Detection of epimuscular myofascial forces by Golgi tendon organs

Huub Maas,Hiltsje A Smilde,Wendy Noort,Timothy C Cope,Jacob A Vincent,Paul Nardelli

doi:10.1007/s00221-021-06242-1

Abstract

Skeletal muscles embed multiple tendon organs, both at the proximal and distal ends of muscle fibers. One of the functions of such spatial distribution may be to provide locally unique force feedback, which may become more important when stresses are distributed non-uniformly within the muscle. Forces exerted by connections between adjacent muscles (i.e. epimuscular myofascial forces) may cause such local differences in force. The aim of this exploratory study was to investigate the effects of mechanical interactions between adjacent muscles on sensory encoding by tendon organs. Action potentials from single afferents were recorded intra-axonally in response to ramp-hold release (RHR) stretches of a passive agonistic muscle at different lengths or relative positions of its passive synergist. The tendons of gastrocnemius (GAS), plantaris (PL) and soleus (SO) muscles were cut from the skeleton for attachment to servomotors. Connective tissues among these muscles were kept intact. Lengthening GAS + PL decreased the force threshold of SO tendon organs (p = 0.035). The force threshold of lateral gastrocnemius (LG) tendon organs was not affected by SO length (p = 0.371). Also displacing LG + PL, kept at a constant muscle–tendon unit length, from a proximal to a more distal position resulted in a decrease in force threshold of LG tendon organs (p = 0.007). These results indicate that tendon organ firing is affected by changes in length and/or relative position of adjacent synergistic muscles. We conclude that tendon organs can provide the central nervous system with information about local stresses caused by epimuscular myofascial forces.

Highlights

Feedback from Golgi tendon organs plays an important role in the neural control of movement (Akay et al 2014; Donelan et al 2009; Gregor et al 2006; Maas et al 2007; Communicated by Francesco Lacquaniti.Rossignol et al 2006), the regulation of limb stiffness (Nichols 2018) and the senses of force and heaviness (Proske and Gandevia 2012)
We recently showed that lengthening a synergistic muscle, and the force exerted via epimuscular connections, affected the firing behavior of muscle spindles located within a neighboring muscle (Smilde et al 2016)
Lengthening GAS + PL by 6 mm resulted in an increase in the force exerted at their own distal tendons prior to the ramp-hold release (RHR) protocol (Fig. 3A, p < 0.001), and in a decrease in the force exerted at the distal tendon of SO (Fig. 3B, p < 0.001)

Summary

Introduction

Rossignol et al 2006), the regulation of limb stiffness (Nichols 2018) and the senses of force and heaviness (Proske and Gandevia 2012). Tendon organs are located at the junction between a group of skeletal muscle fibers and aponeurosis or tendon (Huber and DeWitt 1900; Zelena and Soukup 1983). When a force is exerted, in response to excitation of the inseries muscle fibers or whole muscle lengthening, the tendon organ will be stretched. Tendon organs are generally known as receptors signaling muscle force. As tendon organs respond predominantly to contractions of muscle fibers that are in the same muscle region (Cameron et al 1981), they can be considered “regional tension sensors” (Proske and Gandevia 2012)

Methods

Results

Conclusion