Muscle stiffness and running efficiency

As I discovered in my impromptu duel with Emily in the Turkey Trot half marathon three weeks ago, one of the consequences of the episode of arthritis which I had suffered earlier in the year has been a serious loss of strength in my leg muscles.  The Turkey Trot is run on the hilly roads that connect the villages of the Wolds that straddle the Nottinghamshire-Leicestershire border.  I simply could not match Emily on the hill-climbs, and the repeated pattern in which she surged ahead up the hills and I struggled to close the gap on the descents set us up for an exciting duel in the final mile.  A week later, the hopping test confirmed that I had indeed lost a lot of strength in my leg muscles since the recurrence of the arthritis in February.   So one of the challenges of the next few months is how best to recover that strength.

This challenge raises four of the major unanswered questions regarding training for distance running:

1)      what is the role of resistance training?

2)      what is the role of plyometrics?

3)      what is the role of stretching?

4)      when should these forms of exercise be performed?

While there is no doubt that aerobic capacity is of paramount importance in distance running, the available evidence suggests that leg strength and stiffness play a role.   Many studies show that less flexible runners are more efficient (e.g. J Strength Cond Res 23(1):158-62, 2009; J Orthop Res.8(6):814-23 1990.)

Anecdotal evidence supports this.  Although it is probable that several things, including an increase in aerobic capacity, contributed to Paula Radcliffe’s transformation from a non-medal winner in Sydney in 2000 to the world’s best female marathon runner in 2003, I think that one important contribution was the introduction of hopping and other plyometric exercises which increased her jump height in association with a decrease in her flexibility. In his article on Radcliffe in International Journal of Sports Science & Coaching (Vol 1 • Number 2 • 2006) Anthony Jones reports in the period 1996 to 2003 her vertical jump height increased from 29 cm to 38cm while her ‘sit and reach distance’ decreased from 8cm to 3 cm.

However the anecdotal evidence regarding the world’s all-time greatest distance runner, Haile Gebrselassie, is a less clear.  In an interview prior to his unsuccessful attempt to break his own world record, in Dubai in January 2009 , Haile made it clear that he considers that it is important to take the time to stretch all major muscle groups.  In particular, he advised: “focus on your hamstrings and calf muscles to avoid injury during the race.”   According to Constantine Njeru, Geb includes both jumping on the spot and stretching during the cool-down after a session.   I was a little surprised to see plyometrics included in the cool-down, but I note that Terrence Mahon (former coach of Ryan Hall) also recommends hopping at the end of a training session.

The anecdotal evidence suggests the need for a compromise between stiffness and flexibility, and furthermore raises the issue of how one might sensibly integrate plyometrics, which tend to promote stiffness, with stretching, which reduces stiffness.  Because the question of whether or not plyometrics, stretching, or both, are useful for a distance runner probably depends on a complex interplay between an individual’s genes, their past training experience and the way in which these forms of exercise might be integrated into a training program, it is unlikely that either anecdotal evidence, or scientific studies that compare outcome of a particular form of training with another in a random selection of athletes, will provide a clear answer.   I think the only way to decide what is best is to weigh up the evidence from anecdote and from scientific studies of training procedures, with an estimate of what makes sense in light of muscle physiology.

What makes muscle-tendon units stiff?

Muscle-tendon units perform two types of function: they can either move or stabilise joints. Many studies have provided very clear evidence that in order to run efficiently the muscle tendon units that act at hip, knee and ankle must act as stiff springs to maximise the rapid capture and release of elastic energy after footfall.  However there is much uncertainty about the best way to achieve the flexibility that allows our joints to move with minimal resistance yet have the stiffness necessary to stabilize them

I think it helpful to examine more carefully the nature of the mechanisms that produce stiffness.  There are two main factors that contribute to the stiffness of a muscle-tendon unit.

1)      Isometric contraction of the muscle.  This requires the formation of temporary cross bridges between the actin and myosin molecules in the muscle, and consumes energy.  These cross bridges can be created and released within a fraction of a second.

