Eccentric Contractions: The Hypothesis

Statement

The basic hypothesis is that rapid lengthening of active muscle at long length does not occur by uniform lengthening of the sarcomeres or anything approximating uniform lengthening, but can be more nearly described as occurring by rapid, uncontrolled lengthening of individual half sarcomeres, one at a time, in order from weakest towards the strongest. The term "popping" is used to describe this process.

Rationale

The argument to support this rests on the two common characteristics of muscle, the isometric length-tension curve and the isovelocity force-velocity curve. The existence of a descending limb of the length-tension curve implies an unstable distribution of sarcomere lengths in the following sense. Any departure from uniform sarcomere length will lead to disparities in isometric tension, with longer sarcomeres being weaker in the sense of having a lower isometric force. However a series connection requires equal force in all elements. This will cause the longer sarcomeres to be lengthened more rapidly, becoming even weaker. This inequalities laeading to an increase in inequalities is the instability.

The force-velocity curve provides some damping to this situation, so that the sarcomeres can make up for finite differences in isometric tension by finite differences in velocity. This does not prevent the non-uniformities from developing, but does limit the speed at which this occurs. That is, the instabilites are damped. The steep force velocity curve for slow lengthening implies that the instabilities are heavily damped, so that non-uniformites will develop slowly. Note that this description making several assumptions. 1. That the length-tension and force-velocity curves are multiplicative. This follows from the crossbridge model, and can be demonstrated for shortening of tetanized single frog fibres. 2. That this process is occuring slowly enough for the fore-velocity curve to be operative.

The force-velocity curve for lengthening is however found to assymptote to a near constant value for rapid lengthening, as in the "back" part of the surface plot. This means that any sarcomere that reaches this part of the curve becomes undamped, in the sense that it is unable to generate more tension (or maintain tension in the face of declining isometric capability) by lengthening more rapidly. At this point the instability becomes instantaneous. While this situation could occur in an extremely non-uniform fibre after an extremely long duration tetanus, it will most often occur during a stretch of a fibre, ie an eccentric contraction.

Once a sarcomere reaches this point, it will be unable to support the existing tension at any speed, and will lengthen very rapidly, limited only by intertia and passive damping, until the tension in passive structures (shown in the surface plot below) rises to carry the tension. Note:

• This will cause a shortening of all the other sarcomeres with a consequent fall in tension. However in a real fibre with many thousands of sarcomeres and significant compliance in the connections, this fall will be infinitessimal.
• This discussion assumed that the force-velocity curve continues to operate at high velocities. While this is not true, it is unlikely that departures from this significantly affect the process.
• These popped sarcomeres may well be stretched beyond any overlap of thick and thin filaments, at least for frog single fibres at moderately long lengths.

These weakest sarcomeres will in general be scattered throughout the three dimensional lattice of the muscle, that is independently scattered along most of the length of each myofibril. Electronmicrographs of muscle show close sideways connections between the filaments of a myofibril, but much more freedom for myofibrils to slide past each other. When a fibre is stretched to a long length, the shortest and so strongest sarcomeres are found near the ends, but no such pattern has been reported for the location of the weakest sarcomeres.

The movie below shows some of this. The red bands are the A bands and the yellow are the thin filament arrays. The black lines are the z-lines. All myofibrils stretch equally, but different myofibrils stretch by popping different sarcomeres.

The extreme non-uniformity of sarcomeres developed during a stretch is expected to remain as long as stimulation continues. However, when stimulation stops, the descending limb of the length tension curve ceases to exist (the passive tension increases with length) and passive structures are expected to return the sarcomeres to a near uniform pattern.

To a first approximation, each popping half-sarcomere is expected to approxiately double its sarcomere length. This implies that the fraction of sarcomeres popped is approximately equal to size of the stretch as a fraction of optimum length. That is a 10% stretch should pop on the order of 10% of the sarcomeres.

Analogy

An analogy is the stretching of a flexible straw. The folds have a length-tension curve that includes a region with negative slope, that is, where tension decreases with increasing length. The folds are not intentionally made unequal, but lengthening of the straw will always involve popping the folds, one at a time, in order from the weakest towards the strongest. The speed of lengthening will not affect the process involved, nor the tension required at any point in the process.

Explanation of known facts

Rise of tension during stretch

When lengthening occurs by popping, the tension at any point is simply the yield point of the next weakest sarcomere. By definition, the next weakest sarcomere will be stronger than the last, so the tension must continue to rise. This will predict that the rise will be steeper in a fibre with greater non-uniformity.

Fall of stiffness during stretch

A popped sarcomere is expected to be less stiff than an active sarcomere. This comes simply by comparing the passive length-tension curve with the stiffness of active muscle. Consequently, popping of more sarcomeres will result in a decreased stiffness. Note that this decrease will be somewhat countered by the increasing slope of the passive length-tension curve as tension increases, so that the stiffness of already popped sarcomeres will increase as the stretch progresses. This will also contribute to the fall of stiffness that accompanies the fall of tension at the end of a stretch.

Permanent extra tension

At the end of a stretch, a minority of sarcomeres will be at long length carrying tension passively, while most will be near the initial sarcomere length, generating tension actively. It is these sarcomeres that will determine the level of the isometric tension, which will consequently be close to that appropriate to the initial length. As the tension falls after the end of the stretch, the popped sarcomeres will shorten, so prolonging the raised tension.

On the ascending limb of the length tension curve, the weakest sarcomere will be stretched most, and so become stronger. Consequently, there will be no increase in non-uniformity, and the tesnion will be appropriate to the final length, as observed. Furthermore, the permanent tension after a stretch can never be more than the isometric tension at optimum length, also as observed.

Assymptote of force-velocity curve for rapid lengthening

As the tension during the stretch is determined by the strength of the next weakest sarcomere, a sarcomere force-velocity curve that fell at high velocities would never been seen when stretching a fibre.

Shift of length-tension curve after many eccentric contractions.

The disruption of sarcomeres effectively converts them from active to passive sarcomeres, as Katz noted would explain all his observations. This shift assumes new importance as a quantitative measure of an early (pre histological damage) effect of the eccentric contractions. It is fully developed at the end of a bout of eccentric contractions.

Damage from eccentric exercise

The damage arises as explained. The loss of calcium homeostasis has been previously postulated as an early event in the damage process. The known dependencies of eccentric exercise damage, ie more damage from more contractions and from longer stretches follow naturally.