, we use the leg extension to measure quad contraction (the most recruited muscle in endurance exercise).
  • We will have participants pushing against an immovable object (no movement around the joint). We measure the force produced during that effort.
  • They will do isometric contraction before and after exercise on a knee extension dynamometer.
  • And this can allow us to measure fatigability.
  • We can also use neuromuscular stimulation to access the two components that affect fatigue (voluntary muscle activation and muscle contraction magnitude)
  • Participants perform a maximum muscle voluntary contraction of the knee extension to measure voluntary muscle activation.
  • When they are at their peak force of muscle contraction, we deliver a supramaximal electrical stimulation of the femur nerve (the nerve that sends the signals to the quadriceps).
  •  When doing that voluntary contraction, if the activation of the muscle is incomplete (motor units not recruited or not discharging at the muscle capacity), we will "artificially" activate those muscles, which leads to an increase in the force produced.
  • So, we have a volunteer muscle contraction, and an imposed twist on top of the force produced voluntarily.
  • The lower the volunteer muscle contraction, the higher the twist size. 
  • Immediate after the contraction, the participants relax, and 2-3 seconds later, we will deliver the same supramaximal stimulus at rest.
  • What we obtain is the potentiated twist (resting response). If there are impairments within the muscle, the amplitude of that twist will be lower. The signal only travels from the nerve to the muscle, so reductions in amplitude will be from some factor in the muscle.
  • These methods can measure maximum force generating capacity, voluntary muscle activation and contractile function.

Getting an additional force/contraction even in a fresh state

16:34 -

  •  Even in a fresh state, we never see a 100 % maximum voluntary activation, meaning most participants will not recruit the muscle entirely.
  • The maximum voluntary activation will typically reach 80-90 % of the muscle capacity.

Different fatigue mechanisms in cycling and running

17:43 -

  • In the last 20 years, research has looked at fatigue mechanisms associated with endurance-type exercise.
  • However, there has been no comparison between running and cycling.
  • When comparing studies, running seems to have more impact on the nervous system than cycling.
  • Cycling appears to affect the muscle more than running.
  • So, we designed a study to test that. We took seven well-trained endurance athletes familiar with running and cycling.
  • They performed efforts with the same intensity and duration while running and cycling on separate days. (three hours of running and three hours of cycling slightly above the first lactate threshold - 105 %)
  • We measured muscle function before, halfway, and after exercise with the methods described.
  • The reduction magnitude of the muscle force-generating capacity in the knee extension was similar between the two conditions. The muscle capacity was lowered by 25 %, but the factors responsible for that reduction differed between the different modalities.
  • During cycling, there was a more significant impairment of the contractile function (the response to the resting twist responses were much lower than for running - five times lower)
  • The quads were still contracting well in the running, but the muscle capacity was still lower. This happens because muscle activation capacity is lower. (more impairment in nervous system function to activate the muscle)

Reasons for this difference

22:22 -

  • The relative contribution of the quadriceps to force or power production during exercise differs from running to cycling.
  • Cycling is a weighted supported sport, so there is a more significant involvement during cycling than running, which recruits the whole body.
  • In cycling, the recruitment of the quads is higher, so the metabolic demand and stress are higher. The fuel utilisation rate in the quads should be more significant in cycling than running.
  • More stress lead to the development of metabolites that impair the contraction of the quads. 
  • Another issue is the contraction type. During cycling, the quad contractions are concentric during a more significant part of the pedal stroke.
  • Running is the repetition of stretch/shortened cycles, where the muscle elongates under tension, and when we move forward, we have those concentric contractions. (which is more efficient)
  • In cycling, the contraction type is less efficient, which increases metabolic stress.
  • There are some reasons we expected that impairments in the muscle would be higher in cycling than in the running.
  • In the running, fatigue mechanisms are more speculative. 
  • In review papers that recognise that running damage the nervous system, muscle damage was the proposed cause.
  • However, I do not think that is the case. The changes in resting twist responses were minimal. If there were muscle damage, the twist responses would be lower.
  • Three hours of running did not cause so much damage to the quads.
  • Nervous system responses seem to be lower despite minor damage in the quads. Therefore, it is something else that might be responsible for fatigue.
  • We did other measuring techniques to try to assess what affects running fatigue. For example, we stimulated the spinal cord. We put electrodes in the thoracic spine and spinal cord and delivered an electrical stimulation that provides electrons that descend to neurons in the spinal cord. 
  • These neurons are the neurons responsible for transmitting the signal for muscle contraction. We found that the capacity of these neurons to respond to that stimulus was lower following running.
  • Therefore, there seems to be an impairment in the motor neurons' responsiveness, which could be the reason for the lower muscle contractile activation.