2)      The formation of fibrous collagen bands which are more permanent.  They are produced over a period of hours or days as a result of inflammation due to tissue damage and do not require energy to maintain them.  The collagen molecules are helical proteins; in other words they are miniature coiled-up springs that can undergo compression or extension.  They can contract in response to small electric currents generated by collateral nerve terminals that branch off from the nerve supplying the muscle to terminate on the surface of the tendon.  However the time scale of this contraction and its subsequent release is much slower than the making and breaking of actin-myosin cross-links within the muscle fibre.

Cleary if we are to have adequate mobility we cannot rely only on permanent collagen fibres to stabilise the joint.  Furthermore, if the stiffness is due to collagen fibres we are more likely to tear the muscle when a sudden force is applied, so we would be at great risk of injury.

However, if we have very few collagen fibres so that our muscles are very floppy when not actively contracting, it is likely to be difficult to build up enough tension quickly enough at footfall to produce the required stiffness, and furthermore, the isometric contraction will consume energy.  If we were as floppy as a new born baby, we would probably be very inefficient at running.

If our goal is to run fast and injury free we need the right balance between stiffness due to isometric contraction and stiffness due to collagen. I believe that the right balance depends on how well we have trained our nervous system to contract the muscles very quickly at precisely the right time in the gait cycle.   If we have trained our nervous system well, we can rely more on muscle contraction and less on collagen, allowing us to run efficiently with low risk of injury.

However the picture is even more complex, because the way in which muscle contraction is controlled is very complex.

Feedback control of muscle contraction

There are two main feedback systems that control the tension of the muscle-tendon unit – the system that senses muscle tension via the intrafusal fibres within the muscle spindles that are attached in parallel with the body of the muscle, and the system based on  Golgi tendon organ that is attached to the tendon near the point where the tendon becomes a sheath that envelopes the muscle.

The intrafusal system

Nerve ending attached to the intrafusal fibres detect tension in the muscle and can initate a rapid reflex contraction mediated via a single synapse with the alpha motor neuron in the spinal cord responsible for driving a contraction of the muscle.  This reflex which occurs in less than  1/10th of a second is responsible for the stretch-shortening cycle that is activated during plyometrics.  A sudden sharp stretch produces a strong concentric contraction of the muscle.    The strength of this contraction can be enhanced by plyometric training.  It is probable that this stretch-shortening cycle contributes to the elastic recoil during stance while running.  The force of footfall produces an eccentric contraction of the major leg muscles, and the associated stretch would be expected to initiate a powerful reflex contraction.

However the intrafusal system is more complex than this.   There are two types of intrafusal fibre: ‘nuclear bag’ fibres that respond to a rapid stretch, and ‘nuclear chain’ fibres which are viscoelastic and respond to more sustained tension.  As far as I am aware, the circuitry is not fully understood, but it is probable that the nerves from these nuclear chain fibres send signals to the cerebellum (at the base of the brain) and the cerebellum computes the required steady state level of activity that is required to maintain posture.   However, if the local milieu around the nuclear chain fibres is too acidic or otherwise unfavourable to the generation of nerve signals, the transmission of the signal regarding current muscle tone is obstructed and the cerebellum sends a signal to increase muscle tone.  Thus, the muscle might develop a potentially damaging hypertonic state in which the muscle remains in a sustained over-contracted state.  In this hyper-contracted state the muscle pulls on the tendon and is likely to trigger the build-up of additional collagen fibres at the junction of muscle and tendon, making the muscle even stiffer.

