tendon. Initially, the primary myotube provides a scaffold for the lon
gitudinal growth of the secondary myotubes but eventually they sepa
rate. At the time of their formation, the secondary myotubes express an
Proliferation ‘embryonic’ isoform of the myosin heavy chains, whereas the primary
of myoblasts myotubes express a ‘slow’ muscle isoform apparently identical to that
found in adult slow muscle fibres. In both primary and secondary
myotubes, sarcomere assembly begins at the periphery of the myotube
and progresses inwards towards its centre. Myofibrils are added con
Fusion of
stantly and lengthen by adding sarcomeres to their ends. Ttubules are
myoblasts
formed and grow initially in a longitudinal direction; since they contain
specific proteins not found in plasma membranes, they are probably
assembled via a different pathway from that which supports the growth
of the sarcolemma. The sarcoplasmic reticulum wraps around the
Primary myotube formation myofibrils at the level of the Ibands.
By 9 weeks, the primordia of most muscle groups are well defined,
contractile proteins have been synthesized and the primitive beginnings
of neuromuscular junctions can be observed, confined initially to the
primary myotubes. Although some secondary fibre formation can take
place in the absence of a nerve, most is initiated at sites of innervation
of the primary myotubes. The pioneering axons branch and establish
contact with the secondary myotubes. By 10 weeks these nerve–muscle
Secondary myotube formation contacts have become functional neuromuscular junctions and the
Secondary muscle fibres contract in response to impulse activity in the motor
myoblasts nerves. Under this new influence, the secondary fibres express fetal
(sometimes referred to as neonatal) isoforms of the myosin heavy
chains. At this stage, several crucial events take place, which may be
Primary dependent on, or facilitated by, contractile activity. As the myofibrils
muscle encroach on the centre of the myotube, the nuclei move to the periphery
fibre and the characteristic morphology of the adult skeletal muscle myofibre
is established. The myofibrils become aligned laterally, and A and


Ibands in register across the myotube produce crossstriations that are
Secondary visible at the light microscopic level. Ttubules change from a longitu
tubules dinal to a transverse orientation and adopt their adult positions; they
may be guided in this process by the sarcoplasmic reticulum, which is
Axon more strongly bound to the myofibrils.
Neuromuscular The myotubes and myofibres are grouped into fascicles by growing
junction connective tissue sheaths, and fascicles are assembled to build up entire
muscles. As development proceeds, the increase in intramuscular
volume is accommodated by remodelling of the connective tissue
matrix.
Maturing
muscle At 14–15 weeks, primary myotubes are still in the majority, but by
fibre 20 weeks the secondary myotubes predominate. During weeks 16–17,
tertiary myotubes appear; they are small and adhere to the secondary
myotubes, with which they share a basal lamina. They become inde
pendent by 18–23 weeks, their central nuclei move to the periphery,
Satellite cell
and they contribute a further generation of myofibres. The secondary
Fig. 5.44 Stages in formation of skeletal muscle. Mononucleate and tertiary myofibres are always smaller and more numerous than the
myoblasts fuse to form multinucleate primary myotubes, characterized
primary myofibres. In some large muscles, higherorder generations of
initially by central nuclei. Subsequently, other myoblasts align along the
myotubes may be formed.
primary myotubes and begin to fuse with one another, forming secondary
Late in fetal life, a final population of myoblasts appears, which will
myotubes. In large animals, such as humans, further generations of new
become the satellite cells of adult muscle. These normally quiescent
muscle fibres are similarly formed. As the contractile apparatus is
cells lie outside the sarcolemma beneath the basal lamina (see Fig. 5.44;
assembled, the nuclei move to the periphery, cross-striations become
Fig. 5.45). Mcadherin, a cell adhesion protein of possible regulatory
visible and primitive features of the neuromuscular junction emerge. Later,


small adult-type myoblasts – satellite cells – can be seen lying between significance, occurs at the site of contact between a satellite cell and its
the basal lamina and the sarcolemma of the mature muscle fibre. These muscle fibre. In a young individual, there is one satellite cell for every
too appear to be derived from cells that originated in the somites during 5–10 muscle fibre nuclei. The latter are incapable of DNA synthesis and
early development. (Redrawn from a figure provided by Terry Partridge, mitosis, and satellite cells are therefore important as the sole source of
Department of Genetic Medicine, Children’s National Medical Center, additional muscle fibre nuclei during postnatal growth of muscle (to
Washington DC.) maintain the ratio of cytoplasmic volume per nucleus as fibres increase


skeletal muscle
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in mass). After satellite cells divide, one of the daughter cells fuses with In humans, unlike many smaller mammals, muscles are histologi
the growing fibre, the other remaining as a satellite cell capable of cally mature at birth, but fibre type differentiation is far from complete.
further rounds of division. In adult skeletal muscle, satellite cells In postural muscles, the expression of type I (‘slow’) myosin increases
provide a reservoir of cells that enable exerciseinduced hypertrophy, significantly over the first few years of life. During this same period, the
and regeneration of muscle after damage (see below). proportions of fibre types in other muscles become more divergent. The
presence in adult muscles of a small proportion of fibres with an appar
Development of fibre types
ently transitional combination of protein isoforms reinforces the view
Developing myotubes express an embryonic isoform of myosin that is that changes in fibre type continue to some extent in all muscles and
subsequently replaced by fetal and adult myosin isoforms. The major throughout adult life. Fibre type transitions also occur in relation to
isoform of sarcomeric actin in fetal skeletal muscle is cardiac αactin; damage or neuromuscular disease; under these conditions, the devel
only later is this replaced by skeletal αactin. The significance of these opmental sequence of myosins may be recapitulated in regenerating
developmental sequences is not known. fibres.
The pattern of expression is fibrespecific and changes over time. In
Growth and regulation of fibre length
primary myotubes, embryonic myosin is replaced by adult slow myosin
from about 9 weeks onwards. In secondary and higherorder myotubes, Muscle fibres grow in length by addition of sarcomeres to the ends of
the embryonic myosin isoform is superseded first by fetal and then by myofibrils. In order for the mean sarcomere length, and hence filament
adult fast myosin, and a proportion go on to express adult slow myosin. overlap, to be optimized for maximum force, the number of sarcomeres
Other fibrespecific, tissuespecific and speciesspecific patterns of must be regulated throughout life. This is achieved by the addition or
myosin expression have been described in mammalian limb muscles removal of sarcomeres in response to any prolonged change of length.


and jaw muscles. For example, if a limb is immobilized in a plaster cast, the fibres of
The origin of this diversity in the temporal patterns of expression of muscles that have been fixed in a shortened position lose sarcomeres,
different fibres, even within the same muscle, is far from clear. It has while those that have been fixed in a lengthened position add sarcom
been suggested that intrinsically different lineages of myoblast emerge eres; the reverse process occurs after the cast has been removed.
at different stages of myogenesis or in response to different extracellular
cues. If this is the case, their internal programmes may be retained or Satellite cells and muscle repair
overridden when they fuse with other myoblasts or with fibres that have
already formed. The fibres that emerge from this process go on to
Until the mid20th century, the mechanisms responsible for mainte
acquire a phenotype that will depend on the further influence of hor
nance and repair of skeletal muscle were unclear. These issues were
mones and neural activity.
largely resolved by the discoveries that multinucleated muscle fibres
were formed by the fusion of mononucleated precursors, myoblasts,
and that a population of satellite cells, so called because of their posi
tion on the edge of the fibre, exist between the basal lamina of the
mature muscle fibre and its sarcolemma, where they constitute 2–5%
of the nuclei enclosed by the basal lamina.
Studies in mouse models, where genetic analysis is possible, have
shown that the functional properties of postnatal satellite cells depend
on the expression of the Pax7 gene, whereas the prenatal development
of muscle is not similarly dependent. This implies that satellite cells are
not simply the relics of prenatal myogenic cells, even though they
appear to be derived from the same embryonic source in the somites.
Moreover, satellite cells are not a homogeneous population: no two
differentiation markers concur completely. This is also the situation
in human tissue (Fig. 5.46). It has yet to be determined whether this
variation reflects a difference in position in the lineage, functional status
or adjacent environment.
The satellite cell has been established rigorously in mice as being
both necessary and sufficient for effective regeneration of damaged
skeletal muscle (Relaix and Zammit 2012). These cells proliferate to


replace their resident region of muscle in 3–4 days and to replenish the
quiescent satellite cell population. In humans, there is histological
Fig. 5.45 An electron micrograph of a satellite cell. Note the two plasma
evidence of the rapid accumulation of myoblasts, presumably derived
membranes that separate the cytoplasm of the satellite cell from that of
the muscle fibre, and the basal lamina (arrows) of the transversely from local satellite cells, at sites of muscle damage. The presumed
sectioned muscle fibre, which continues over the satellite cell (see also central role of satellite cells in muscle growth and adaptation has,
Fig. 5.39a). Compare this appearance with the normal muscle nucleus, however, been questioned by some recent research. Satellite cells are
which is seen in the adjacent fibre at the top of the micrograph. undoubtedly important during early postnatal development and
(Photograph by Dr Michael Cullen, School of Neurosciences, University of growth, and in muscle regeneration following acute injury or eccentric
Newcastle upon Tyne.) damage. In other situations, however, regulation of protein synthesis
Fig. 5.46 Two adjacent sections, fluorescence-
immunolabelled, of a regenerating muscle fibre in
a power lifter’s trapezius. A, Anti-laminin antibody
(red) shows basal lamina. Anti-CD56 (green) is a
marker of myogenic cells and of newly formed
myotubes. B, Basal lamina (red) and myogenin-
positive nuclei (green). Basal laminae outline
transversely sectioned muscle fibres, including the
original outline of the regenerating fibre (centre
field). Numerous small blood vessels, also outlined
by basal laminae, are present and probably reflect
local inflammation. Within the CD56-positive zone,
several nuclei (one arrowed) are positive for
myogenin, indicating their terminally differentiated
status. Numerous other nuclei (Hoechst dye, blue)
within the basal lamina surrounding the area of
regeneration probably include proliferating
myogenic cells and inflammatory cells. (Courtesy
of Ms Mona Lindström and Professor Lars-Eric
A B Thornell, Department of Anatomy, Umeå
University, Sweden.)


