The role of connective tissue in the embryology of the musculoskeletal system: towards a paradigm shift

Anatomy and physiology

Classically, more attention is given to the connections between the muscles and the skeleton via the tendons of origin and insertion. The recruitment of muscle fibers generates mechanical tension that, via these tendon connections, produces either musculoskeletal movement or maintenance of a static position, thus stabilizing the body (Turrina et al., 2012). Different authors (Hujing, 2003; Huijing & Baan, 2001a; Huijing & Baan, 2001b; Stecco, 2009a; Stecco, 2009b) describe myotendinous expansions that extend from the deep fascia, or extramuscular connective tissue, of muscles to attach to the deep fascia in adjacent segments, periarticular soft tissues, intermuscular septa, interosseous membranes and neurovascular sheaths (Platzer, 1978; Standring et al., 2005; Tidball & col., 1991). Due to these connections, muscles acquire additional surfaces for leverage and the generation of movement (Huijing & Jaspers, 2005; Stecco, et al., 2010a; Stecco, et al., 2010b; Yucesoy et al., 2010). Via these myotendinous expansions, which are a type of extension of the tendons, muscles can directly stretch deep fascia in a number of body segments in a longitudinal sense (Huijing, 2009; Stecco et al., 2007a). They can also stretch it transversally through intramuscular connective tissue (endomysium, perimysium and epimysium) (Huijing & Jaspers, 2005; Monti et al., 1999; Purslow, 2010), as well as through other parts of the musculoskeletal connective tissue (such as the intermuscular septum and neurovascular bundles).

It is also well established that, during a muscular contraction, not all motor units within recruited muscles are activated simultaneously (Finni et al., 2003; Pappas et al., 2002). The presence of intramuscular connective tissue plays a fundamental role in the synchronization of the many variables involved in force production. (Rowe, 1981), as does the retinacula of deep fascia (Sanchis-Alfonso & Rosello-Sastre, 2000).

Intramuscular connective tissue, from the macroscopic to the microscopic aspect, can be defined as:

Epimysium: thicker than the other elements of the intramuscular tissue, it is formed by large diameter collagen fibers (Sakamoto, 1996). In the extreme of the muscle the epimysium thickens before it merges with the tendons of origin and insertion (Benjamin, 2009) and converges in the paratenon, while the muscle belly, which it covers, forms a thin layer that determines the volume of the muscle. Wherever epimysium of two muscles connects, it forms a connective tissue sheath that envelops vessels and nerves destined to reach these muscles. Between the collagen fibers, there is the ground substance, which is rich in hyaluronic acid and other glycosaminoglycans (McCombe et al., 2001). In particular, the hyaluronic acid component allows collagen fibers to slide freely, allowing relative mobility of intrafascial layers (Stecco et al., 2011).

Perimysium: surrounding the muscle and the tendon of origin and insertion of the same muscle, this perimysium does not present a solution of continuity with the epimysium. The amount of perimysium within each muscle and each region of the body varies. The perimysium divides the muscle belly into fascicles of different sizes. Histologically, perimysium has a smaller percentage of elastic fibers and especially collagen fibers type I, III, IV, V, VI and XII, immersed in a matrix of proteoglycans (Kurose et al., 2006; Petibois et al., 2006). The collagen type I fibers provide the perimysium with great resistance to traction. It is probable that, in the transmission of force generated by the muscle towards bone levers, intramuscular connective tissue play an important role (Turrina et al., 2012). In addition, in between two adjacent muscle bundles is placed the same perimysium that contacts with both fascicles by its opposite surface.

Endomysium: is the thinner portion of intramuscular connective tissue. It is directly in contact with the sarcolemma and therefore with every single muscle fiber. Covering the muscular fiber in its entire surface, it takes on a structural role, similar to the parenchyma within organs (Moore, 1983). Endomysium creates a network that unites adjacent fibers. It is the only intramuscular element that, within each muscular fascicle, has contact with the individual muscular fibers innervated by the same motor unit. Other muscular fibers may be interposed but they may remain inactive during the activation of a given motor unit. Thanks to the endomysium, the muscle fibers that are not recruited represent a ‘true tendon’ for the transmission of force laterally, without having to change length (Trotter, 1990). To analyze the properties and structure of a muscle must take into account the arrangement of fibers in relation to the aponeurosis and tendons. (Finni et al., 2003; Turrina et al., 2012) Figure 4.

Figure 4. Intramuscular septa (ims) of Pectoral Major (PM) disinserted of sternal portion.

Department of Anatomy at the University of Salvador, School of Medicine, Buenos Aires, Argentina.

It is evident that right from embryological development, the fascia determines the structural and functional characteristics of the muscle.

During evolution: the independence of the various segments meant that the myomeres and myosepta were required to align themselves according to new lines of force, thus abandoning metamerism altogether. Previously the entire musculature of a body intervened every time it was moved in any direction, or plane, but at this stage each part of the body required its own musculature (Chiarugi, 1975; Stecco, 2004). In this way, the method of Fascial Manipulation organized into six myofascial units, formed by mono and biarticular fibres as well as muscle spindles, were created for each segment.

The evolutionary process proceeded in the following manner:

From the observation of this process in bony fishes we find that lateral flexion of the trunk stimulated the myomeres to elongate in a cephalo-caudal sense which in turn induced the myosepta-fasciae to align parallel to the traction. Hence, these fibres lengthened and they connected to a number of segments (Figure 5).