Practical applications for triathletes

28:15 -

  • The study we did was mechanical.
  • Running causes little change in the muscle cell. (small perturbation in the quads)
  • From a training perspective, the small perturbation in the quadriceps in response to running has some implications on the crossover of the different modalities.
  • We understand that all triathletes are training for running and cycling anyway. The impairments that occur in contractile function lead to impairments in muscle function and might promote adaptations.
  • Three hours of running perturbs the quadriceps slightly, meaning the adaptive stimulus is low. If you are a triathlete and you do not do much cycling but a lot of running, you will not get the peripheral adaptations crucial to perform in cycling.
  • Therefore, this research shows the importance of training both modalities and ensuring you get the adaptations for those disciplines.

The influence of different intensity domains on fatigability in cycling

30:30 -

  • The boundary between heavy and severe exercise (often measured with critical power) has crucial implications for neuromuscular fatigue.
  • When we exceed the threshold, aerobic metabolism and anaerobic phosphorylation are no longer sufficient to maintain the intensity. We must tap into anaerobic energy resources that produce metabolites, impairing contractile function. Moreover, we are progressively less efficient in severe exercise because the energy cost of the task is not stable, and there is an increased influx of metabolites, so our neuromuscular function is progressively impaired.
  • The implications of exceeding that boundary in neuromuscular terms was a topic still not understood. And this is important for patients whose VO2max and lactate threshold are very low.
  • For more prolonged endurance events (between moderate and heavy domains), this topic of neuromuscular function impairment is essential.
  • We did three constant power output trials performed on separate days. One was at 70 % (140 minutes) of the first threshold, the other at 90 % (110 minutes) and the last at 110 % (90 minutes).
  • We accessed neuromuscular function at various percentages of task completion (0, 25, 50, 70 and 100 % of the task).
  • We compared the changes in neuromuscular function during those three bouts of exercise.
  • If fatigability is disproportionally higher above the first threshold, the difference between 90 and 110 % of the threshold would be higher than the difference between 70 and 90 %.
  • During all three bouts, there was a reduction in maximal force generating capacity, which occurred early in the task (even 25 % of task completion)
  • However, the reductions were higher in the heavy domain. For a percentage of tasks completed, the reduction in muscle force was 2.6 times higher in the heavy domain compared to moderate exercise.
  • These reductions occur primarily due to mechanisms within the muscle.

Practical applications of these results

36:29 -

  • I would say that you should make your easy days easy. Crossing the boundary between moderate and heavy intense exercise, the cost of that intensity is disproportionally higher and neuromuscular function is disproportionally impaired.
  • We did not measure recovery, but a recovery cost is likely following heavy versus moderate intensity exercise. And that cost occurs early in the heavy domain exercise.
  • If you know where those thresholds are and want to do a recovery session with a limited recovery cost, ensure that we stay below that boundary between moderate and heavy intense exercise to reduce the impairments in neuromuscular function.

Impact of the severe and extreme domains in fatigue

39:12 -

  • The MLSS is the boundary between heavy and severe exercise. 
  • Below that threshold (measured as critical power), oxidative phosphorylation is sufficient to meet the energy demands of the task. (aerobic metabolism is producing sufficient ATP for the power output)
  • When we cross that boundary, that is no longer the case, so phosphorylation is insufficient to meet the ATP demands, and we have to use anaerobic energy resources. Phosphocreatine continues to decrease, and there is an increase in inorganic phosphate, which hurts contractile function. (He impairs the muscle from responding to the stimulus promoted by the nervous system)
  • As the energy demand of the task is not stable for the same power output, the flux for the metabolite pathways keeps increasing. So there is a VO2 component (oxidative phosphorylation needs to keep increasing), and there is a slow component in terms of the metabolite concentrations in the muscle.
  • These metabolites impair contractile muscle function during intense severy exercise, and the impairment is disproportional compared to heavy intense exercise.
  • I do not know if there are differences in the neuromuscular mechanisms between severe and extreme domains. It is probably the exact mechanism occurring at a faster rate.
  • You can see a reduction in muscle contraction activation in severe intensity exercise.
  • We separate the concepts of central and peripheral fatigue, but they are not mutually exclusive.
  • During severe intensity exercise, there is that build of metabolites in the muscle, and there are sensors within the muscle that are sensitive to those changes.
  • These three components are sensitive to metabolic perturbations, and metabolites within the muscle activate these sensors that send signals to the nervous system.
  • Within the nervous system, they can have inhibitory effects on the nervous system. So, the chances in the muscle affect the nervous system.
  • The impairment in the nervous system in voluntary activation increases with exercise duration.

