 Fascia and motor control Eur J Transl Myol 29 (3): 185-194, 2019 - 185 - Fascial organisation of motor synergies: a hypothesis Alessandro Garofolini (1), Daris Svanera (2) (1) Institute for Health and Sport (IHES), Victoria University, Melbourne, Australia; (2) Independent researcher, Brescia, Italy This article is distributed under the terms of the Creative Commons Attribution Noncommercial License (CC BY-NC 4.0) which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited. Abstract In the field of biomechanics and motor control understanding movement coordination is paramount. Motor synergies represent the coordination of neural and physical elements embedded in our bodies in order to optimize the solutions to motor problems. Although we are able to measure and quantify the movement made manifested, we do not have confidence in explaining the anatomical bases of its organisation at different levels. It is our contention that the flexible hierarchical organization of movement relies on the fascial structurers to create functional linkages at different levels, and this concept attunes with the neural control of synergies. At the base of movement organization there is a (somatic) equilibrium point that exists on the fascia where the neurologically- and mechanically-generated tensions dynamically balance out. This somatic equilibrium point is at the base of postural control, afferent flow of information to the nervous system about the state of the muscles, and of the coordinative pre- activation of muscular contraction sequences specific for a synergy. Implications are discussed and suggestions for research and clinical applications are made. Key Words: Motor control, degrees of freedom, myofascial continuity, movement coordination, muscle spindle. Eur J Transl Myol 29 (3): 185-194, 2019 The anatomical elements involved in the organisation of motor synergies, and voluntary movements in general, are still not clear for several reasons. First, the difficulty in explaining movement organisation which is inherited in the traditional anatomical understanding of the human body, often seen as the sum of the parts that compose it.1 Second, classical anatomy has been based for centuries on the concept that we can extract a part, we can study how it works by breaking it down to its components, and once we have all the parts extracted and analysed, the sum of all those parts will explain how the human body works.2 Although this view has been challenged over the years,3,4 our understanding of function is still biased by a segmental anatomical knowledge of our body. This is manifest in biomechanical models of the musculoskeletal system that represent muscles as independent units connected to the bones at their origin and insertion.5,6 In this perspective, muscle forces are transmitted serially, and the torque developed around a joint depends only on the muscle’s torque arm geometrical configuration. Movement patterns are therefore, analysed through a linear framework of isolated muscle groups, based on singular muscle attachments and isolated joint actions. However, complex movements result from simultaneous interaction of multiple parts of many human systems and denying this may overlook the complexity of the human system and limit our understanding of movement organisation. An alternative view regards the human body as a tensegrity-like network,7 with the connective tissue (fascial structure) acting as linking component.8 In this view, the direct morphological continuum between muscles and fasciae is at the base of the mechanical interactions between agonist muscles (i.e., producing the same movement at a joint) as well as between antagonistic muscles;9 this tensional continuous coordinates intermuscular and extramuscular force transmission.10 The central role of the fascia in movement coordination has been shown in a series of experiments,10-13 where muscle tendons were transposed (insertion shifted to antagonistic location) and movement recorded. The assumption that a muscle would change its action after tendon transposition was rejected: muscle still conserved its function due to the orientation of the connective tissue. This proves the controlling function of the fascia over muscle activity. While evidence consistent with the role of synergies in movement organisation is growing,14-17 much work is still needed to delineate their anatomical basis.18 Non co mmerc ial us e o nly Fascia and motor control Eur J Transl Myol 29 (3): 185-194, 2019 - 186 - Although it is relatively easy to observe a synergistic movement, explaining the anatomical structures responsible for generating and organising such a movement is not an equally easy task. Research has focused on whether synergies have a neural origin,19 or they are a product of experimental or biomechanical constraints.20 It is believed that basic foundation of covariant muscle combinations (motor primitives) are modulated by the central nervous system to perform complex motor behaviors,21,22 that is, information is encoded into motor neurons (either by genetic design or learnt through experience) so that higher neural discharge rate is present in a preferred movement direction.23 However, by varying the length change of muscle groups individually, synergies between muscles emerge as a result of non-neural coupling,20 showing that the central nervous system does not need to control a group of muscles to observe muscle activation.24 Synergies are difficult to investigate because it is still not completely clear how the nervous system combines synergies, or how and where (anatomically) the synergies are scaled and weighted.25 In our hypothesis, both neural and non- neural control of motor synergies coexist and they are linked through the fascial system. Aim of this review is to present possible anatomical explanations of