Defining Biotensegrity

The concept of tensegrity as a new structural principle really started in the 1940’s with Kenneth Snelson,Snelson who explored and developed it through sculpture, and Buckminster Fuller who considered it as part of a wider system of geometry. The application to living organisms began in the 1980’s with Stephen Levin, an orthopaedic surgeon who considered it from a structural, energetic and evolutionary perspective, and Donald Ingber who was investigating the role of the cellular cytoskeleton in angiogenesis.

Many definitions have been proposed for tensegrity but they all vary according to the sculptural, engineering or biological interests of their authors. Engineers have introduced new terminology and mathematics suited to their purpose of making robotics and deployable structures in space, while biologists have approached the subject through experiment and evolutionary considerations. Definitions provide a foundation for further inquiry and both Snelson and Fuller developed their own essentially similar versions.

SNELSON: “Tensegrity describes a closed structural system composed of a set of three or more elongate compression struts within a network of tension tendons, the combined parts mutually supportive in such a way that the struts do not touch one another, but press outwardly against nodal points in the tension network to form a firm, triangulated, pre-stressed, tension and compression unit.”

FULLER: “Tensegrity describes a structural-relationship principle in which structural shape is guaranteed by the finitely closed, comprehensively continuous, tensional behaviours of the system and not by the discontinuous and exclusively local compressional member behaviours.”

hierarchyThere is no standard method of naming tensegrity structures at the present time because artists, mathematicians and biologists take different approaches and use a variety of terminologies; and while it is assumed that developments in one field are directly transferable to another, examples in the literature show that this is not always the case, at least without further qualification. For example, engineering research confuses things by using a classification that is not directly applicable to living tissues, which prompted Levin to introduce the term ‘biotensegrity’ as a means of distinguishing biological tensegrity from its man-made engineering applications.

THE BIOTENSEGRITY MODEL

Most experimental work on biotensegrity has been carried out on cells, which are essentially complete organisms that can be examined individually, collectively, or in parts. Single cells are easily manipulated, abundant in variation and supply and there are few issues that might restrict their use; but multi-celled organisms such as humans are quite different. They consist of multiple heterarchical levels, with all the increases in complexity that might be expected, and examination of any part in isolation can be misleading. The experimental use of cadavers is questionable because they don’t behave exactly like living structures, and in-vivo experimentation is restricted due to practical and ethical issues. Generalizations from a ‘whole-body’ perspective have thus been reasoned from first principles or inferred from models and observation.

Although the principles of tensegrity are easily demonstrated in simple models, they are built with components on the same size scale, and the essence of biotensegrity is structural and functional inter-dependency between components at multiple size scales; and the following should be considered from this perspective.

T-helixesThe ‘simplest’ tensegrity model has 3-struts and is referred to as the T3-prism (simplex or tripod); and is the first of an infinite series that continues with the T4-prism (quadruplex), T5-prism (pentaplex) and T6-prism (hexaplex) etc. Although they are called ‘prisms’ they all have a left or right-handed twist between their polygonal ends that conforms to the formula:

angle of twist = 90o – 180o/n                 where n = number of struts.

Thus a T3-prism has a 30o twist between the ends, a T4-prism has a 45o twist and a T5-prism has a 54o twist etc.

IcosahedronPugh classified them as ‘cylindrical’ tensegrities and when joined end to end they form what can be called T-helixes. Tensegrity helixes are not continuous like springs, but form tubes with struts that are distinct, just like the components in biology (see helix page).

T3-prisms of opposite chirality can form a 6-strut tensegrity with nodes (strut-ends) that almost, but not quite, correspond with the vertices of an icosahedron; Kenner classified this as a spherical tensegrity and it is commonly referred to as the Tensegrity-icosahedron, T6-sphere, T6-icosahedron and T-icosa.

The T-icosa is the most important model from a biotensegrity perspective because of its multiple properties that relate to the minimal-energy efficiencies of the sphere and icosahedron.

A  ‘higher-frequency’ tensegrity-icosahedron can also be made with 30 struts – T30-icosahedron or T30-sphere.