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and degradation may be more important determinants of muscle mass fied, and terms denoting action may emphasize only one of a number
(Schiaffino et al 2013). of usual actions. A given muscle may play different roles in different
A detail of wide pathological interest is the demonstration that the movements and these roles may change if the movements are assisted
failing regenerative potency of satellite cells in ageing muscle seems in or opposed by gravity.
large part to be attributable to agerelated changes in the systemic envi
ronment rather than a decline in the intrinsic capabilities of the satellite Fibre architecture
cells themselves (Conboy et al 2005).
Muscles can be classified according to their general shape and the pre
Regulation of muscle mass
dominant orientation of their fibres relative to the direction of pull (Fig.
5.47). Muscles with fibres (cells) that are largely parallel to the line of
Muscles respond to resistance exercise in training, or rehabilitation fol pull vary in form from flat, short and quadrilateral (e.g. thyrohyoid)
lowing illness or injury, by increasing in mass. This process is termed to long and straplike (e.g. sternohyoid, sartorius). In such muscles,
hypertrophy, particularly when applied to the increased muscle bulk individual fibres may run for the entire length of the muscle, or over
that occurs in response to intense physical activity. Individual muscle
fibres increase in size by the synthesis of new myofibril proteins,
increased protein turnover rates and the recruitment of satellite cells to Table 5.2 Terms used in naming muscles
provide new nuclei for existing fibres or to form new myotubes. In
inactivity, as seen in those confined to bed or wheelchair, in immobi Shape Depth Position
lized limbs, and in patients with disorders of voluntary movement, Deltoid (triangular) Superficialis (superficial) Anterior, posterior, medial,
muscles decrease in mass. This is termed atrophy, or disuse atrophy, in Quadratus (square) Profundus (deep) lateral, superior, inferior,
Rhomboid Externus/externi (external) supra-, infra-
contrast to the pathological wasting of skeletal muscle associated with


(diamond-shaped) Internus/interni (internal) Interosseus (between
some disease states, including cancer cachexia, heart failure, diabetes Teres (round) bones)
and obesity. It is also recognized that loss of skeletal muscle mass and Gracilis (slender) Attachment Dorsi (of the back)
function may be a consequence of normal healthy ageing, when it is Rectus (straight) Sternocleidomastoid (from Abdominis (of the abdomen)
Lumbrical (worm-like) sternum and clavicle to Pectoralis (of the chest)
termed sarcopenia. There is experimental evidence that this process may
mastoid process) Brachii (of the arm)
be associated with apoptosis of satellite cells and capillary endothelial Size Coracobrachialis (from the Femoris (of the thigh)
cells (Wang et al 2014). Major, minor, longus (long) coracoid process to the Oris (of the mouth)
Brevis (short) arm) Oculi (of the eye)
Latissimus (broadest)
FORM AND FUNCTION OF SKELETAL MUSCLE Longissimus (longest) Action
Extensor, flexor
Number of heads or Abductor, adductor
The names given to individual muscles are usually descriptive and are bellies Levator, depressor
based on their shape, size, number of heads or bellies, position, depth, Biceps (two heads) Supinator, pronator
attachments or actions. The meanings of some of the terms used are Triceps (three heads) Constrictor, dilator
Quadriceps (four heads)
summarized in Table 5.2. The functional roles implied by the names
Digastric (two bellies)
should be interpreted with caution because they are often oversimpli
Strap with tendinous
Quadrilateral Strap intersections Fusiform Digastric Tricipital Triangular Cruciate
Unipennate Bipennate Radial Multipennate Spiral
B
M
B— Bone
M— Muscle
T
T— Tendon
Fig. 5.47 Morphological ‘types’ of muscle based on their general form and fascicular architecture.


skeletal muscle
113
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Fig. 5.48 The ‘detorsion’ or Vector along tendon Fig. 5.49 Force vectors in
untwisting that results from the an idealized pennate
contraction of a spirally muscle. The increase in
arranged muscle. effective cross-sectional
area made possible by
Force of muscle this architecture outweighs
contraction
the small reduction in the
component of force acting
in the direction of the
tendon.
Vector at 90° to
line of tendon
Relaxed
Contracted
shorter segments when there are transverse, tendinous intersections at If these principles are applied to a long, straplike muscle in which
intervals (e.g. rectus abdominis). In a fusiform muscle, the fibres may the fibres are predominantly parallel to the line of pull (see Fig. 5.47),
be close to parallel in the ‘belly’, but converge to a tendon at one or it will be evident that the whole muscle will be able to contract by 30%
both ends. Where fibres are oblique to the line of pull, muscles may be of its length (the same as each muscle fibre). However, such a straplike
triangular (e.g. temporalis, adductor longus) or pennate (featherlike) muscle contains relatively few muscle fibres, so the maximum tension
in construction. The latter vary in complexity from unipennate (e.g. it can develop will not be great. Compare this to the bipennate muscle
flexor pollicis longus) and bipennate (e.g. rectus femoris, dorsal interos in Figure 5.49, which contains perhaps three times as many muscle
sei) to multipennate (e.g. deltoid). Fibres may pass obliquely between fibres, all set at an angle (typically 30°) to the axis of the tendon. Each
deep and superficial aponeuroses, in a type of ‘unipennate’ form (e.g. short fibre will not be able to contract very far, and the contraction of
soleus), or they may start from the walls of osteofascial compartments the tendon will be even less, because the muscle fibres are pulling on


and converge obliquely on a central tendon in circumpennate fashion it obliquely. So, the bipennate muscle has a poor contraction distance.
(e.g. tibialis anterior). Muscles may exhibit a spiral or twisted arrange However, the total force its fibres can generate will be approximately
ment (e.g. sternocostal fibres of pectoralis major or latissimus dorsi, three times as great as the tension in the straplike muscle. Even after
which undergo a 180°twist between their medial and lateral attach this force is reduced to allow for its obliquity (in this case by cos 30°,
ments). Muscles may spiral around a bone (e.g. supinator, which winds which equals 0.87), the overall tension in the direction of the tendon
obliquely around the proximal radial shaft), or contain two or more will exceed that in the straplike muscle by a factor of 2.6 (3 × 0.87).
planes of fibres arranged in differing directions, a type of spiral some So, the bipennate muscle sacrifices contraction distance for greater
times referred to as cruciate (sternocleidomastoid, masseter and adduc maximum force. This effect would be much greater in the multipennate
tor magnus are all partially spiral and cruciate). Many muscles display muscle shown in Figure 5.47.
more than one of these major types of arrangement, and show regional
variations that correspond to contrasting, and in some cases independ
Force, strength and power
ent, actions.
Direction of force In descriptions of muscle performance, ‘force’, ‘strength’ and ‘power’ are
often used interchangeably but these terms are not synonymous. When
considering human performance, it is possible for strength to increase
Although muscles differ in their internal architecture, the resultant force
without a concomitant increase in the true forcegenerating capacities
must be directed along the line of the tendon, so forces transverse to
of the muscles involved. Strength is usually measured under circum
this direction must be in balance (see Fig. 5.47; Fig. 5.48). In straplike
stances that require the participation of several muscles, and so depends
muscles, the transverse component is negligible. In fusiform, bipennate
on skilful coordination of these muscles as well as the forces they gener