The Golgi tendon organ

Nerve fibres from the Golgi tendon organ send signals to the spinal cord (and probably to the brain) indicating the amount of tension in the tendon.  In the spinal cord the incoming nerve from the Golgi organ synapses on an interneuron.  In some circumstances, it appears that the interneuron acts on the alpha motor neuron to inhibit muscle contraction – a so-called autogenic inhibitory reflex.   It was once thought that this mechanism was responsible for the potentially protective release of tension in a muscle that is maintained in a stretched state for a sustained period.  More recent evidence suggests that that inhibitory process might, at least in some circumstances be mediated via the intrafusal system.   Furthermore, in other circumstances, the Golgi tendon organ can initiate an autogenic excitatory response that produces an increase in muscle tone.   This mechanism appears to play a part in the lift-off from stance.

The net effect of feedback control of muscle tone

It appears that both the intrafusal system and Golgi tendon organ system are able to initiate either increases or decreases in muscle tone under appropriate circumstances.  However, as far as the athlete is concerned, the three important conclusions regarding the regulation of muscle tension are:

1)      rapid stretch of the muscle promotes a rapid concentric contraction – the stretch shortening cycle.

2)      Sustained stretching tends to produce a release of muscle tension via an autogenic inhibitory response.

3)      When the muscle environment is too acidic or otherwise unfavourable, the signal providing feed back about muscle tone to the cerebellum might be impaired resulting in potentially damaging hypertonic contraction.  This hypertonic state is likely to promote the deposition of additional collagen fibres at the junction of muscle and tendon.

The effect of muscle tension on collagen at the junction of muscle and tendon

When the nerve innervating a muscle sends an excitatory signal, a collateral signal to tendon in the vicinity of the junction of muscle and tendon promote tensioning of the coiled collagen springs.  This is likely to trigger the laying down of more collagen making the muscle stiffer.  However, the tension in the muscle produced by a slow contraction of the muscles sustained over a period of 8-10 seconds appears to be able to reverse this process.   Thus slow contractions appear to be capable of reducing the excessive stiffness due to excessive build up of collagen.   A sudden, very strong muscle contraction, especially a strong eccentric contraction, is likely to tear the collagen fibres and damage the muscle.

How is the stiffness of the muscle-tendon unit regulated during running?

Recordings from the motor nerves that drive the leg muscles reveal that shortly before footfall there is a burst of activity in the muscles controlling hip and knee (quads and hams) that generates an isometric contraction that is maintained through stance.  This contraction would also be expected to stiffen the collagen springs.  Thus, a potentially trainable muscle contraction appears to make a major contribution to creating the rigid strut that is required to capture the kinetic energy of the falling body and store it as elastic energy within the tendon.  When the isometric contraction is released, possibly via a nerve impulse from the Golgi tendon organ, the rebound will propel the body upwards off stance.

If the isometric contraction is not adequate to prevent stretching of the muscles (as is likely when running downhill or when sprinting) the stretch-shortening reflex will be activated thereby generating a powerful concentric contraction that will propel the body upwards.  Unless the muscle is adequaltey conditioned, the eccentric contraction is likely to tear collagen fibres producing DOMS the following day

Practical conclusions regarding training

The first priority is to train the preloading contraction that occurs just before footfall.  This contraction is not under conscious control.  However it appears that it can be trained by drills that focus on producing a short sharp landing and lift-off from stance.  I consider that various hopping drills are best for this.  I am currently doing two-footed bunny hops and two footed hurdle jumps (6 inch hurdles) as I need to be very careful to avoid aggravating my recently inflamed knee joint.  However, once the knee has fully recovered, I will do one-footed hops and also bounding from foot to foot.

However these plyometric-type exercises are likely to produce sustained tension in the collagen springs and perhaps to induce the formation of new collagen.  While this would be expected to increase the stiffness of the muscles and thereby improve the efficiency of capture and storage of  kinetic energy, it will also make my hips and knees more resistant to movement at other phases of the gait cycle.  Furthermore, excessive stiffness due to collagen might increase the risk of injury.  In my opinion it is undesirable to allow too much build up of collagen near the muscle-tendon junction.  Therefore, after a plyometric session I engage the hams and quads in slow controlled contractions (eg squats with each cycle lasting around 10 seconds).   Furthermore, because the plyometric sessions place substantial strain on the muscle-tendon unit, I do not do these session after heavy training, at which time there are likely micro-tears that might be exacerbated by the plyometrics.  Nor do I do them before heavy training as the muscle requires time to recover.   Therefore, I only do plyometrics on a day when I intend to do light training or cross-training on the elliptical machine.