The T-icosahedron is also sometimes described as the ‘expanded octahedron’ and ‘reducing cuboctahedron’, and relates to its place in the jitterbug – a model that demonstrates the changes in energy state from one position to another.

oct_expandThis model sequence shows how the T-icosahedron as an ‘expanded octahedron’ can be developed from the octahedron, with the central struts passing through the middle of each other, followed by the struts and cables dividing, and the separated struts expanding into the 6-strut model. The term ‘expanded octahedron’ also relates to the octahedral phase of the jitterbug – a dynamic energy system that shows how these ‘energy shapes’ can transform from one to another.

Similarly, the term ‘reducing cuboctahedron’ derives from contraction of the vector equilibrium (cuboctahedron) into the icosahedral form, followed by the octahedron.

STRUTS AND CABLES

double_T-icosaIn describing simple models, tensioned elements are often called cables or cords and compression elements are struts, but the distinctions between ‘cables’ and ‘struts’ can be relative. One of the simplest models is the T-icosa, six compression struts suspended between twenty-four tension cables, with nodes of attachment closely matching (but not quite) the vertices of an icosahedron.

In the model shown, two T-icosa’s of different size are joined together by replacing the strut from the model on the right (red dotted) by a cable from the model on the left, which now pulls the nodes of the ‘strut’ apart. We now have an apparent paradox because it is still a cable with respect to the left model but continues to behave like a strut as far as the right model is concerned. It could be said that the entire [left] model has taken the place of the [right] strut, or the entire [right] model the place of the [left] cable, but they have actually become united into a different tensegrity configuration as part of a simple heterarchy. An example of how this might apply in the fascial network is given below and further significance to biological development is described later.

Originally considered as mere packing tissue, fascia is known to play an important role in the transfer of tension.Huijing; Stecco It is continuous with the extra-cellular matrix that surrounds virtually every cell in the body, is part of a heterarchy that connects to every level,Guimberteau and has been described as part of a biotensegrity system.

fascia 2Considering a sheet of tensioned fascia between two bones, or even both ends of the same bone, any two points along that tension line (x,y) will be separated by a pull from either end. The points are held apart by tension, but as the tissue between them is functioning like the ‘virtual’ strut described above, it could behave as such to other parts lower down in a tensegrity hierarchy. Fascia could thus be considered as a network of tensioned cables and [virtual] ‘struts’, but only if it is part of a larger tensegrity system that includes ‘real’ struts such as bones at a higher level .

At the macro level, bones (struts) are compressed by muscles and fascia under tension. Muscles are cables that generate axial tension on contraction, but the resulting changes in their diameter also make them variable length compression struts perpendicular to this, which probably contributes to the tension in associated fascia and force appearing at tendons. The balance of ‘agonist/antagonist’ muscle tensions has been shown to reduce stress concentrations in long bones (bending stresses), making them compatible with the resiliency required of tensegrity struts. Sverdlova

Any particular piece of a tensegrity structure might thus be a cable and strut at the same time, depending on how it is considered within the heterarchy, or change emphasis from one to the other throughout movement. Each part may be affected by multiple tensional or compressional influences, but these will ultimately resolve into one or the other at any particular point in space and moment in time. In a sense the difference between what we call ‘cables’ and ‘struts’ is just relative, a useful way of functionally distinguishing between components, but it has its limitations.

icosa_cablestrutIn this multi-unit polymer of the T-icosa, every cable is under tension and every strut under compression, but the whole structure can be stretched to form a cable (tension) or compressed to form a strut, and each of these could be part of other levels in the heterarchy of a larger structure, and so on. In a biological context, the stability of any particular part may depend on a huge number and variety of smaller components, each one with specific material properties that affect how it responds to tension and compression; these will then influence the mechanical properties of other components at different levels in the heterarchy.

Tension and compression can also be described in various ways that depend on how and where they are being considered.

