Elsevier

Journal of Biomechanics

Volume 45, Issue 6, 5 April 2012, Pages 913-918
Journal of Biomechanics

Residual force enhancement during voluntary contractions of knee extensors and flexors at short and long muscle lengths

https://doi.org/10.1016/j.jbiomech.2012.01.026Get rights and content

Abstract

Residual force enhancement (RFE) is a term describing the observation that muscle tension during a contraction that includes a stretch and hold remains above that during an isometric contraction at the hold length. RFE has been observed during in vitro and in vivo experiments, but results involving voluntary contractions are mixed, particularly with respect to large muscles. The purpose of this study was to determine if RFE can be observed in large muscles such as knee extensors and flexors at joint configurations corresponding to the ascending and descending limbs of the muscle force–length curve. Two groups of twenty participants (ten males and ten females per group) performed maximum voluntary contractions on a Biodex machine in purely isometric conditions and in isometric conditions immediately following eccentric stretch. Knee extension trials were performed at 40° (short muscles) and 100° (long muscles) flexion from full extension (0°), and knee flexion trials were performed at 70° (short muscles) and 10° (long muscles) flexion. Stretch-isometric trials terminated at these angles following 30° of eccentric motion at 30°/s. Statistically-significant RFE was observed for both tasks at long-muscle joint configurations, but was not observed for either task at short-muscle joint configurations. Passive torque enhancement was also observed following muscle relaxation at long-muscle joint configurations for both tasks, but for only knee flexion at short-muscle joint configurations. These results reinforce for voluntary contractions of large muscles the RFE behavior observed in smaller muscles, and provide further evidence that RFE occurs primarily on the descending limb of the muscle force–length curve.

Introduction

Residual force enhancement (RFE) is a term describing the observation that muscle tension during a contraction that includes a stretch and hold remains above that during an isometric contraction at the hold length (Abbott and Aubert, 1952). This phenomenon has been demonstrated in vitro for single fiber preparations (Edman et al., 1982, Rassier et al., 2003, Peterson et al., 2004) and whole muscle preparations (Abbott and Aubert, 1952, Herzog and Leonard, 2000, Schachar et al., 2004), and in vivo with electrical stimulation (Cook and McDonagh, 1995, De Ruiter et al., 2000, Lee and Herzog, 2002, Pinniger and Cresswell, 2007) and with voluntary contractions (Lee and Herzog, 2002, Oskouei and Herzog, 2005, Pinniger and Cresswell, 2007, Tilp et al., 2009, Hahn et al., 2010). However, the physiological mechanisms responsible for RFE, and the role of RFE in daily muscle activities, remain poorly understood.

Two prevailing theories have been proposed to explain RFE in actively-contracting muscles: sarcomere length non-uniformity (SLNU) and cross-bridge action (CBA). The SLNU theory holds that the stretch of a muscle on the descending limb of the force–length curve lengthens some of the weaker sarcomeres far into the passive elastic region while most of the stronger sarcomeres experience little to no stretch, and thus the muscle produces an enhanced force corresponding to the stronger sarcomeres prior to stretch (Julian and Morgan, 1979, Morgan, 1990, Morgan et al., 2000). The CBA theory holds that RFE can occur through additional cross-bridge attachments during stretch, or through an increase in the average force produced by each cross-bridge (Sugi and Tsuchiya, 1981, Lee and Herzog, 2002, Lee and Herzog, 2008).

The SLNU theory arose in part from early observations of RFE exclusively on the descending limb of the muscle force–length curve (Julian and Morgan, 1979, Edman et al., 1982, Morgan, 1990, Morgan, 1994). It has been argued (e.g., Herzog et al., 2006) that any observed RFE on the ascending limb would compromise the theory because the positive slope of the ascending limb creates an inherent stability for the lengths of the serially-arranged sarcomeres. That is, on the ascending limb the sarcomeres will increase strength with stretch, causing the weaker sarcomeres to stretch into equilibrium with stronger sarcomeres at which point all sarcomeres should stretch uniformly. Though some studies have reported a small RFE on the ascending limb (Sugi, 1972, Peterson et al., 2004, Herzog and Leonard, 2002) if conditions are optimal (Herzog et al., 2006), other studies report RFE only on the descending limb (e.g., Edman et al., 1982, Brown and Loeb, 2000, Morgan et al., 2000). And, some question remains as to whether RFE occurs on the ascending limb during voluntary contractions (see Section 4).

In recent years attention has been drawn to the study of RFE during voluntary contractions because of the possible role of RFE during daily activities. Several studies have tested RFE at single joint positions with muscles on or near the descending limb of the force–length curve, and have reported somewhat mixed results. Studies involving smaller muscles of the hand (Lee and Herzog, 2002) and moderately-sized muscles of the ankle (Pinniger and Cresswell, 2007, Tilp et al., 2009) have observed RFE during maximum and submaximum voluntary contractions. However, Hahn et al. (2007) studied RFE during maximum voluntary contractions of the human knee extensors and reported no significant effect. Hahn et al. (2007) did report reduced activation levels during the stretch-isometric contractions, and reasoned that the lack of RFE may be due to increased inhibitions in the large muscles. We also speculated that, due to the two-stage ordering of trials, fatigue may have masked an RFE effect (see Section 4).

The present study had two aims: (1) determine if RFE can be observed during voluntary contractions of large leg muscles, and (2) test whether RFE can be observed on both the ascending and descending limbs of the force–length curve during voluntary contractions. To accomplish these aims we have measured maximum voluntary isomeric and stretch-isometric knee extension and flexion torques at joint positions corresponding to short and long muscle lengths. In addition, to permit comparison of total RFE with any observed passive residual enhancement, we have measured the passive knee torques occurring during the rest phase following muscle contractions.

Section snippets

Participants

Two groups of twenty participants with no prior joint injuries in the lower body participated in this study. Ten males and ten females performed the knee extension task, and ten males and ten females performed the knee flexion task. All participants were college students (age=22.4±2.5 yr) with the exception of one 53-year-old female participant. The study was approved by the Baylor University IRB, and each participant completed a medical history and informed consent form.

Procedures

Prior to testing, each

Results

The 2×5 (condition×interval) repeated measures ANOVA showed that stretch-isometric torques significantly exceeded purely isometric torques at joint positions corresponding to long muscle lengths, but not at joint positions corresponding to short muscle lengths. That is, RFE was observed during both knee extension and knee flexion tasks for long muscles but not for short muscles (Fig. 2, Fig. 3). In all analyses, no interaction was observed between interval and condition (p>0.05).

For the knee

Discussion

The first aim of this study was to determine if residual force enhancement (RFE) could be observed during maximum voluntary contractions of large leg muscles actuating the knee. Though many previous studies have observed RFE in muscle preparations or with electrical stimulation, only a few have observed RFE during voluntary muscle contractions that more closely reflect what may occur during daily activities. Lee and Herzog (2002) reported 12–16% RFE in maximum contractions of the small adductor

Conflict of interest statement

Both authors declare no conflict of interest.

Acknowledgment

This study was funded in part by Baylor URC internal grant.

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