and multipennate muscles, symmetry in the arrangement of the fibres
ate. This disparity can be marked during the early stages of physical
produces a balanced opposition between transverse components,
training.
whereas in asymmetrical muscles (e.g. unipennate muscles), the fibres
Power is the rate at which a muscle can perform external work, and
generate an unopposed lateral component of force that is balanced by
is equal to force multiplied by contraction velocity. Since force depends
intramuscular pressure.
on the total crosssectional area of muscle fibres, and velocity (the rate
Muscles that incorporate a twist in their geometry unwind it as they
of muscle shortening) depends on muscle fibre length, powerful
contract, so that they tend not only to approximate their attachments
muscles tend to be long as well as fat. A prime example is the quadri
but also to bring them into the same plane. Muscles that spiral around
ceps, which is the prime mover when someone stands up from a seated
a bone tend to reduce the spiral on contraction, causing rotation.
position. A lack of power in this and other muscles is the critical factor
that limits the ability of many elderly people to live independently
Force versus range of contraction
(Reid and Fielding 2012).
Muscle fibre architecture varies because some muscles are required to
Actions of muscles
develop a large force on their tendinous insertion, whereas other
muscles are required to move their insertion through a considerable
distance. These demands are largely incompatible and require different Historically, the actions of specific muscles were estimated from simple
muscle architecture. observation. Muscle attachments were identified by dissection, and
The force developed by an active muscle depends on the tension their probable action deduced from the line of pull. With the use of
developed in each muscle fibre. If all of the muscle fibres are parallel localized electrical stimulation it became possible to study the actions
(as in the straplike muscle in Figure 5.47), then the muscle force is of selected muscles systematically in the living subject. This approach
equal to the sum of the tension in each fibre, and so will be propor was pioneered by Duchenne de Boulogne in the mid19th century.
tional to the total crosssectional area of those fibres. The range of However, the study of isolated muscles cannot reveal the manner in


contraction generated by an active muscle depends on the relative which they interact during voluntary movements. Duchenne appreci
motion that can take place between the overlapping proteins in the ated this, and supplemented electrical stimulation with observations
sarcomere, and this sets a natural limit (approximately 30%) to the of patients with partial paralysis to make more accurate deductions
amount of fibre shortening that can take place. Hence, the movement about the way in which muscles cooperate. Manual palpation can
of the tendinous insertion is proportional to the length of the muscle be used to detect muscle contraction, but only in superficial muscles
fibres. under quasistatic conditions. Modern knowledge of muscle action has


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been acquired almost entirely by recording the electrical activity that
accompanies mechanical contraction, a technique known as electromy
ography (EMG). This technique can be used to study activation of deep
as well as superficial muscles, under static and dynamic conditions.
Multiple channels of EMG can reveal coordination between different
muscles that participate in a movement. These data can be further sup
plemented by monitoring joint angle and ground reaction force, and
by recording the movement on camera or with a threedimensional
motion analysis system.
Conventionally, the action of a muscle is defined as the movement
that takes place when it contracts. However, this is an operational defi
nition: equating ‘contraction’ with shortening, and ‘relaxation’ with
lengthening is too simple in the context of whole muscles and real
movements. Whether a muscle approximates its attachments on con
traction depends on the degree to which it is activated, and the forces
against which it has to act.
Movements that involve shortening of an active muscle are termed
concentric, e.g. contraction of biceps/brachialis while raising a weight
and flexing the elbow. Movements in which the active muscle undergoes Fig. 5.50 The attachment of a tendon (pink) to skeletal muscle (orange).
lengthening are termed eccentric, e.g. in lowering the weight previously The regular dense connective tissue of the tendon consists of parallel
bundles of type I collagen fibres, which are orientated in the long axis of
mentioned, biceps/brachialis ‘pays out’ length as the elbow extends.
the tendon and the muscle to which it is attached. A few elongated
Eccentric contractions stretch the collagenous tissue sheaths within
fibroblast nuclei are visible in the tendon. (Trichrome stain.)
muscle (see below), which increases the risk of tears in muscles such as
the hamstrings, and of a more general delayedonset muscle soreness
(Proske and Morgan 2001). Muscle contraction that does not involve
TENDONS
change in muscle length is isometric.
Natural movements are accomplished by groups of muscles. Each
Gross structure and function
muscle may be classified, according to its role in the movement, as a


prime mover, antagonist, fixator or synergist. It is usually possible to
identify one or more muscles that are consistently active in initiating Tendons take the form of whitishlooking cords or straps, with a round
and maintaining a movement: these are its prime movers. Muscles that or oval crosssection. They are composed of dense, regular connective
wholly oppose the movement, or initiate and maintain the opposite tissue; 60% of their dry weight consists of large crimped fibres of col
movement, are antagonists. For example, brachialis is the prime mover lagen type I (Fig. 5.50). Other components of their matrix include
in elbow flexion, and triceps is the antagonist. To initiate a movement, collagen types II and V, elastin, glycoproteins and proteoglycans (Wang
a prime mover must overcome passive and active resistance and impart 2006). Fascicles (bundles) of collagen fibres are orientated mainly par
an angular acceleration to a limb segment until the required angular allel to the long axis of the tendon but are to some extent interwoven;
velocity is reached; it must then maintain a level of activity sufficient they may be conspicuous enough to give tendons a longitudinally stri
to complete the movement. ated appearance to the unaided eye. Tendons generally have smooth
When prime movers and antagonists contract together they behave surfaces, although large tendons may be ridged longitudinally by coarse
as fixators, stabilizing the corresponding joint by increased transarticu fasciculi (as in the osseous aspect of the angulated tendon of obturator
lar compression, and creating an immobile base on which other prime internus). Loose connective tissue between fascicles provides a conduit
movers may act. For example, flexors and extensors of the wrist for small vessels and nerves; it condenses on the surface as a sheath or
cocontract to stabilize the wrist when an object is grasped tightly in epitendineum, which may contain elastin and irregularly arranged col
the fingers. lagen fibres. The loose attachments between this sheath and the sur
Acting across a uniaxial joint, a prime mover produces a simple rounding tissue present little resistance to movements of the tendon.
movement. Acting at multiaxial joints, or across more than one joint, In situations where greater freedom of movement is required, a tendon


prime movers may produce more complex movements that contain is separated from adjacent structures by a synovial sheath.
elements that have to be eliminated by contraction of other muscles. Tendons are slightly elastic and can be stretched by 6–15% of their
The latter assist in accomplishing the movement and are considered to length without damage (Wang 2006). Some of this extensibility is
be synergists, although they may act as fixators, or even as partial attributable to the reorientation of collagen type I fibres, some to the
antagonists of the prime mover. For example, flexion of the fingers at straightening of the crimped (wavelike) structure of these fibres, and
the interphalangeal and metacarpophalangeal joints is brought about some to sliding between adjacent collagen fibrils and fibres (Screen et al
primarily by the long flexors, superficial and deep. However, these also 2004). Sliding is possible because discrete collagen fibres appear to
cross intercarpal and radiocarpal joints, and if movement at these joints reinforce connective tissue in the manner of a ‘chopped fibrecomposite’
were unrestrained, finger flexion would be less efficient. Synergistic material such as fibre glass (Hukins and Aspden 1985), rather than by
contraction of the carpal extensors eliminates this movement, and even forming a fixed scaffold (which would make growth difficult). It takes
produces some carpal extension, which increases the efficiency of the a great deal of energy to stretch a long and strong tendon, and most of
desired movement at the fingers. this elastic ‘strain energy’ can be recovered when the tension is released.
In the context of different movements, a given muscle may act as a During locomotion, the rhythmic storing and releasing of strain energy
prime mover, antagonist, fixator or synergist. Even the same movement in stretched tendons helps to smooth the movement, so that tendons
may involve a muscle in different ways if it is assisted or opposed by (rather than cartilage) act as the body’s natural shock absorbers. This
gravity. For example, in thrusting out the hand, triceps is the prime energy storage and release also reduces the metabolic cost of locomo
mover responsible for extending the forearm at the elbow, and the flexor tion. Tendons are sufficiently flexible that they can be diverted around


antagonists are largely inactive. However, when the hand lowers a heavy osseous surfaces or deflected under retinacula to redirect the angle of
object, the extensor action of the triceps is replaced by gravity, and the pull.
movement is controlled by active lengthening (eccentric ‘contraction’) The vascular supply of tendon is sparse but not negligible. Small
of the flexors. It is important to remember that all movements take arterioles from adjacent muscle tissue pass longitudinally between the
place against the background of gravity and its influence must not be fascicles, branching and anastomosing freely, and are accompanied by
overlooked. venae comitantes and lymphatic vessels. This longitudinal plexus is
augmented by small vessels from adjacent loose connective tissue or
synovial sheaths. Vessels rarely pass between bone and tendon at
osseous attachments, and the junctional surfaces are usually devoid of
TENDONS AND LIGAMENTS
foramina. A notable exception is the calcaneal (Achilles) tendon, which
does receive a blood supply across its osseotendinous junction. During
Forces developed by skeletal muscles are transferred to bone by postnatal development, tendons enlarge by interstitial growth, particu
tendons, aponeuroses and fasciae, whereas ligaments prevent excessive larly at myotendinous junctions, where there are high concentrations
separation of adjacent bones. All of these structures comprise dense of fibroblasts. Growth decreases along a tendon from the muscle to the
fibrous connective tissues containing a high proportion of type I osseous attachments. The thickness finally attained by a tendon depends
collagen. on the size and strength of the associated muscle, but also appears to