the phenomena – synergies – described and quantified in motor control. We will look at synergies and their pillars from a fascia point of view, giving evidences for an alternative way of thinking about movement organisation. Before proceeding to examine synergies, it is important to define the fascial anatomical organisation, and its physiological meaning. Fascial System Fasciae are classified as a proper connective tissue that are dense and regular,26 made of collagen and elastic fibres; the former gives structure while the latter gives elasticity to the tissue. At different levels, the type of fibres and their orientation will define the role of the connective tissue. In this section we will illustrate the muscular fasciae (or deep fasciae); for a comprehensive review of the cellular characteristics of the fasciae see Stecco C, Macchi V, Porzionato A, et al., 2011 and Stecco C. 2014.26,27 The muscular fascia (Figure 1) is divided in (from inner to outer layers): 1. The endomysial fascia surrounds muscle fibres; its collagen fibres are directly connected to the basal lamina overlying each muscle fibre.28 The motor (alpha axon) endplate terminates on the endomysium. The outer layer of the endomysium is made of loose connective tissue ensuring gliding between muscle fibres. 2. The perimysial fascia surrounds secondary bundles of muscles. With a small inner layer (connected to endomysial fascia) of loose connective tissue, an external layer of gliding, and an intermediate layer of Fig 1. Representation of the muscular fasciae. Aponeurotic fascia is not displayed as it will contain all muscles with similar directional meaning. Reproduced with permission from Handspring Publishing Ltd, taken from "Fascia: what it is and why it matters" by D. Lesondak (2018). Non co mmerc ial us e o nly Fascia and motor control Eur J Transl Myol 29 (3): 185-194, 2019 - 187 - collagen fibres, the perimysium has high resistance to traction,29 The ends of the neuromuscular spindle insert on to the perimysium. 3. The epimysial fascia surrounds the individual muscles (i.e. bicept brachi); it is a fibrous-elastic tissue closely connected to the muscle. Multiple septa exist connecting the epimysial fascia to the underlying muscle fibres and the perimysium, and the overlying aponeurotic fascia. The intermediate layer is constituted by about 20% of collagen fibres and elastic fibres; those give the ability to the epimysial fascia to resist tractions.29 4. The aponeurotic fascia is the outermost component of the muscular (deep) fascia. It is composed of two (or three) independent layers of about 1% elastic fibers and 80% collagen fibres arranged longitudinally, transversally, and obliquely.30 Each layer has parallel collagen fibres separated from the underlying one by a layer of loose connective tissue that allows collagen fibers to glide freely one onto the other.27 The function of the aponeurotic fascia is to transmit forces, and thanks to the different orientations of the collagen fibres, the aponeurotic fascia can transmit forces in any direction. Somatic Equilibrium Point (SEP) Only 70% of the extrafusal muscle fibres (those that lay outside the muscle spindle) have a tendinous insertion, while 30% have a fascial insertion,31 which allow muscle tension to be transmitted onto the fascia at the level of the epimysium.29 Similarly, the intrafusal muscle fibres (those that lay inside the muscle spindle) tension the perimysium. Thanks to the bindings between different layers and their collagen nature (see previous section), a somatic point of equilibrium is formed on the epimysium that represent the equilibrium between alpha motor- neurons’ activity (extrafusal muscle fibres activation) and gamma motor-neurons’ activity (intrafusal muscle fibres activation). We hypothesise this neuro-mechanical system to be the anatomical base for basal muscle tone and muscle synergies. We acknowledge that computational models already exists for alpha-gamma coordination,32 and they comprised physiologically realistic spinal circuitry, muscles, proprioceptors, and Fig 2. Motor synergies characteristics. Movement intention Premotor area Action Plan Task Elemental variables – (Muscle Spindle) Elemental variables – (Muscle and segmental joint) Elemental variables – (Sequential joints) Elemental variables – (Limbs in diagonal movements) Elemental variables – (Limbs in spiral movements) Action on the environment Movement organisation Spinal cord Spinal cord Spinal cord Retinacula Retinacula Epimysium Multidirectional movement SEP in spiral organisation Synergy- 4 Task-4 (Regulation of Limbs motion in three planes of the space) Aponeurotic fascia Aponeurotic fascia Bidirectional movement SEP in diagonal organisation Synergy- 3 Task-3 (Regulation of Limbs motion in two planes of the space) Unidirectional global movement sequential SEP Synergy- 2 Task-2 (Regulation of Limb motion in one plane of the space) Aponeurotic fascia Ia & IIa Alpha & Gamma neurons Unidirectional segmental movement Epimysium Synergy- 1 Task-1 (Regulation of Muscle activity and segmental join motion) Task-0 (Pre-activation) segmental SEP Action destabilization (ASA) Perimysium Primary motorneurons – co-activation gamma-alfa Alpha & Gamma neurons Primary motor area Synergy- 0 Non co mmerc ial us e o nly Fascia and motor control Eur J Transl Myol 29 (3): 185-194, 2019 - 188 - skeletal biomechanics. Although model behavior can match human movement and postural data, it omits the fascial system, thus its contribution to sensorimotor function. Synergies Degrees of freedom How the body organises redundant degrees of freedom (DoF) is a crucial question in motor control.33 For a system to be redundant, a hierarchical organisation is assumed in which each level has more elemental variables (i.e. n muscles) than the higher level (i.e. m joints) where m