The possibility that any acid in the local environment within the muscle tissue might impede the transmission of signals regarding postural tone  from the intrafusal fibres to the cerebellum  thereby leading to a faulty computation in the cerebellum and excessive drive to the motor neurons, resulting in chronic excessive contraction and the possible build up of excessive collagen makes it essential to perform an adequate cool-down after any training session in order to stimulate blood flow that clears acid and any other toxic substances from the muscle.  After running sessions I simply jog at a pace well below the first ventilatory threshold.  After plyometric sessions, I usually do some low-aerobic elliptical cross-training.

What about stretching?  It is clear that static stretching before running is undesirable because it will result in decreased stiffness and therefore decreased efficiency, in addition to the risk of tearing of collagen fibres.  However after running and after plyometrics, either static stretching or slow contractions (e.g. slow body-weight squats) are desirable as such exercises are likely to minimise the risk of chronic hypertonic contraction and thereby minimise the build up of excessive collagen.

Finally, what is the role of resistance training for runners?   While much of the drive that gets the body airborne comes from the release of stored elastic energy, the process of energy capture is not 100% efficient and some of the energy must be generated by concentric contraction. Therefore powerful type 2A fibres are required for sprinting and also for running uphill during distance events.  Furthermore, if you plan to do plyometrics it is essential to ensure that the muscles are strong enough to withstand the eccentric contraction, so some resistance work is advisable before undertaking higher intensity plyometrics, such as bounding and single leg hopping.

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14 Responses to “Muscle stiffness and running efficiency”

  1. Ewen Says:

    Another interesting subject! How much tendon/muscle stiffness comes from simple workouts like 200 or 400m intervals, and how much might that be improved by plyometrics and hopping? The decreased ‘sit and reach’ distance for Radcliffe is also interesting. I’d read about that. I remember Deek being unable to ‘touch his toes’ but no point was made at the time that this might be and advantage for distance runners.

    • canute1 Says:

      Ewen, thanks for your comment.

      200m or 400m repetitions will help increase stiffness, but are probably not as effective as hopping. If we want to increase the contribution to stiffness from muscle contraction rather than collagen formation, the major goal is training the muscles to produce precisely timed preloading an instant before footfall. It is probably best to do a small number of very precisely timed hops than a larger number of strides during repeated 400’s, during which increasing tiredness is likely to impair the precision of timing.

      On the other hand, hopping does not exactly mimic running so there is some loss of specificity of the movement. It might be that drills such as high knees or butt kicks (with the heel drawn straight up to the buttocks), or Pose ‘change of stance’ or ‘pony’ would also be useful provided they are executed crisply with few repeats to avoid exhaustion.

  2. canute1 Says:

    Ewen,
    Yes I think the hopping exercises that Terrence Mahon advocates are very useful. In the videos he recommends doing these after training, which is fine provided the training was not heavy. I think the benefit might be less after heavy training because timing will be less precise due to tiredness, and also there is a risk of exacerbating micro-tearing of muscles. I usually do hopping on days when I do elliptical cross training. Perhaps ideally one should do easy stride-outs, aiming for light quick steps, after the hopping to encourage incorporation of the precise pre-loading into the running action, but I do not have any direct evidence to support this proposal.

  3. Rick Says:

    Both Steve Cram and Ceb Coe had amazingly long strides.
    The UKA seem to have had an obsession with muscle stiffness over the last year going by their coaching website,
    I know Steve Cram has talked about the importance of stretching and the great Earl Fee is another good example.
    Is static stretching know a dirty work in Athletics and should we do only dynamic stretching ?