Biomechanics
115
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Fig. 5.51 The microstructure of bone at entheses.
A, B, The cortical shell of bone (short arrows) is
very thin at fibrocartilaginous attachment sites. In
these examples showing the attachment of the
tendons of triceps brachii (TB) and of fibularis
longus (FL), the cortical shell is approximately the
same thickness as the underlying trabeculae (T).
T
Note that in A, the superficial trabeculae (long
T
arrows) are aligned along the direction of pull of
the tendon of triceps. C, In marked contrast, the
layer of cortical bone (CB) at the fibrous
attachment site of pronator teres (PT) to the
mid-shaft of the radius, is much thicker.
D, Higher-power view of the cortical calcified shell
of tissue at a fibrocartilaginous attachment site
TB (the calcaneal or Achilles tendon), which consists
of bone (B) and calcified fibrocartilage (CF). In this
specimen, there are two tidemarks, TM1 and TM2,
associated with the cortical shell of calcified
FL
tissue. TM1 is adjacent to the zone of uncalcified
fibrocartilage (UF), and marks the mechanical
boundary between hard and soft tissues. TM2 lies
nearer the bone and indicates an earlier phase of
A B
calcification. Note the relative straightness of the
tidemarks but the highly irregular interface
between calcified fibrocartilage and bone (arrows),
PT CB UF which is important in anchoring the tendon to the
TM1 bone. Sections of human cadaveric bone stained
TM2 with Masson’s trichrome. (Photographs courtesy
of Professor Michael Benjamin, Cardiff University,
from sections cut and stained by S. Redman.)
CF
B
C D
be influenced by additional factors such as the degree of pennation of tilaginous or fibrous (Benjamin et al 2006). In fibrocartilaginous
the muscle. The cellularity, and hence the metabolic rate, of large adult entheses, four zones of tissue can be distinguished: pure dense fibrous
tendons is very low, but increases during infection or injury. Repair connective tissue (continuous with and indistinguishable from the


involves an initial proliferation of fibroblasts followed by interstitial tendon), uncalcified fibrocartilage, calcified fibrocartilage, and bone
deposition of new collagen fibres (Wang 2006). Complete remodelling (continuous with and indistinguishable from the rest of the bone).
(replacement) of the tissue, as seen in bone, does not occur in adult There are no sharp boundaries between zones, and the proportions of
tendons, so healing tendons do not quite recover their original strength. each component vary between entheses. A fibrocartilaginous enthesis is
Tendons can adapt their stiffness and strength to match prevailing usually found where a tendon approaches the bone at a high angle, e.g.
mechanical demands, but the process is slow and may be incomplete triceps brachii (Fig. 5.51A,B,D). At fibrous entheses, which are charac
(Rumian et al 2009). teristic of the shafts of long bones, the tendon approaches the bone at
The nerve supply to tendons is largely sensory and there is no evi an acute angle and merges with the periosteum before attaching to bone
dence of any capacity for vasomotor control. Golgi tendon organs, by dense fibrous connective tissue, e.g. pronator teres (Fig. 5.51C).
specialized endings that are sensitive to force, are found near myotendi Fibrous entheses generally attach to a greater area of bone compared to
nous junctions; their large myelinated afferent axons run within fibrocartilaginous entheses, enabling them to reduce stress.
branches of muscular nerves or in small rami of adjacent peripheral
nerves. They play an important role in ‘tendon reflexes’, which serve to
protect the musculoskeletal system from injury. LIGAMENTS
The microstructure and biology of ligaments is broadly similar to that
Tendon attachments
of tendons (Rumian et al 2007). Ligaments consist mostly of large
crimped fibres of collagen type I, and their cells are predominantly
Muscles connect to bones by means of tendons, aponeuroses and elongated fibroblasts. However, there are two major differences between


fasciae. The epimysial, perimysial and endomysial sheaths within tendons and ligaments: one relating to gross structure, the other to
muscle coalesce at these attachments, and interdigitate with adjacent composition. Structurally, ligaments tend to have fibres orientated in a
collagenous structures to form strong connections in which force trans range of directions because they must resist the separation of bones in
mission is aided by shear stress transfer. more than one direction, whereas collagen fibres in a tendon must align
At the myotendinous junction, muscle fibres separate into fingerlike with tension in the adjacent muscle. More diverse mechanical roles of
processes separated by insertions of tendinous collagen fibres. Although ligaments are also reflected in their composition. For example, the liga
there are no desmosomal attachments at these junctions, other speciali mentum flavum, which joins adjacent vertebrae in the spine, has a very
zations assist in the transmission of force from the interior of the fibre high elastin content which enables it to be stretched more than 80%
to the extracellular matrix. Actin filaments from the adjacent sarcom when the spine is flexed, and yet remain under tension in all postures.
eres, which would normally insert into a Zdisc at this point, instead Maintaining tension is important because this ligament lies adjacent to
penetrate a dense, subsarcolemmal filamentous matrix that provides the spinal cord, and could impinge on it if it became slack (and buckled)
attachment to the plasma membrane. This matrix is similar in character when the spine was moved into extension.
to the cytoplasmic face of an adherens junction. The structure as a
whole is homologous to the intercalated discs of cardiac muscle.
BIOMECHANICS
Integrins at the extracellular surface of the junctional sarcolemma
provide contact with the basal lamina, which adheres closely to colla
gen and reticular fibres (type III collagen) of the adjacent tendon or The purpose of this section is to explain, in a nonmathematical way,
other connective tissue structure. how mechanical principles shape the human musculoskeletal system.
Tendinous attachments to bone (also known as entheses or osteo Mechanical considerations explain why bones are stiff and tendons are


tendinous junctions) have been broadly categorized as either fibrocar tough, why the surfaces of some synovial joints are imperfectly matched,


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Body weight Fig. 5.53 The combined effect of
several muscle forces (M–M) and
1 3
Tensile force, FT body weight can be calculated by
resolving each force into two
components acting in two
Compressive force, FC M
3
a (inn a tt ho ism cic aa sl ely pm ae raa ln lein
l
g af nu dl directions
perpendicular to the mid plane of
the lumbosacral intervertebral
M 1 disc). The components acting in
these two directions are then
summed to give the total
C compressive (C) and shear (S)
Resultant force, M 2 forces acting on the disc. The
R magnitude and direction of the
S
A B C resultant force (R), which
represents the combined effect of
Torsional moment or torque, T all four forces, can be calculated
using trigonometry.
Shear force, FS Bending moment, M
Ultimate strength Ultimate failure
D E F
Fig. 5.52 The effects of different types of loading on a solid object (A) are
illustrated in B–F.
and why some tendons insert closer to joints than others. The emerging
subject of ‘mechanobiology’ considers how cells adapt their matrix to
prevailing mechanical demands and explains why some tissues are
better at doing this than others.
MECHANICAL CONCEPTS
Forces, moments and torques
A force is an action that deforms an object, or that causes it to move,
and can be termed compressive, tensile or shear, according to the 0
Deformation (mm)
manner in which it deforms that object (Fig. 5.52). A force F acting at
the end of a lever of length L will generate a bending moment (F × L) Fig. 5.54 A typical force-deformation graph for a skeletal structure
acting about the pivot point of the lever. A torque or torsional moment subjected to mechanical loading. In the initial ‘toe region’, deformation
increases rapidly with force, but this is followed by a linear region in
(Fig. 5.52F) may be quantified in similar terms. The combined influ


which the deformation increases more slowly, and in proportion to the
ence of several forces can be calculated as shown in Figure 5.53. If the
applied force. The gradient of the graph indicates the stiffness of the
forces all act in the same direction, they may be added. However, if they
structure at any given load. Strength is the force at which an object
act in different directions, each force must be resolved into two imagi
becomes damaged, and this is usually interpreted either as the force at
nary components that act in two anatomically convenient directions at
which the gradient first reduces (the elastic limit) or as the force when the
90° to each other, using simple trigonometry. All components acting
gradient falls to zero (the ultimate strength).
in the same direction are added to form two forces (S and C in
Fig. 5.53), which can be used to calculate the magnitude and direction
of the single resultant force (which has a similar effect to all of the
individual forces combined). Forces acting on a stationary object are
analysed according to the principle that all forces acting in any given
direction must balance each other (i.e. add to zero), and all moments
or torques acting about a given pivot point must also balance each
other.
Mechanical properties of structures
Most anatomical structures deform readily when a sufficient force is
applied to them, but their resistance to deformation increases steadily
as the magnitude of the force increases. The resulting graph of force
against deformation resembles the one shown in Figure 5.54. Stiffness
is the ratio of force to deformation (typical units N/mm) and so is
represented by the gradient of the graph. The initial region of low stiff
ness, or ‘toe region’, is followed by a stiffer region in which the graph
is almost linear. In many biological structures, the ‘toe region’ can be
explained by the straightening out of the zigzag ‘crimped’ structure of
collagen type I fibres, whereas the linear region represents direct stretch
ing of the straightened collagen fibres and some slipping between them.
If the deformed structure springs back immediately to its original
)N(
ecroF
Elastic limit
y
Stiffness = ––
x
‘Linear’ region
y
‘Toe’ region
x
dimensions when the deforming force is removed, the deformation is


termed ‘elastic’; a deformation that shows no sign of recovering is
plastic; a deformation that recovers eventually, but gradually, is visco
elastic (see below). ‘Strength’ is the force at which an object becomes
damaged, and is usually interpreted either as the force at which the
gradient of the graph first reduces (the elastic limit) or as the force when
the gradient falls to zero (the ultimate strength).
Properties of materials
The properties of materials must be expressed in such a way that they
are independent of the size and shape of the structure they constitute.
A force divided by the area over which that force is applied gives a stress
value (force per unit area); the resulting deformation divided by the
original length of the object gives a strain value (fractional or percentage
deformation). Stress divided by strain is the sizeindependent material
equivalent of the stiffness of an object, and is an important physical
property termed the ‘modulus’ (sometimes ‘Young’s modulus’). There
are different types of modulus but essentially they are measures of stiff
ness, or resistance to deformation.