Figure 5. Intramuscular septa (ims) of Gluteus Maximus (GM).

Department of Anatomy at the University of Salvador, School of Medicine, Buenos Aires, Argentina.

As a consequence, the myosepta-fasciae, which are no longer metameric, lengthened between the muscle fibres to form the perimysium. The deep muscles maintained parallel fibres between one vertebra and the next, somewhat similar to the first metameric stage. The more superficial muscles however formed links extend over a number of metameres. The multisegmentary muscular fibres have the muscle spindles, which are placed in parallel to them, as their point of reference. The muscle spindle is the connection between the unidirectional muscular fibres and the relative portion of the primordial fascia (Stecco, 2004). Only the presence of the muscle spindles, plus the activation of the muscular fibres in succession, allows for the arrest of movement at any angle of the entire joint range. Due to the muscle spindles and the Golgi tendon organs, the unidirectional fibres intervene in succession during the movement of a body part in one plane (Stecco, 2004). The evolution of peripheral receptors clearly demonstrates how the brain depends upon the fascia in order to be able to formulate the concept of space and time. To enable it to organise movement, in general the brain requires feedback concerning whatever is taking place in the periphery. Normally the free nerve endings are involved in deep somaesthetic activity or the perception of the body´s position and movement in space. This feedback transmits information to the CNS regarding the exact position of any given body segment. The fascia and, in particular, its directional sequences, have a predefined length and therefore can act as a type of measuring device in the periphery. Furthermore, because of its elasticity, it is also capable of applying stretch to neuroreceptors (Kent, 1997); (Stecco, 2004). According to the angle of the articulation and therefore, the fascial stretch, either a sequence, a diagonal or a spiral is activated with each step or movement. In other words the mind initiates a motor scheme and the fascia assists in the process of its realisation (Stecco, 2004). The functional meaning of this relationship between the activity of the muscle, the mobility of intra and extramuscular connective tissue and, function of intermuscular septa to achieve the formation of sequences, diagonals, and the spirals of movement, should be studied by also taking into account the presence of numerous embedded receptors that may play a role in peripheral coordination of movement. (Stecco, 2004; Stecco, 2007a; Stiwell, 1957; Turrina et al., 2012; Yahia et al., 1992).

Organization of movement patterns

In the 1940s, when Doctor Herman Kabat began to develop the concept of Proprioceptive Neuromuscular Facilitation (PNF) (Voss et al., 2001), it was sustained that normal neuromuscular mechanisms were capable of developing a wide range of motor activities within the limits of the anatomical structure, the level of development, and innate and previously learnt neuromuscular responses. In other words, the countless combinations of movement that an individual employs to satisfy everyday needs are acquired by means of a well-established process of development and an abundance of learning situations. Neuromuscular mechanisms are assimilated and become efficient without paying attention to individual muscular activity, reflex activity, or the enormous amount of neurophysiologic reactions involved. In the introduction to the PNF method (Voss et al., 2001) it is stated that ‘movement patterns are mass movement patterns. Mass movement is a characteristic of normal motor activity and it is in consonance with Beevor’s Axiom: the brain knows nothing of individual muscle action, but knows only of movement. In normal motor activity, the varied combinations of movement, or mass movement, demand shortening and lengthening reactions from many muscles and in different degrees. Mass movement, which has the purpose of setting out a specific demand, has to consist of a special combination of movements, ideal to the specific sequence of muscles responsible for that movement and has to allow those muscles to contribute with their action components in a harmonic way’.

More recently, (Myers, 2009) has suggested that perhaps there are not in fact 600 muscles but a single connective tissues system with "pockets, which gives muscles and muscles fibers to settle their spaces in different directions to perform its function.

In neurophysiology, we find that movement is programmed by the mind and carried out by the contraction of the muscle fibers. Nerve impulses generated from the brain determine the displacement of a certain segment and it is subject to a vast number of variables in the periphery (Stecco & Stecco, 2010).

Given that each muscle has fibers with different functions and innervations (Burke et al., 1974), according to the Fascial Manipulation® concept (Stecco, 2004), the musculoskeletal system could be divided into myofascial units (MFUs). Each MFU is said to be composed of motor units responsible for moving a segment in a specific direction and, along with the fascia surrounding these fibers, these forces generate movement vectors. A MFU necessarily includes the nerve components innervating these elements. Furthermore, the main vectors of each MFU generate other smaller, more distant vectors (Stecco, 2013).

The fascial context in which muscle fibers are inserted could potentially coordinate movement in the periphery. The MFU is the element that could synchronize the action of motor units innervated by the same axon. While the brain sends impulses to muscle fibers scattered within the muscle via the axon of a single motor neuron, diminishing the activity of the more distal fibers and increasing it in the most proximal ones in relation to changing positions of the limb or the required force presents neurological challenges. An elastic structure, sensitive to stretch, such as the fascia, could assist modulation of recruitment or inhibition via the activation of mechanoreceptors embedded in this tissue (Stecco & Stecco, 2004) The potential role of these mechanoreceptors in the coordination and synchronization of movement via their proprioceptive function is emphasized. As connective tissue continues in the tendons and the muscle insertions (Hujing, 2003; Huijing & Baan, 2001a; Huijing & Baan, 2001b; Stecco, 2009a; Stecco, 2009b), it also distributes and directs the muscular force to the bone in an appropriate way (Stecco & Stecco, 2010).