Intensity and fatigue impairments

43:58 -

  • If you perform intense heavy exercises to task failure, you will produce as much power as possible when you reach task failure.
  • The contributor to that would be the reduction in voluntary contractile activation of the nervous system, but impairment in muscle contractile function will still affect fatigue. (glycogen depletion)
  • Nevertheless, overall, the nervous system becomes more critical at lower intensities.
  • The longer you perform the exercise, the higher the impact on the nervous system. So, fatigue becomes more "central" in origin.

Recovery time course in neuromuscular function

45:33 -

  • It will depend on the exercise modality. After running, it takes much longer to recover neuromuscular function than in cycling.
  • It could relate to muscle damage, although we did not observe any damage in the quadriceps.
  • However, the study we did was on a treadmill. Muscle damage could be more significant in variable terrain because eccentric muscle contractions can induce muscle damage and impact recovery.
  • Moreover, recovery will depend on the intensity of the exercise.
  • My PhD looked at the recovery of nervous system function. We evaluated recovery after intermittent sprint exercise. (football match)
  • There is a high degree of damage in sports like football. We found an impaired nervous system for an extended period following football match play. After 24h, the capacity of the nervous system to activate the muscle was still at a low level.
  • It can have relationships with muscle damage. The more damage you have in the muscle, the more significant the impairment.
  • Concerning contractile function, it will depend on the intensity of exercise.
  • If we perform a high-intensity exercise with a build-up of metabolites but stop soon, the contractile function will recover fast.
  • So there is a fast and a slow component of the recovery.
  • The reductions due to glycogen depletion will depend on the nutrition taken for exercise. If there are appropriate nutrition strategies, we can increase muscle glycogen above the levels that impair contractile function and will recover within a few hours. (even if muscle glycogen is not topped up)

Other factors that impact fatigue and neuromuscular function

50:01 -

  • Hypoxic conditions reduce voluntary activation (impairments in exercise at high altitudes)
  • It reduces activation of the muscle, so it preserves contractile function. (less impaired at high altitudes)
  • Concerning nutrition, I have not seen evidence of impacts on neuromuscular function.
  • Some studies depleted muscle glycogen, gave participants carbs or a placebo, and then measured the contractile muscle function. And there was no difference between groups.

Future research in fatigue mechanisms

52:56 -

  • From an integrative perspective, my goal is to have a more holistic understanding of what is limiting the neuromuscular system systemically. (in both clinical and athletic populations)
  • It is an area with much room for development. (system interaction)
  • The impairments we see in the neuromuscular system during exercise manifest everything occurring upstream of the muscle. So, the causes could be factors within the muscle (e.g. oxidative muscle capacity and metabolic perturbations). In turn, these factors depend on the cardiovascular system's ability to transport oxygen to the muscle for aerobic metabolism.
  • The oxygen transportation depends on pulmonary function (the ability to get oxygen from the lunch to the bloodstream and the capacity of the cardiovascular system to pump blood)
  • Therefore, I am interested in how all of these systems will affect neuromuscular fatigue in various types of exercises.
  • "Durability" is a concept in endurance performance where neuromuscular fatigue could be a factor, so it would be interesting to understand how neuromuscular fatigue can influence "durability".

Rapid-fire questions

57:28 -

What is your favourite book, blog or resource?

Muscle and Exercise Physiology by Jerzy Zoladz

What is an important habit that benefited athletically, professionally or personally?

Perseverance.

Who is someone you have looked up to or who has inspired you?

I would say my two former supervisors: Guillaume Millet and Doctor Kevin Thomas.

LINKS AND RESOURCES:


Bernardo Gonçalves

Bernardo is a Portuguese elite cyclist and PhD student in the field of aerodynamics at the University of Coimbra. He writes the shownotes for That Triathlon Show, and also produces social media content for each new episode.

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