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‘Hysteresis energy’
‘Strain energy’
0
Deformation (mm)
Fig. 5.55 This force–deformation graph shows how an object deforms
when a force is applied to it (upward arrow) and how it recovers its
shape when the force is gradually released (downward arrow). The area
under the loading curve represents the strain energy that has been
expended in deforming the object. The area under the unloading curve
represents the energy that is given up when the object is allowed to
spring back to its original shape. The small area in between represents
energy that cannot be recovered but is dissipated as heat. This is the
hysteresis energy.
Energy and shock absorption
Deforming an object may require a considerable expenditure of energy.
Technically, the work done (i.e. energy expended) is proportional to
the average force exerted, multiplied by the distance moved. This is
mathematically equivalent to the area under the graph in Figure 5.55,
and is referred to as the strain energy, i.e. the energy expended in
deforming the object. If the object has elastic properties, it will spring
back to its original shape when the deforming force is removed, and
all the strain energy is then released. (This release of strain energy Viscoelasticity
explains why a stretched rope can recoil violently if it snaps.) Struc
tures such as coiled springs, which can resist high forces and also
Materials are said to be viscoelastic if they behave partly like a thick
deform extensively, are capable of storing large amounts of energy, and
(viscous) fluid and partly like an elastic solid. Viscoelastic deformations
so can act as shock absorbers when they are continually compressed
change with time, even when the deforming stress is constant, and
and stretched. Tendons act in a similar manner during locomotion:
complete recovery from such deformations also takes some time after
they store strain energy when they are stretched by muscle contraction,
the stress is removed (Fig. 5.56). In most biological materials, viscous
and release most of this energy when the muscles relax later in the gait
behaviour occurs because applied loading causes fluid to flow from the
cycle. A small fraction of the stored strain energy, the hysteresis energy,


most heavily loaded regions to the least loaded, by percolating through
is dissipated as heat (see Fig. 5.55). This heat can cause the tempera
very small (nanometrescale) pores in the matrix, a process that can
ture to rise by several degrees centigrade in large tendons that are
take hours; for this reason, the term poroelastic is often preferred to
involved in vigorous repetitive activity. Any material or structure that is
viscoelastic when referring to tissues such as cartilage.
capable of absorbing large amounts of strain energy before failure is
Creep and stress relaxation are two important manifestations of
termed tough; otherwise it is brittle. From Figure 5.55 it is apparent
viscoelasticity. Creep may be described as continuing deformation
that tough materials must be both strong and extensible. In contrast,
under constant load (see Fig. 5.56), whereas stress relaxation is a
brittle materials such as glass and tooth enamel undergo minimal
gradual decrease in force resisted by a viscoelastic material when it is
deformation and so absorb little strain energy, even though they are
initially deformed by a certain amount, and then held with the same
strong. The shockabsorbing characteristics of tendons are important
constant deformation. Creep can reduce the thickness of loaded articu
during locomotion, making movements smoother and reducing meta
lar cartilage and intervertebral discs, typically by 20% in 5 minutes and
bolic cost (Alexander 1988).
3 hours, respectively. Creep deformation is reversed over a similar time
scale when the compressive loading is reduced and water is reabsorbed.
Liquids Bone creeps at a much slower rate, but in old osteoporotic vertebrae,
creep probably contributes to vertebral deformity (Luo et al 2012).
A liquid has negligible rigidity and so deforms readily to take the shape
of its container. When compressed, it maintains practically the same
MATERIAL PROPERTIES OF SKELETAL TISSUES
volume, but it flows to equalize the intensity of loading within it. As a
result, a static liquid under load exhibits a single internal pressure (force
The material properties of several skeletal tissues are compared in
per unit area) that does not vary with location or direction. Even deli


cate objects are not deformed when immersed in a highpressure liquid Table 5.3.
if they themselves are filled with liquid, because the internal and exter
Bone
nal pressures on them are exactly equal; this explains why cells can
survive high pressures in liquids without damage to their delicate
plasma membrane. Of the musculoskeletal tissues, only the nucleus Bone consists mainly of collagen type I and microcrystals of the mineral
pulposus of intervertebral discs exhibits true liquid behaviour (Adams hydroxyapatite. Collagen gives bone considerable tensile strength, and
2013). Some other tissues, including bone and cartilage, contain liquid renders it very tough when fractured, whereas the mineral component
that is able to move through pores in the solid matrix. gives bone a very high compressive modulus and high compressive
)N(
ecroF
0
Time
Fig. 5.56 The deformation of viscoelastic materials varies with time. In
this example, a load is applied at zero time, which causes an immediate
elastic deformation, followed by a slowly increasing time-dependent
deformation (creep). When the load is removed, some deformation is
recovered immediately, but full recovery is achieved only slowly.
noitamrofeD
Load removed
Creep deformation
Recovery
Elastic deformation
Table 5.3 Tensile material properties of skeletal tissues*
Cortical bone Tendon (ligament) Articular cartilage
Strength (MPa) 130 50–110 5–20?
Modulus (MPa) 17,000 500–1800 (150–800) 4–10
Failure strain (%) 1–2.5 10–20 30–100
*For comparison, alloy steel has a strength of 600 MPa and a modulus of 20,000 MPa.


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strength. Rigidity (stiffness) is the defining characteristic of bone; it MECHANICAL PROPERTIES OF
enables the tissue to provide precisely shaped surfaces in synovial joints SKELETAL STRUCTURES
that will deform very little under load, and it also enables fast locomo
tion when muscles pull on bones. If bones were strong and tough but Long bones
not rigid, rapid muscle contractions would cause them to bend alarm
ingly and would slow the angular movement of limbs.
Long bones are characterized by enlarged ends covered in cartilage, a
long hollow shaft and various bony protuberances. The enlarged ends
Tendon, ligament and fascia serve to reduce contact stress where long bones meet in synovial joints,
and to increase the stability of such joints (Fig. 5.58). A different rela
Tendons, ligaments and fascia consist primarily of densely packed col tionship between stability and mobility can exist in different anatomi
lagen type I fibres, giving these tissues high tensile strength. The crimped cal planes, even for the same joint, e.g. the knee joint favours stability
nature of the collagen fibres allows them to be stretched by up to 15% in the frontal plane and mobility in the sagittal plane. The hollow shaft
before failure, and this combination of strength and extensibility of a long bone confers high strength in bending for a given mass of
enables tendons, ligaments and fascia to absorb more strain energy per material, but also minimizes bone mass and so increases the speed of
unit weight than any other biological material. An important difference movement. Bending strength is increased by having as much bone mass
between tendons and ligaments is that ligaments often contain bundles as possible far from the axis of bending (Fig. 5.59). The precise cross
of collagen fibres orientated in a range of directions, presumably sectional shape of a long bone therefore gives a clear indication of the
because bones can be moved apart in a range of directions, whereas the planes in which the shaft is most likely to be subjected to severe
fibres in a tendon are all aligned with the direction of muscle tension. bending. Bony prominences or processes on long bones serve to


Fascia usually contains collagen fibres aligned in adjacent sheets to increase the lever arm of muscles that are attached to them: if a large
resist forces in at least two different directions. prominence is close to the centre of rotation of a joint, then it can
increase the lever arm by over 100%, and the maximum torque devel
oped by the muscle about that centre of rotation would increase by the
Hyaline cartilage
same amount.
Hyaline cartilage consists mainly of very fine collagen type II fibrils and
large proteoglycan molecules, which have the property of attracting
water and swelling. Collagen gives cartilage its tensile strength and stiff Stability
ness, and the proteoglycans give the tissue a high water content that
confers compressive ‘turgor’. During growth and healing, proteoglycans
enable the growing cartilage to swell and occupy space that later will
be strengthened by other components of the matrix. Articular cartilage
is a particular type of hyaline cartilage that covers the ends of articulat
ing bones; its high water content enables it to distribute loading evenly
on the underlying bone. Since cartilage is softer than bone, it deforms
more when loaded, increasing the area of contact between articular
surfaces and reducing contact stress (Fig. 5.57). Cartilage creep (see
above) causes the area of contact to increase, and further reduces
contact stress. Creep in articular cartilage also causes water to be exuded
into the joint cavity, assisting in fluidfilm lubrication (see below).
Articular cartilage ‘wear’ (loss of material) during high and repetitive
loading is minimized because the collagen type II fibrils in the super
ficial zone are aligned parallel to the surface, an arrangement that
provides maximal resistance to surface splitting and the subsequent
loss of tissue. A B C
Mobility
Fibrocartilage and elastic cartilage
Fig. 5.58 In synovial joints, the shapes of the opposing bone ends largely
Fibrocartilage and elastic cartilage combine the high proteoglycan and determine how much movement is possible, and the stability of the joint.
water content that characterizes cartilage with a high proportion of Tapered bone ends (A) lead to high mobility but low stability (in the plane


either collagen type I (fibrocartilage) or elastin (elastic cartilage). Col of the page). Conversely, very wide bone ends (C) lead to low mobility
lagen type I confers extra tensile strength and toughness, whereas elastin and high stability. Some joints resemble (A) in one plane but (B) or (C) in
fibres provide elastic recoil, i.e. the ability to spring back to shape after others.
large deformations.
A
D
A B
Bone Cartilage
B
C
Fig. 5.59 A cross-section through the shaft of a long bone, showing how
the irregular shape gives information about the bone’s strength in bending
about different axes. Strength will be greatest about the axis A–B
Fig. 5.57 Articular cartilage in a synovial joint is not as stiff as the because a high proportion of bone mass is located a long distance from
underlying bone, so the presence of cartilage in a loaded joint increases this axis, and so will resist bending very strongly. Strength will be minimal
the area of contact (B) compared to a joint without cartilage (A). about the axis C–D for a similar reason.