TENSION AND COMPRESSION

Tension and compression result from the action of forces on particular structures. In simple models, tensioned cables pull on the ends of compression struts and try to shorten them, while the struts resist the pull of the cables and hold the cable ends apart; they automatically balance in a state of minimal energy.

Actin and Myosin MyofilamentAt atomic and molecular levels the forces of attraction (tension) and repulsion (compression) ultimately balance through tensegrity and stabilize as crystals and organic molecules. Connelly; Edwards These configurations assemble spontaneously because of the inter-related principles of close-packing, geodesic geometry and minimal-energy (see geodesics page). Van der Waal forces can both attract and repel, depending on the relative position of atoms or a change in pH. Ionic and covalent bonds attract and maintain a fixed distance apart that depends on the atoms involved; hydrogen bonds attract but are a bit flexible in spacing; and then there is steric repulsion. ‘Attraction’ and ‘repulsion’ seem to be better terms at the nano scale, although the same principles operate at all levels.

cablePull’ (tension) and ‘push’ (compression) are also commonly used terms, and in simple models tensioned cables pull on the nodes and compress the struts, while the struts resist this by ‘pushing’ the nodes apart. Some cables in complex tensegrities could also pull on strut ends and make them longer as part of a functional mechanism regulating strut length. Conversely, the struts could elongate and push on the cables, whose tension now increases, or shorten and become tensioned as the cables try to pull their ends apart. Tension and compression always act in straight lines but can have effects in other directions.

A floppy cable is not under tension until its ends are pulled apart and it starts to straighten itself. As it does so, the middle of the cable pushes to the side (perpendicularly) anything that might be in its way, ceasing this when it becomes straight. Similarly, the orientation and angles of all the tension cables pulling on a node contributes to the resultant compressional force pushing into the strut (‘parallelogram of forces’ in mechanics terminology), and in a balanced tensegrity structure this is always an axial load. A tension vector thus leads to a compression one when there is a change in angle, and vice versa, and more tension means more compression. Interestingly, a tensioned structure will generally tend to get thinner in the middle, ie. at 90o (‘convergent compression’) while a compressed one bulges (‘divergent tension’), and both have a positive Poisson ratio.  The T-icosa and many biological tissues demonstrate the opposite effect and a negative Poisson ratio.Alderson

curvesIn the cytoskeleton, microtubule length increases in response to a pull from the extracellular matrix, while actomyosin motors are able to modulate this by increasing actin tension and maintain a dynamic balance, or generate tension that itself pulls on the matrix. Cellular growth may generate a push on surrounding cells/tissues, and an increase in muscle diameter (on muscle contraction) pushes on associated tissues. Blechschmidt described how tension and compression influence tissue development as a consequence of unequal growth. He proposed that cartilage develops in regions of dense mesenchyme through a push (compression) from surrounding cells, and an increase in osmotic pressure. Constrained cells then differentiate into chondrocytes, and align in a longitudinal arrangement that pulls on surrounding mesenchyme and leads to muscle formation. Blechschmidt was unaware of the molecular and cytoskeletal interactions that have overshadowed his findings in recent years,Stamenovic; but such mechanical effects have been confirmed to influence morphogenesis.Radlanski

In the tensegrity model of the cranial vault,  tensions in the dural membrane and sutural collagen have the effect of pushing the skull bones (compression) apart (~ 100 microns) because of the particular combination of curves in 3-D around the edges of the bones. The bones remain distinct, or as Fuller described it: in “discontinuous compression” (see biology page).

CONTINUOUS TENSION AND DISCONTINUOUS COMPRESSION

A particular feature of biotensegrity models is their compression elements (struts) that do not touch each other at any point; there are no levers, fixed-fulcrums or bending moments. Considering bones as such implies that the joints between them have similar characteristics, but this has been contentious as anatomy texts assume joint surfaces are compressed together.

