Regional variation in recruitment and physiological properties of a single muscle

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This research published in the Journal of Neurophysiology was carried out in Amsterdam by Jo De Ruiter as part of his doctoral thesis supervised by Professor Anthony J Sargeant and Arnold de Haan. It was part of a series of studies examining the regional differences within a single muscle of physiological properties and hence pattern of recruitment in response to different intensities of exercise.

Fast-twitch muscle unit properties in different rat medial gastrocnemius muscle compartments

DeRuiter CJArnold de HaanAnthony J Sargeant.

Journal of Neurophysiology
J Neurophysiol. 1996 Jun;75(6):2243-54
  • 1. The effect of muscle unit (MU) localization on physiological properties was investigated within the fast-twitch fatigue-resistant (FR) and fast-fatigable (FF) MU populations of rat medial gastrocnemius (MG) muscle. Single MG MUs were functionally isolated by microdissection of the ventral roots. FR and FF MU properties of the most proximal and distal muscle compartments were compared. The most proximal and distal compartment are subvolumes of the MG innervated by the most proximal and distal primary nerve branch, respectively. A subsample of the isolated units was glycogen depleted and muscle cross sections were stained for glycogen and myosin-adenosinetriphosphatase.
  • 2. It was shown that proximal FF and FR units reached optimum length for force production at shorter muscle lengths compared with the distal FR and FF units.
  • 3. The fast MUs of the proximal compartment had small territories that were located close to and/or within the mixed region (containing type I, IIA, IIX, and IIB fibers) of the muscle. The fast MUs of the distal compartment had greater territories that were located in the more superficial muscle part (containing only type IIX and IIB fibers) and in some cases spanned the entire area of the distal muscle compartment.
  • 4. FR and FF MUs consisted of muscle fibers identified histochemically as type IIX and IIB, respectively.
  • 5. Within each of the FR and FF MU populations, MUs that were located in the most proximal muscle compartment were more resistant to fatigue compared with the units located in the most distal compartment.
  • 6. Cross-sectional fiber areas were smaller for the proximal FR and FF fibers, but specific force did not differ among units. Consequently, when account was taken of the innervation ratio, the proximal FR and FF units produced less force than distal units of the same type. Tetanic forces were 87 +/- 27 (SD) mN (proximal FR), 154 +/- 53 (SD) mN (distal FR), 142 +/- 25 (SD) mN (proximal FF), and 229 +/- 86 (SD) mN (distal FF).
  • 7. The present findings suggest that with increasing demand placed on rat MG during in vivo locomotion, recruitment is likely to proceed from proximal to distal muscle parts within the FR and FF MU populations.
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Within a single muscle there can be large differences in fatiguability and other physiological properties

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This research carried out in Amsterdam under the direction of Professor Anthony J Sargeant demonstrated how within the same anatomical muscle there can be quiet different physiological properties in different areas of the same muscle. This work was part of the PhD research of Jo de Ruiter supervised by Professor Tony Sargeant and Arnold de Haan.

Repeated force production and metabolites in two medial gastrocnemius muscle compartments of the rats

De Ruiter CJArnold de HaanAnthony J Sargeant.

Journal of Applied Physiology
J Appl Physiol. 1995 Dec;79(6):1855-61
  • The most proximal and distal motor nerve branches in the rat medial gastrocnemius innervate discrete muscle compartments dominated by fast-twitch oxidative and fast-twitch glycolytic fibers, respectively. The functional consequences of the difference in oxidative capacity between these compartments were investigated. Wistar rats were anesthetized with pentobarbital sodium (90 mg/kg ip). Changes in force of both compartments during 21 isometric contractions (train duration 200 ms, stimulation frequency 120 Hz, 3 s between contractions) were studied in situ with and without blood flow. Without blood flow, force and phosphocreatine declined to a greater extent in the proximal than the distal compartment compared with the run with intact flow. After the protocol without blood flow, when flow was restored, the time constants for force recovery (which were closely associated to the recovery of phosphocreatine) were 37 +/- 7 (SD) (proximal compartment) and 148 +/- 20 s (distal compartment). It was concluded that the proximal compartment had a four times higher oxidative capacity and, therefore, a superior ability for repeated force production.

Different regions within the same muscle can have very different properties

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This research was part of the PhD thesis of CJ (Jo) de Ruiter. It shows how within a single muscle there may be marked regional differences in physiological characteristics implying task dependent differences in recruitment patterns of motor units. The work was carried out under the direction of Anthony J Sargeant and Arnold de Haan.

Physiological characteristics of two extreme muscle compartments in gastrocnemius medialis of the anaesthetized rat

De Ruiter CJArnold de HaanAnthony J Sargeant
Acta Physiologica Scandavica
Acta Physiol Scand. 1995 Apr;153(4):313-24
Rat medial gastrocnemius (GM) muscle is a compartmentalized muscle. The functional properties and fibre type composition of the most proximal and most distal compartment were studied in in situ preparations. The proximal compartment contained predominantly fast twitch oxidative fibres. The distal compartment was mainly composed of fast twitch glycolytic fibres. With the use of two small electrodes placed around the primary nerve branches, both compartments could be separately stimulated within the same muscle. The length-force relationship was less broad and maximal twitch and tetanic forces were obtained at lower muscle lengths for the proximal compartment. The differences (mm) were 0.9 +/- 0.2 and 1.2 +/- 0.2 for maximal twitch and tetanic force (120 Hz) production, respectively (P < 0.001). The shortening velocity for maximal power production was lower (P < 0.001) for the proximal compartment (proximal: 57.1 +/- 2.7 mm s-1, distal: 73.1 +/- 3.0 mm s-1). During a standard fatigue test the fatiguability was significantly lower for the proximal compared with the distal fibres. Our findings suggest that the proximal compartment is likely to be activated in vivo during activities requiring relatively low power outputs for longer time periods. In contrast the distal compartment is probably recruited only during high power demanding short lasting activities. The presented model makes it possible to study fatigue related changes in power production of the ‘red’ and ‘white’ areas of the GM separately in a way that is probably meaningful with respect to in vivo function.