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Synovial joints MUSCLES AND LEVER SYSTEMS
Typically, synovial joints are designed for full and free movements, but Collagenous architecture of muscle
they must also provide some stability in specific planes (see Fig. 5.58).
In a joint with a small range of movement, intrinsic stability provided Muscles are supported by a hierarchy of collagenous sheaths (endomy
by the articular surfaces and ligaments of that joint may be more impor sium, perimysium and epimysium), which surround individual muscle
tant than the extrinsic stability provided by surrounding muscles. Low fibres, fascicles and whole muscles respectively. Muscles are bound
friction movement is facilitated by the smooth surfaces of articular together into functional groups by collagenous fascia. Together, these
cartilage being made slippery by the presence of the boundary lubricant sheaths create a strong honeycomb structure that contributes to the
lubricin, which is bound to the cartilaginous surfaces. This boundary muscle’s resistance to tension. When muscle is stretched during eccen
lubrication reduces friction during slow movements, especially when tric (lengthening) contractions, high tensile forces in the collagenous
forces are high. During rapid movements, microscopic undulations in structures add to the tension generated by muscle fibre contraction,
the cartilage surface trap small quantities of synovial fluid between the leading to high and potentially damaging forces acting on the musc
articular surfaces, so that fluidfilm lubrication (akin to aquaplaning) ulotendinous junction.
can also occur (Fig. 5.60), and friction and wear are greatly reduced.
The sticky, viscous nature of synovial fluid enables it to persist between Internal muscle forces
the cartilage surfaces for longer than water, which would be squeezed
out much too quickly. Fluidfilm lubrication is assisted by joint incon
Generally speaking, muscle forces exert greater mechanical loading on
gruity, in which the opposing articular surfaces have slightly different
the skeleton than does body weight. For example, during relaxed
curvatures (Fig. 5.61), producing a potential fluidfilled gap that moves
standing, 50% of the compressive force acting on the lumbar spine
as the joint moves, washing synovial fluid across the cartilage surfaces.
arises from the antagonistic activity of the muscles of the back and


Incongruity can also help to reduce peak loading on the apex of the
abdomen, and 50% comes from superincumbent body weight (Adams
joint.
2013). However, when bending the trunk to lift weights from the
ground, more than 90% of the compressive force acting on the spine
Intervertebral discs
can be attributed to muscle tension (Fig. 5.62). Similarly, muscle
forces acting on the knee can exceed body weight by a factor of 200–
Intervertebral discs are composed of three tissues: the anulus fibrosus 400% during stair climbing and during deep squatting movements.
(fibrocartilage), the nucleus pulposus (a hydrated collagen–proteoglycan Muscle forces can exceed the strength of adjacent bones if they contract
gel) and the endplates (hyaline cartilage). The water content of the in alarm, so that normal inhibitory reflexes are suppressed; it is not
nucleus pulposus can reach 90% in children and young adults, enabling uncommon for vertebrae to be crushed by muscle tension during
the tissue to behave like a fluid. When compressive loading is applied major epileptic fits. According to Newton’s 2nd Law of motion (force
to the vertebral column, the fluid pressure in the nucleus presses evenly = mass × acceleration), muscle forces also rise to high levels when
on the adjacent vertebral bodies, even when they are orientated at small attempting to accelerate body parts, e.g. during jumping or throwing.
angles to each other. The anulus resists radial expansion of the nucleus It follows that any attempt to achieve maximum acceleration will natu
and can deform vertically to facilitate spinal bending in various planes. rally require maximal muscle tension. The size and potential dangers
The relatively dense hyaline cartilage endplate helps to maintain a fluid of internal muscle forces are often overlooked, leading some authors
pressure in the nucleus by slowing down water loss into the vertebral to draw spurious distinctions between weightbearing and nonweight
body through perforations in the vertebral endplate. Nevertheless, discs bearing joints, and to suggest erroneously that only the former are
lose approximately 20% of their water gradually, in the course of each subjected to high loading. It is likely that a watchmaker’s finger joints


day. This net loss of water is regained at night when, in recumbency, are subjected to stresses as high, and as often, as those applied to his
the load on the spine is relieved. Diurnal variations in disc water ankles.
content cause adults to be approximately 2 cm taller in the early
morning, and more flexible in the evening.
D
Contact between asperities
Synovial fluid
Cartilage Boundary lubricant
O F
d
1 µm
Fig. 5.60 The articular cartilage surfaces of synovial joints contain
microscopic undulations that trap small quantities of synovial fluid
between the surfaces, enabling fluid-film lubrication to occur. Boundary
lubrication at the points of contact between cartilage asperities
(roughness) is facilitated by lubricants adhering to the cartilage surface.
A B
Synovial
fluid W
F F
Fig. 5.62 During manual labour, muscle tension often rises to high levels
in order to generate sufficient bending moment to move external objects.
Fig. 5.61 Some synovial joints are incongruent in the sense that the In this example, the back muscles act only a short distance (d) from the
opposing articular surfaces have slightly different curvatures. This ensures pivot point in the intervertebral discs (O), whereas the weight being lifted
that there is a fluid-filled gap between them when the joint is subjected to acts on a much bigger lever arm (D). In order for the moments to balance,
low loading (A). Under high loading (B) this gap disappears, but peak the back muscle tension (F) must exceed the weight being lifted (W) by
loading at the apex of the joint remains lower than it would be if the the ratio of D/d. In practice, this can lead to the lumbar spine being
surfaces had the same curvature, and this is a major advantage for an compressed by approximately 500 kg during moderate manual handling.
incongruent joint. The shape of the concave articular surface is (For simplicity, the above analysis disregards the weight of the upper
sometimes referred to as a Gothic arch. Abbreviation: F = loading force. body.)


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Fig. 5.63 Muscle lever systems can be
Force
classified as first-class (A), second-class (B) or
A First-class lever
Motion third-class (C), according to the relative
positions of the fulcrum (or pivot), the muscle
insertion, and the externally applied load.
Fulcrum
Load
B Second-class lever
Motion Force
Load
Fulcrum
C Third-class lever Force
Load
Motion Fulcrum
Muscle lever systems
Muscle tension generates bending moments and torques about joints. A
Moments and torques depend on lever arms as well as muscle forces.
It is conventional (although not particularly illuminating) to distin
guish between three types of muscle lever system (Fig. 5.63). Generally,
the length of the lever arm (the perpendicular distance between the line
of action of the muscle and the centre of rotation of the joint) is more
important than lever type (Fig. 5.64). If the lever arm is short, then a
given muscle contraction will move the joint through a large angle, so
the lever system is suited to large and/or rapid movements of that joint.
Conversely, a long lever arm leads to small and/or slow movements but
F
greater moment generation. Elite weightlifters may have muscle inser d
tions with particularly large lever arms about particular joints.
MOVEMENTS
Movements of bones
B
Movement of a bone is referred to as translation if it does not involve
any change in orientation relative to a fixed frame of reference (or to
another bone). A pure rotation involves no translation, merely a pivot
ing of the bone about some fixed point or centre of rotation. Spin is
the rotation of a bone about its mechanical axis, which for a long bone
would coincide with its long axis. Spin can occur in conjunction with F
other joint rotations (Fig. 5.65). Most body movements involve some
combination of rotation, translation and spin, although the transla d
tional component is often small. 2
Movements at articular surfaces
Fig. 5.64 The precise location of a muscle insertion relative to a joint
greatly influences the function of that joint. A, If the perpendicular


Opposing joint surfaces are never perfectly congruent, but substantial distance (d) between the muscle’s line of action and the centre of rotation
regions of these surfaces may fit together exactly in a certain position of the joint (•) is large, then the joint is suited to slow but forceful
known as the closepacked position, in which the joint is most stable. movements. B, If d is small, then the joint is suited to rapid but less
For example, the closepacked position of the knee joint corresponds forceful movements. Abbreviation: F, force, showing line of muscle action.