Levin observed, during surgery, that normal bones never compress each other in living subjects, and that cartilaginous meniscii are too soft to withstand much compression in any case. This would imply that bones are held apart by soft tissues, but the details of the particular anatomical parts that would enable this remain largely unresolved. One of the reasons is the difficulty in modelling complex joint structures at multiple size scales – a feat easily accomplished in biological heterarchies.

elbowIn the elbow, the brachioradialis muscle has a mechanical advantage over other flexors because of its high attachment to the supra-condylar ridge, yet it is reported to be active in rapid and forced flexion, and extension!. Bizarrely, it is supplied by the same nerve that innervates triceps and anconeus, its supposed ‘antagonists’. When brachioradialis contracts it exerts a distraction force between the bones that is contained by triceps, anconeus and posterior fascia (blue arrow), and it may be that the brachioradialis and anconeus act together as a ‘rapid response unit’ that causes the joint surfaces (humerus and ulna) to just slide against each other, without being compressed, or maybe even maintain a certain amount of space between the bones; with ligaments, capsular and fascial structures providing the necessary proprioceptive feedback. Cretu mathematically analyzed a tensegrity elbow, confirming the feasibility of this proposal. (See the elbow page)

Skelton extended tensegrity definitions in engineering applications and divided it into different classes:

Class 1 – compression struts do not touch (conventional tensegrity as defined by Snelson and Fuller).

Class 2 – compression struts contact each other at their ends through fixed fulcrums and levers.

This division might be useful in robotic structures but is questionable in a biological context without considering joints from a heterarchical perspective. Engineers are not constrained by the laws of natural selection and evolution but by the structural properties of the materials they use, the practicalities of construction and cost. Most man-made structures use materials that are put together in such a way that they can withstand damaging stresses such as shear, torque and bending moments, but also require stronger components to counteract the huge forces generated as they get bigger.

Biological structures have evolved in ways that avoid these stresses by distributing the load amongst smaller components within a heterarchy; if they didn’t, they are likely to collapse through material fatigue and that would be the end of them. For example, increasing tension in the extra-cellular matrix causes integrins within associated cell membranes to cluster in ‘focal adhesions’ and distribute the stresses amongst them;Vogel and in bone, a coupled deformation mechanism between collagen and mineral apatite effectively redistributes the strain energy and protects against micro-fractures.Gupta

The separation of tension and compression into different components allows material properties to be optimized, a result of natural physical processes and evolution, and a significant reduction in mass is achieved in a heterarchical biotensegrity arrangement. In the natural world the most energy-efficient system will always win out, which so far makes tensegrity the most likely candidate in structural evolution. Although biological compression struts can appear to make direct contact with each other at some particular level in the heterarchy, when looked at on a smaller scale they are clearly separate, it is just that the detail of the biotensegrity configuration is not recognized in the first instance; and the knee, elbow and cranial sutures etc are all examples of this. This reasoning goes some way to clarifying Fullers’ assertion that: “everything, properly understood, is a tensegrity structure” and the controversy that followed, which also illustrates the point in biology.Fuller sec 794.00

GEODESIC DOME OR TENSEGRITY

icosasphereThe shape of a geodesic dome is based on the icosahedron, a shape that encloses the largest volume within a given surface area of any regular structure apart from a sphere; subdividing each of its triangular faces into smaller triangles produces a higher order, or frequency (1st,2nd and 4th shown here). A sphere is the simplest of all shapes and any point on its surface is equidistant from the centre, just like the vertices of the icosahedron that it can surround; so a line drawn from the centre through each new vertex will project it onto the surface of that sphere. Each higher order of the icosahedron now gets closer to matching the sphere, and because each point is equidistant from all its neighbours, Fuller termed it the geodesic dome. Although the lines now appear to be curved, when looked at closely they are still lots of straight lines.

