Passive mechanical properties of the medial gastrocnemius muscle of the cat

Abstract

1. This is a report on the history dependence of the passive mechanical properties of the medial gastrocnemius muscle of the anaesthetised cat. 2. The muscle was conditioned with an isometric contraction at the test length, or at 3 mm longer than the test length and then returned to the test length, where the level of resting tension was measured, as well as tension changes during a slow stretch. 3. The level of resting tension depended on the form of conditioning and, at the optimum length for active tension, the history-dependent component was 9 % of the total passive tension. 4. During a slow stretch, tension initially rose steeply up to a yield point, beyond which it rose more gradually. The shape of the tension rise depended on the form of conditioning. The level of tension at the yield point consisted of a stretch-dependent component, the 'short-range tension' plus the resting tension for that length. 5. The short-range tension increased with muscle length to peak close to the optimum for active tension. The slope of the tension rise during a stretch, the short-range stiffness, peaked at 2 mm beyond the optimum. 6. The short-range tension was small immediately after a conditioning contraction but grew in size as the interval was increased up to 60 s, with a time constant of 9.9 +/- 0.6 s. After a series of conditioning movements, it recovered more rapidly, with a time constant of 6.6 +/- 0.5 s. 7. The history-dependent changes in passive tension and the response to stretch are interpreted in terms of the presence, in sarcomeres of resting muscle fibres, of crossbridges between actin and myosin which have very slow formation rates, both at rest and during movements.

Figure 1. The method of muscle conditioning

Tension responses to stretch of the passive medial gastrocnemius muscle of the cat. Tension (upper traces) and length (lower traces) are shown superimposed, in response to two conditioning test sequences. The thick traces show hold-test conditioning, where the muscle was contracted isometrically (for 0.5 s at 15 pulses s⁻¹) and then a slow test stretch (3 mm at 1 mm s⁻¹) was applied 24 s later. For hold-long conditioning (thin traces), the muscle was stretched by 3 mm, held at that length for 1 s then contracted isometrically as before. After 4 s it was shortened back to its original length and a test stretch was applied 20 s later. Note, peak tension during the isometric contractions is not shown. The periods of stimulation are indicated on the length traces. The dotted line below the tension traces indicates zero tension. Muscle length, L_opt–6 mm.

Figure 2. Measurement of short-range tension

At short muscle lengths, up to L_opt (upper panel), there were two components of tension, the level of resting tension (RT) before onset of stretch and the tension during a slow stretch (3 mm at 1 mm s⁻¹) up to a maximum, called the short-range tension (SRT). The dotted line below the record indicates zero tension, the thin continuous line the level of resting tension. At longer lengths (L_opt+ 6 mm) an additional component of the tension rise during stretch was attributed to elastic structures, not associated with short-range properties. To extract this component, the elastic tension (ET), a line was drawn parallel to the second, more gradual tension rise which intersected the tension trace at the start of the stretch (dashed line). It represented the amount by which tension increased with length, independent of short-range properties. For each record with a significant component of elastic tension this was subtracted to derive the short-range tension. The bottom panel shows the record at L_opt + 6 mm after subtraction of the elastic tension. The tension calibration applies to all three panels.

Figure 6. Time course of development of short-range tension

Upper panel, sample records of tension (upper traces) and length (lower traces) during muscle conditioning using five rapid (50 mm s⁻¹) stretch and shortening movements of 5 mm amplitude and lasting 1 s. Following conditioning, a slow test stretch of 3 mm amplitude at 1 mm s⁻¹ was given at various times. Thick traces, conditioning-test interval of 1 s; thin traces, 5 s interval. Lower panel, plot of short-range tension measured at various times after muscle conditioning. ○, means ±s.e.m. from four experiments using movement conditioning. •, values after conditioning with an isometric contraction, 1 s duration at 15 pulses s⁻¹. ▵, values after conditioning with an isometric contraction, 1 s duration at 80 pulses s⁻¹. All measurements were made at L_opt.

Figure 3. Length dependence of passive tension and length to yield point

Upper panel, measured level of resting tension after hold-long conditioning (○) or hold-test conditioning (•). Values are means ±s.e.m. from five experiments. The squares joined by a dotted line indicate, for one experiment, the muscle's active length-tension relation. Asterisks indicate lengths where hold-long and hold-test values were significantly different (P < 0.05). Lower panel, plot of length to yield point against muscle length. •, values after hold-test conditioning; ○, values after hold-long conditioning. Values are means ±s.e.m. At L_opt–10 mm, after hold-long conditioning there was no measurable yield point. After hold-test, only values from three experiments could be used. At L_opt–8 mm for hold-long, only values from two experiments could be used. In both upper and lower panels length has been shown relative to the optimum for active tension (L_opt).

Figure 4. Tension changes during a slow stretch

Tension changes in the passive MG muscle during a slow stretch (3 mm at 1 mm s⁻¹), starting 20 s after muscle conditioning. Upper three pairs of traces, tension; bottom trace, length change. Each pair of tension traces consists of two records superimposed. Thin traces, after hold-long conditioning; thick traces, after hold-test conditioning. The stretches were carried out at three different muscle lengths, L_opt–4 mm, L_opt and L_opt + 2 mm. Dotted lines indicate zero tension.

Figure 5. Length dependence of short-range tension and stiffness

Upper panel, length dependence of the short-range tension (circles, continuous lines) measured in response to a slow stretch (3 mm at 1 mm s⁻¹) after hold-long conditioning (open symbols) or hold-test conditioning (filled symbols). For values at L_opt + 2 mm or longer, the sum of elastic and short-range tensions have also been shown (squares, dotted lines). Lower panel, plot of short-range stiffness against muscle length. Stiffness was calculated from the slope of the tension rise during stretch. Symbols as in upper panel. Asterisks show lengths where values after hold-test conditioning were significantly different from hold-long values (P < 0.05). Values in both panels have been shown only down to a length of L_opt–6 mm because measurements at shorter lengths were unreliable.