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(90° + 90°+ 90°) - (90° + 90°) = 90° Table 5.4 The close- and loose-packed positions of joints
Joint Close-packed position Loose-packed position
Shoulder Abduction + lateral rotation Semi-abduction
Ulnohumeral Extension Semi-flexion
Radiohumeral Semi-flexion + semi-pronation Extension + supination
Wrist Dorsiflexion Semi-flexion
A 2nd–5th Full flexion Semi-flexion + ulnar deviation
metacarpophalangeal
Interphalangeal (fingers) Extension Semi-flexion
90° 1st carpometacarpal Full opposition Neutral position of thumb
Hip Extension + medial rotation Semi-flexion
Knee Full extension Semi-flexion
Ankle Dorsiflexion Neutral position
Tarsal joints Full supination Semi-pronation
90° 90° Metatarsophalangeal Dorsiflexion Neutral position
Interphalangeal (toes) Dorsiflexion Semi-flexion
B C Intervertebral Extension Neutral position
Data from MacConaill MA, Basmajian JV 1977 Muscles and Movements, 2nd edn. New York: Kriger.
Fig. 5.65 Complex movements of the body’s joints are sometimes
required to produce apparently simple movements of the limbs. In this
example, moving the hand as shown from A to B to C requires a hidden
‘spin’ movement of the arm of 90° about its mechanical (long) axis.
Spin Roll Slide
CoR
Fig. 5.66 The surfaces of incongruent joints move relative to each other
by various combinations of spin, roll and slide. Fig. 5.67 When a bone is rotated, the centre of rotation (CoR) can be
located by drawing lines between the initial and final positions of
anatomical landmarks on the bone, and then determining where the
to full extension. In other (loosepacked) positions, the surfaces of perpendicular bisectors of these lines meet. The CoR may not correspond
incongruent joints are not perfectly matched, and are able to move rela to a precise anatomical landmark.
tive to each other by a combination of spin, roll and slide (Fig. 5.66).


In final closepacking, surfaces are fully congruent, in maximal contact be included in Table 5.4. However, most of the positions given do cor
and tightly compressed or ‘screwed home’, the fibrous capsule and liga respond with postures adopted when maximal stress is encountered.
ments are maximally spiralized and tensed, and no further movement
is possible. Closepacked surfaces cannot be separated by normal exter Centre of rotation
nal force (as they may be in other positions), and bones can be regarded
as temporarily locked, as if no joint existed. Closepacking is a final, The centre of rotation is a theoretical concept and may not correspond
limiting position, and any force that tends to further change can only closely to any anatomical landmark or natural pivot. For a finite move
be resisted by contraction of appropriate muscles. Failure to stop further ment of one bone relative to a fixed reference (perhaps an anatomical
movement results in injury to joint structures. Therefore, movement just plane), the centre of rotation can be located by drawing theoretical lines
short of closepacking is physiologically most important. between the initial and final positions of two anatomical landmarks on
Ligaments and articular cartilage are, to a small degree, elastically the bone, and determining where the perpendicular bisectors of these
deformable: in the final stages of closepacking the articular position is two lines meet (Fig. 5.67). Real movements of real joints often involve
an equilibrium between the external moments and torques applied varying combinations of rotation and translation as the movement
(often by gravity) and resistance to tissue deformation by the tense, progresses. It can be instructive to break the whole movement down
twisted capsule and compressed cartilage surfaces. In symmetrical into a series of small movements, calculate the centre of rotation for
standing, the knee and hip joints approach closepacked positions suf each one, and then join up the centres to create the locus of the instan
ficiently to maintain an erect posture with minimal energy. In all other taneous centre of rotation for the whole movement. Joint disease some
positions, the articular surfaces are not congruent and parts of the times leads to an abnormally long and tortuous locus of the centre of
capsule are lax; the joint is said to be loosepacked. Close and loose rotation, because degenerative changes can reduce the restraint to


packed positions of several major joints are shown in Table 5.4 (see motion offered by one or more tissues.
MacConaill and Basmajian (1977)). Capsules are sufficiently lax near
Coupled movements
the midrange of many movements to allow separation of the articulat
ing surfaces by external forces. Opinions may vary in connection with An attempt to move a joint in one plane sometimes causes articular
some of the positions in Table 5.4, e.g. a closepacked position may surfaces to meet at an oblique angle, creating small rotations in other
possibly occur in occasional joints at both extremes of the range of planes. These secondary rotations, which are usually smaller than the
movement. It is difficult to assess the situation in small tarsal and carpal primary rotations, are referred to as coupled movements, e.g. lateral
joints and the first carpometacarpal joints. Intervertebral movements bending of the lumbar spine, which occurs in the coronal plane, also
are the result of integrated simultaneous changes at all elements that normally produces coupled axial rotations. Joint pathology can lead to
make up the intervertebral articular complex, and perhaps should not abnormal coupled movements.


FunCTionAl AnATomy oF THE musCuloskElETAl sysTEm
122
1
noiTCEs
Increased matrix
Matrix deposition
modulus (stiffness)
Decreased Cell Increased
Low strain Adaptive remodelling High strain
mechanical loading Matrix mechanical loading
Reduced matrix
Matrix resorption
modulus (stiffness)
Fig. 5.68 Adaptive remodelling is the process by which musculoskeletal tissues adapt to prevailing mechanical demands. If a tissue is subjected to
increased mechanical loading (right), it deforms more. Cells respond to this increased strain by depositing more matrix and increasing its modulus
(stiffness) until strain levels return to normal. Similarly, reduced loading leads to reduced tissue strain (left), reduced modulus and reduced matrix
deposition until strain levels rise to normal.
MECHANOBIOLOGY to tissue strain, possibly by detecting the resulting fluid flow within the
microscopic canaliculi of the matrix. Cells in cartilage and ligaments
Adaptive remodelling also detect tissue strain, possibly because it deforms the cells in shear
(see Fig. 5.52). Cells in articular cartilage and in the nucleus pulposus
of intervertebral discs appear to be able to detect hydrostatic pressure
Skeletal tissues are generally able to adapt their mechanical properties
in their surrounding medium, although only the cells in the nucleus
to match the forces applied to them. This process is best understood
pulposus would normally experience such a pressure in life. (The pore
for bone, and bone biologists refer to this general principle as Wolff’s
pressure in a ‘biphasic’ solid such as articular cartilage can vary from
Law. As illustrated in Figure 5.68, the amount of deformation of a tissue
place to place and is not equivalent to a single hydrostatic pressure.)
(i.e. the strain) is proportional to the mechanical loading to which it is
Muscle cells respond to strain and microinjury, possibly disturbing
subjected. Cells detect this increased strain and respond by producing
intracellular proteins such as titin. Mechanotransduction appears to be
more extracellular matrix, which increases the modulus (stiffness) of
mediated by matrix molecules such as fibronectin pulling on trans
the tissue and returns strain levels to normal. Similarly, reduced loading
membrane proteins such as integrins, which in turn disturb the cell


leads to reduced tissue strain, reduced matrix synthesis and reduced
cytoskeleton.
modulus, so that tissue strain increases to normal values. This negative
feedback system ensures that bone adapts (remodels) to suit its mechan
Degeneration, injury and frustrated repair
ical environment (Currey 2002). Animal experiments suggest that as
few as 36 relatively severe loading cycles per day are sufficient to
produce a maximal hypertrophic response in bone, whereas fewer than Numerous theories have been propounded to explain degenerative
four loading cycles per day leads to tissue resorption (Rubin and Lanyon changes in skeletal tissues. Most presume that the cells behave abnor
1984). Evidently, bone cells respond to maximal loading rather than mally, possibly because of an unfavourable genetic inheritance, so that
timeaveraged loading. There is some experimental evidence that carti the matrix becomes weakened and physically disrupted. Alternatively,
lage adapts similarly to its mechanical environment (Hall et al 1991). degenerative changes may represent an attempt by the cells to repair a
It would be unlikely that they did not, because the mechanical proper matrix where the primary cause of damage has been excessive mechani
ties of adjacent tissues would rapidly become mismatched, increasing cal loading (Adams et al 2013). Excessive loading does not necessarily
the risk of damage to one of them. However, it is equally evident that imply trauma; normal loading is excessive if the matrix has become
different tissues cannot adapt at the same rates. Highly vascularized abnormally weak on account of an unfavourable genetic inheritance or
tissues such as muscle and bone have the potential to adapt rapidly, age. In poorly vascularized tissues, such as cartilage and tendon, low
whereas poorly vascularized tissues such as large tendons do not. Avas cell density and inadequate transportation of metabolites could lead to
cular tissues such as articular cartilage and intervertebral discs can adapt a vicious circle of minor injury, frustrated repair, tissue weakening and
only very slowly, so that turnover times for some matrix macromole further injury.
cules can be as long as 100 years. Large differences in adaptive potential
between adjacent musculoskeletal tissues could lead to problems in the
less wellvascularized tissue when levels of mechanical loading increase
abruptly (Adams et al 2013). Bonus e-book image
Mechanotransduction