  4. Rick Says:

    http://runwitharthurlydiard.blogspot.com/2010/09/steve-cram-had-one-of-longest-strides.html

    • canute1 Says:

      Rick, Thanks for those comments.

      I do think static stretching has its place – mainly to release chronic contraction of muscles that persists even when they are no longer required to contract. This chronic contraction might be released by static stretching after running. I suspect that Triggerpoint Therapy achieves an increase in range of motion by releasing chronic contraction. Maybe Somax therapy has a similar effect though the advertising material for Somax implies that their therapy breaks down microfibres. Unfortunately. I do not find the Somax material to be very convincing.

      I think that for older runners like Earl Fee (and myself), releasing chronic contraction is especially important. However at foot fall we require our legs to act like stiff springs. The main point I was making in my post is that as far as possible, this stiffness should be achieved by a precisely timed contraction that preloads the major muscles acting at hip, knee and ankle immediately before footfall. I believe that hopping can improve the precision of this contraction. However, I think the evidence indicates that it is necessary that collagen fibres provide some stiffness as well. Nonetheless, I consider that stiffness due to persistent muscle contraction is generally inefficient and therefore I think there is value in static stretching after running.

  5. Rick Says:

    Canute check this out;
    Understanding Your Muscles | Men’s Health http://t.co/gIe7x1M

    • canute1 Says:

      Rick, thanks for that link.

      Although rather sensational in style, this article makes some of the points I was trying to make about the roles of collagen and muscle. In particular, it points out that connective tissue (I,e. collagen) is springy. It also emphasizes some important things I didn’t say, such as emphasizing the long range transmission of forces via fascia. Many physios will tell you that injuries arise from poor posture or from poor coordination at a site remote from the injury. The article makes some good points about improving a particular action by releasing tension in a distant part of the body.

      However I disagree with some of the things the article says. For example, I disagree that being as floppy as a baby is ideal for matching impulse with action – it may be good if you want to feed from a bottle held with your toes, but that degree of floppiness is not efficient for running. A baby’s inability to run is due to poor neuromuscular control though lack of stiffness of collagen fibres probably contributes. In an attempt to be sensational, the article seriously undervalues the role of muscles.

      The article emphasizes the value of hopping and skipping – but claims that this has nothing to do with muscle action. Hopping and skipping trains both the muscle and the fascia. The EMG evidence of suggests that training the muscles to produce a precisely time contraction to pre-tension the springs is crucial.

      So overall, it is a thought provoking article but in my opinion, a bit unbalanced

  6. Rick Says:

    Good points, Cheers

  7. freeware keylogger Says:

    I remember Deek being unable to ‘touch his toes’ but no point was made at the time that this might be and advantage for distance runners.I’d read about that.?

  8. Jerry Griffin Says:

    Here are the exercises I am currently doing to enhance my running economy:

    Exercises for enhancing springiness and running economy (Do these drills 2 – 3x per week)

    Spring-jogging [track]
    • Jog normally for about 10 seconds, and then ‘spring-jog’ for about 20m, alternating three consecutive spring- like contacts with your right foot with three contacts with the left (i.e. three hops on your right foot, three hops on your left, three more on your right etc until you have traveled about 20m);
    • Jog normally for 10 seconds again, and then spring-hop for 20m on your right foot only, before shifting over to 20m on the left foot alone. Minimize time on support. You are looking for very powerful, productive hops. Avoid the tendency to look downwards, keeping your gaze ahead, as you would do during normal running.

    Indian-hopping [track]
    • Jog for a few strides, and then take a jogging stride diagonally to the right with your right foot; • When your right foot makes contact with the ground, hop once, then explosively hop diagonally to the left,
    landing on your left foot;
    • When your left foot strikes terra firma, hop once, then explode diagonally to the right;
    • Continue for 45 seconds. Rest for 15 seconds, then repeat. Stay relaxed at all times, moving in a coordinated and rhythmic manner and keeping the hops very springy and quick. Avoid the tendency to look at your feet.