A geodesic dome remains stable because of its configuration of triangulated struts; it is ‘obviously’ not a tensegrity. However, if its constituent atoms and molecules are considered as such, as was described earlier, then it must be a tensegrity at the smaller scale but not at the larger – another of those apparent paradoxes with a difference that depends only on the perspective. Although this would literally mean that everything is a tensegrity, the important point that this example illustrates is that things can appear differently at each level in a heterarchy.

icosasIn the construction of a geodesic dome and tensegrity-icosahedron, each strut and/or cable could be made from a series of similar domes or tensegrities, themselves made from smaller shapes within a fractal-like heterarchy.Fuller sec.740.20; Levin The models show a geodesic dome with one strut replaced by a chain of T-icosa, and one with an enlarged vertex beside it. Because the geodesic dome and T-icosa can coexist within each other on the same and multiple levels, so the geodesic dome could become a tensegrity when looked at under a microscope, and the only thing to change would be the size scale.  The same can be said for biological heterarchies such as the knee and elbow joints, where what appear to be simple hinges at the macro level are likely to be complex tensegrity configurations at multiple levels below this.

STRAIGHT OR CURVED STRUTS

icosasphereOne of the principles of geodesic geometry is that two points connect over the shortest path and in 3-dimensional Euclidean space this is always a straight line. However, this is just one of three geometries that describe 3-D space, the others being ‘spherical’ and ‘hyperbolic’.Terrones; Bowick Curves are common in biology and it is useful to make models with curved-struts that are compatible with this because they represent multiple levels of complexity.

Tensegrity structures can assume virtually any shape with the forces of tension and compression separated into ‘cables’ and ‘struts’. Because tension acts in a straight line and always tries to reduce itself to a minimum it causes ‘cables’ to straighten along the direction of stretch. A tensioned structure that resists straightening can create shear stresses that lead to a fracture, while a compressed structure will tend to buckle or bend into a curve if the load gets above a certain limit, and this might also fracture. In spite of this, curves can be a means of minimizing energy,Terrones an important consideration in biology, where component parts automatically arrange themselves according to the forces acting on them.

icosacircleA sphere is the simplest of all shapes and can surround each of the regular (platonic) and semi-regular shapes so that every vertex touches its surface and is equidistant from the centre. A line connecting each vertex now forms a curve on the surface and divides it into equal parts, the ‘geodesic geometry of a sphere’. Each polyhedral edge follows the line of one of the ‘Great Circles’, equatorial lines described on the sphere that surround all the polyhedral axes of symmetry, and the shortest distance between any two points is now a curve. The sphere thus unites the straight lines of the platonic solids (Euclidean geometry) with the curves of spherical geometry, and together they can be used to understand curvature in biology, some particular tensegrity models, and transformations in energy. In the real world, curves are not continuous but made up of lots of small straight lines that just give the appearance of curves at a higher scale.

Curved-struts are upper-level representations of heterarchies, and the forces within them, expressed through spherical geometry at a higher level of complexity (see geodesics page). They only remain stable if they have crystalline or molecular sub-structures strong enough to resist buckling, or they are part of a biotensegrity configuration that eliminates damaging shear stresses by its very nature. T2hierAlthough curves can appear at one or many levels in a complex structure, they must contain components that handle tension and compression in straight lines at some smaller scale in order to remain stable. Here a 2-curved-strut model is shown with its heterarchical equivalent of struts made from T-icosa joined together; the overall appearance is of curves but tension and compression are still acting in straight lines as cables and struts at a lower level; it is the tensegrity configuration that allows it some flexibility in shape without developing shear stresses .

Microtubules can appear to buckle and curve but they are functionally balanced by intermediate filaments in what is probably a tensegrity configuration;Brangwynne curved bones in the skull are at the top of a heterarchy that consists of at least seven different structural levels, etc etc.

Levin introduced the term biotensegrity to describe tensegrity in living systems, and the definitions of Snelson and Fuller are still applicable to this; the laws of physics will always apply no matter what names we use to describe them. Biotensegrity is a description of nature’s structural system and is different from the artificial tensegrities (and limitations) of man-made structures (even though we use the simple stick-and-string models to help understand it).

Some of the examples on these pages may stretch the original definitions but I have tried to reconcile them. Biology generates some interesting quirks and brain-teazers when trying to match the theory with the reality, and hopefully, future definitions will be able to adapt to this by integrating and evolving, whilst at the same time maintaining the essence of the subject.