Growth related changes in muscle properties

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The effect of growth on the dynamic performance of rat medial gastrocnemius muscle was studied. From approximately 1.5 to 5 months of age specific force increased by 18%.

Reductions were found in both optimal stimulation frequency (from 120 to 100 Hz) and optimal shortening velocity (by 16%) indicating that the fibres became slower. Specific power did not change during growth but was obtained at a lower shortening velocity. Possible mechanisms for the observed changes are discussed

Effect of pre-stretching muscle on fatigue

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European Journal of Applied Physiology
Eur J Appl Physiol Occup Physiol. 1991;62(4):268-273

In activities such as running, many muscles of the lower extremities appear to be actively stretched before they are allowed to shorten. In this study we investigated the effect of an active pre-stretch on the fatigability of muscles. Thus muscle contractions were compared in which shortening was preceded by an active isometric phase or by an active stretch.

Rat medial gastrocnemius muscle-tendon complexes (with arrested blood flow) performed a series of ten repeated contractions (1.s-1) with either an active stretch or an isometric phase preceding the shortening. Contraction duration (0.45 s), and shortening duration (0.3 s), distance (6 mm) and velocity (20 mm.s-1) were the same in both types of contraction. Work output during the ten shortening phases was approximately 40% higher in the contractions with an active pre-stretch; in contrast, high-energy phosphate utilization was similar. Over the ten repeated contractions reduction of work output during the shortening phases of both types of contraction was similar in absolute terms (approx. 9.5 mJ). It is suggested that all the extra work performed during the shortening phases after a pre-stretch originated from sources other than cross-bridge cycling, which are hardly affected by fatigue. However, reduction of work output in relative terms, which is how the reduction is often expressed in voluntary exercise, was less after a pre-stretch (26% vs 32%), giving the impression of protection against fatigue by an active pre-stretch.

Effect of Stimulation Frequency on Efficiency of Muscle

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F. Abbate was one of Professor Anthony J Sargeant’s PhD students who submitted this published research as a chapter in his PhD thesis. The research was jointly supervised with Arnold de Haan.
Journal of Applied Physiology. 2002; 92(5):2089-96

ABSTRACT The influence of stimulation frequency on efficiency (= total work output/high-energy phosphate consumption) was studied using in situ medial gastrocnemius muscle tendon complexes of the rat. The muscles performed 20 repeated concentric contractions (2/s) at 34°C. During these repeated contractions, the muscle was stimulated via the severed sciatic nerve with either 60, 90, or 150 Hz.

The muscle was freeze-clamped immediately after these contractions, and high-energy phosphate consumption was determined by measuring intramuscular chemical change relative to control muscles. The average values (±SD) of efficiency calculated for 60, 90, and 150 Hz were 18.5 ± 1.5 (n = 7), 18.6 ± 1.5 (n = 9), and 14.7 ± 1.3 mJ/μmol phosphate (n = 9). The results indicate that the efficiency of the muscles that were submaximally activated (60 or 90 Hz) was higher (+26%,P < 0.05) than that of those maximally activated (150 Hz). Additional experiments showed that the low efficiency at maximal activation levels is unlikely to be the result of a higher energy turnover by the Ca2+-ATPase relative to the total energy turnover. Therefore, alternative explanations are discussed.

Repeated contractions affect the geometry of muscle and hence the force generated

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This study carried out by Costis Maganaris demonstrated how repeated contractions result in tendon creep – which by altering the geometry of human muscle changes the maximum force that is delivered.
Journal of Applied Physiology. 2002 Dec;93(6)

Abstract The aim of this study was to investigate the effect of repeated contractions on the geometry of human skeletal muscle. Six men performed two sets (sets A and B) of 10 repeated isometric plantarflexion contractions at 80% of the moment generated during plantarflexion maximal voluntary contraction (MVC), with a rest interval of 15 min between sets. By use of ultrasound, the geometry of the medial gastrocnemius (MG) muscle was measured in the contractions of set A and the displacement of the MG tendon origin in the myotendinous junction was measured in the contractions of set B.

In the transition from the 1st to the 10th contractions, the fascicular length at 80% of MVC decreased from 34 +/- 4 (means +/- SD) to 30 +/- 3 mm (P < 0.001), the pennation angle increased from 35 +/- 3 to 42 +/- 3 degrees (P < 0.001), the myotendinous junction displacement increased from 5 +/- 3 to 10 +/- 3 mm (P < 0.001), and the average fascicular curvature remained constant (P > 0.05) at approximately 4.3 m(-1). No changes (P > 0.05) were found in fascicular length, pennation angle, and myotendinous junction displacement after the fifth contraction. Electrogoniometry showed that the ankle rotated by approximately 6.5 degrees during contraction, but no differences (P > 0.05) were obtained between contractions. The present results show that repeated contractions induce tendon creep, which substantially affects the geometry of the in-series contracting muscles, thus altering their potential for force and joint moment generation.