    Hop-sprints [track]
    • Hop 20-30 m as fast as possible on one foot, staying relaxed and minimizing vertical displacement. Push off as hard as you can, but forwards rather than upwards, and minimize duration of ground contact; look for very powerful, productive hops.

    High-knee explosions
    • Stand erect but relaxed, with your feet directly below your shoulders; • Begin by jumping very lightly on the spot, but then suddenly – while maintaining fairly erect posture – jump
    vertically while swinging both knees up toward your chest;
    • Land back on your feet in a relaxed and resilient manner, then explode upwards again, aiming for as little time on the ground as possible while trying to maximize vertical jumping height;
    • Complete 15 high-knee explosions, rest for a few seconds and repeat.

    In-place accelerations.
    • Stand erect but relaxed, with your feet directly below your shoulders;
    • Begin by simply jogging on the spot, but then – when you feel ready – begin to dramatically increase your ‘stride’ rate, building up fairly quickly to as rapid a speed as you can sustain on the spot. Keep your feet close to the ground: you’re not going for high knee lift but rather for dramatically minimized foot-contact times – and an ability to get your feet to spring off the ground as soon as they make contact. Maintain erect but relaxed posture at all times. Perform 3 sets of 20 seconds.

    Hamstrings
    • Standing, one [support] foot 12″ in front, full weight on BOF, other foot loose, toes touching ground. Quickly and intensely, un-weight support foot and pull up by contracting hamstrings. Your hips should remain as level and motionless as possible throughout the exercise, with very little vertical displacement. Alternate legs. 12-15 reps.

    One-leg hops on-the-spot
    • Stand with your left foot forward and your right foot back, with your feet about one shin-length apart from front to back and hip-width apart from side to side. Place the toes of your right foot on a block or step 6-8 inches off the ground and direct most of your weight through the mid-point of your left foot;.
    • Hop rapidly on the left foot (180 cadence) for 40 seconds. Left knee rises 4 – 6 “, right leg and foot remain stationary. Hips are held level and motionless, with very little vertical displacement.
    • Repeat with right foot. Rest and repeat as above.

    One-leg squats with lateral hops
    • Stand with your left foot forward and your right foot back, with your feet about one shin-length apart from front to back and hip-width apart from side to side. Place the toes of your right foot on a block or step 6-8 inches off the ground and direct most of your weight through the mid-point of your left foot;.
    • Now, bend your left leg and lower your body until your left knee is bent at an angle of 90°;
    • Then hop about 6-10 inches to the left on your left foot, keeping the right foot in place;
    • Hop back to ‘centre’, then repeat on the other leg and return to the starting position, maintaining upright posture with your trunk and holding your hands at your sides;
    • Perform 2 sets of 12 squats on each leg, with a one-minute break between sets.

    High-bench step-up
    • Begin from a standing position on top of a high bench (approximately knee height), with your body weight on your left foot and your weight shifted toward the left heel. The right foot should be free and held slightly behind the body
    • Lower the body in a controlled manner until the toes of the right foot touch the ground, but maintain all of your weight on the left foot
    • Return to the starting position by driving downward with the left heel and straightening the left leg
    • Repeat for the prescribed number of repetitions, and then switch over to the right leg
    • Maintain absolutely upright posture with the trunk throughout the entire movement, with your hands held at your sides (with or without dumbbells)
    • 2 to 3 sets of 15 to 20 repetitions with 2 to 3 minutes recovery between sets.

  9. Muscle Tension and Restoring “Pop” to Your Running | The Athletic Time Machine Says:

    […] some pretty fantastic ideas on the topic.  Another interesting read in this subject is Canute’s Efficient Running Site, particularly as it relates to running surfaces and […]

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    Muscle stiffness and running efficiency | Canute’s Efficient Running Site

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