Fig. 5.40 B, The arrangement of titin and nebulin in a skeletal
Various mechanisms have been proposed to explain how cells in mus muscle sarcomere.
culoskeletal tissues detect mechanical loading. Cells in bone respond
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123
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Smooth muscle and the cardiovascular CHAPTER
6
and lymphatic systems
The cardiovascular system carries blood from the heart to all parts of longitudinally, so that the wide central portion of one cell lies next to
the body through a series of tubes, all but the smallest of which are the tapered end of another. Such an arrangement achieves both close
muscular. The muscle in these tubes is of two types: smooth muscle is packing and a more efficient transfer of force from cell to cell. In trans-
characteristic of the walls of blood vessels, whereas cardiac muscle verse section, smooth muscle is seen as an array of circular or slightly
provides the walls of the heart chambers with their powerful contractile polygonal profiles of very varied size, and nuclei are present only in the
pumping action. The general characteristics and classification of muscle centres of the largest profiles (Fig. 6.2). This appearance contrasts mark-
tissues are given on page 103. Smooth muscle also forms an important edly with that of skeletal muscle cells, which show a consistent diameter
contractile element in the walls of many other organ systems of the in cross-section and peripherally placed nuclei throughout their length.
body, e.g. the gastrointestinal tract and the airways. Smooth muscle has no attachment structures equivalent to the
fasciae, tendons and aponeuroses associated with skeletal muscle. There
is a special arrangement for transmitting force from cell to cell and,
SMOOTH MUSCLE
where necessary, to other soft tissue structures. Cells are separated by a
gap of 40–80 nm. Each cell is covered almost entirely by a prominent
In smooth muscle tissue, the contractile proteins actin and myosin are basal lamina, which merges with a reticular layer consisting of a network
not organized into regular sarcomeres, visible as transverse striations, of fine elastin, reticular fibres (collagen type III) and type I collagen
and so the cytoplasm has a smooth (unstriated) appearance. Smooth fibres (Fig. 6.3). These elements bridge the gaps between adjacent cells
muscle is also referred to as involuntary muscle because its activity is and provide mechanical continuity throughout the fascicle. The cell
neither initiated nor monitored consciously. It is much more variable, attaches to components of this extracellular matrix at dense plaques


in both form and function, than either striated or cardiac muscle, a (Figs 6.3A and 6.4), where the basal lamina is thickened; cell–cell
reflection of its varied roles in different systems of the body. attachment occurs at intermediate junctions or desmosomes, formed of
Smooth muscle is typically found in the walls of tubular structures two adjacent dense plaques. At the boundaries of fascicles, the connec-
and hollow viscera. It regulates diameter (e.g. in blood vessels, and tive tissue fibres become interwoven with those of interfascicular septa,
branches of the bronchial tree); propels liquids or solids (e.g. in the so that the contraction of different fascicles is communicated through-
ureter, hepatic duct and intestines); or expels the contents (e.g. in the out the tissue and to neighbouring structures. The components of the
urinary bladder and uterus). The actual arrangement of the cells varies reticular network, the ground substance and collagen and elastic fibres,
with the tissue. The account that follows will therefore be concerned are synthesized by the smooth muscle cells themselves, not by fibro-
with the generic properties of smooth muscle. The more specialized blasts or other connective tissue cells, which are rarely found within
morphologies of smooth muscle are described in the appropriate fasciculi.
regional chapters.
MICROSTRUCTURE OF SMOOTH MUSCLE
Smooth muscle cells (fibres) are smaller than those of striated muscle.
Their length can range from 15 µm in small blood vessels to 200 µm,
and even to 500 µm or more in the uterus during pregnancy. The cells
are spindle-shaped, tapering towards the ends from a central diameter
of 3–8 µm (Fig. 6.1). The nucleus is single, located at the midpoint,
and often twisted into a corkscrew shape by the contraction of the cell.
Smooth muscle cells align with their long axes parallel and staggered
Fig. 6.1 Smooth muscle cells (fibres) in longitudinal (bottom) and
transverse (top) section at the boundary of circular and longitudinal muscle
layers in the human intestinal wall. Individual cells are spindle-shaped with Fig. 6.2 A transmission electron micrograph showing smooth muscle
a single central nucleus, aligned in parallel with neighbouring cells in a fibres in transverse section, two at the level of their single central nucleus.


fasciculus. (Courtesy of Mr Peter Helliwell and the late Dr Joseph Mathew, In several places, the plasma membranes of adjacent cells are closely
Department of Histopathology, Royal Cornwall Hospitals Trust, UK.) approximated at gap junctions (arrows).


SmooTH muSClE And THE CARdiovASCulAR And lymPHATiC SySTEmS
124
1
noiTCES
A
Dense plaque incorporating integrins
Elastin, reticular and collagen fibres
Dense plaque
Dense body
Sarcolemma
Nucleus
Actin
Myosin
Gap junction
Desmosome incorporating cadherins
Intermediate filaments
Caveolae
B
Relaxed Contracted
Dense plaque
Nucleus
Dense body
Fig. 6.3 A, A three-dimensional representation of smooth muscle cells. For clarity, some structural features have been separated for illustration in
different cells. The spindle-shaped cells interdigitate with their long axes parallel; mechanical continuity between the cells is provided by a reticular layer
of elastin and collagen fibres. The cytoskeletal framework consists of intermediate filament arrays (mainly longitudinal) and bundles of actin and myosin
filaments (shown in separate cells) inserted into cytoplasmic dense bodies and submembraneous dense plaques to form a three-dimensional network.
The sarcolemma contains anchoring desmosomes (adherens junctions), gap junctions and caveolae. B, The concertina-like change in shape of smooth
muscle cells as they contract.
Fig. 6.4 Transmission electron micrographs
showing the characteristic features of smooth
muscle cells. Vascular smooth muscle in human
kidney tissue, showing a cytoplasm packed
densely with microfilaments (actin and myosin),
cytoplasmic dense bodies (arrows) and
submembraneous dense plaques (arrowheads).
A basal lamina encloses the cell. The inset shows
four caveolae (C) (vesicular invaginations of the
cell surface at high magnification). These are
associated with receptors, enzymes and ion
channels important in smooth muscle function.
(Courtesy of Dr Bart Wagner, Histopathology
Department, Sheffield Teaching Hospitals, UK.
Inset courtesy of Professor Chun Y Seow,
University of British Columbia.)
C


Smooth muscle
125
6
RETPAHC
The membrane of smooth muscle cells contains molecules such as
proteoglycans, glycoproteins and glycolipids on its exterior surface that
form a thin, negatively charged network, the glycocalyx. Whilst less
studied than that of endothelial cells, the smooth muscle cell glycocalyx
has been shown to be important for mechanotransduction in small
blood vessels. There are also a number of cell membrane-spanning
proteins that extend through the glycocalyx and interact with the extra-
cellular matrix, including cadherins and integrins. These provide struc-
tural and signalling links with the extracellular matrix and other cells,
e.g. at desmosomes. The cytosolic ends of these proteins interact with
components of the cytoskeleton via a complex of other proteins and
kinases, and provide an important signalling pathway linking cell func-
tion to the exterior, which can modulate, for example, gene transcrip-
tion and phenotype (Stegemann 2005).
Discontinuities occur in the basal lamina between adjacent cells, and
here the cell membranes approach to 2–4 nm of one another to form
a gap junction (see Fig. 6.2). These junctions are structurally similar to
their counterparts in cardiac muscle, and are formed by binding of
adjacent connexon complexes on the surface of the two cells. They
provide a low-resistance channel through which electrical excitation Fig. 6.5 A confocal fluorescence micrograph illustrating the innervation of
airway smooth muscle in the developing human lung. Smooth muscle
and small molecules can pass, e.g. enabling a coordinated wave of
cells are arranged circumferentially and are labelled for actin (red); nerves
contraction. The incidence of gap junctions varies with the anatomical
and ganglia form a loose network around the smooth muscle, separated
site of the tissue: they appear more abundant in the type of smooth
from it by up to 40 µm. Nervous tissue is labelled for PGP 9.5 (green).
muscle that generates rhythmic (phasic) activity and they link the
(Reproduced with permission from Sparrow MP, Weichselbaum M,
endothelium functionally with the underlying smooth muscle (myoen-
McCray PB Jr 1999 Development of the innervation and airway smooth


dothelial gap junctions) in small resistance arteries and arterioles.
muscle in human fetal lung. Am J Respir Cell Mol Biol 20: 550–60.)
Caveolae, cup-like invaginations of the plasma membrane with a
resemblance to endocytotic vesicles, are a characteristic feature of
smooth muscle cells, and may form up to 30% of the membrane (see
Fig. 6.4). They are associated with many receptors, ion channels, kinases bears a very large number of nerve endings (up to tens of thousands),
and the peripheral sarcoplasmic reticulum, and may thus act as highly as opposed to a maximum of a few hundred in somatic motor neu-
localized signalling microdomains. They may also act as specialized rones. The neuromuscular terminals of autonomic efferents are consid-
pinocytotic structures involved in fluid and electrolyte transport into ered in more detail on page 64.
the cell. Other organelles (mitochondria, ribosomes, etc.) are largely The neuromuscular junctions in smooth muscles do not show the
confined to the filament-free perinuclear cytoplasm, although in some consistent appearance seen in skeletal muscles. The neurotransmitter
smooth muscle types, including vascular smooth muscle, peripheral diffuses across a gap that can vary from 10 to 100 nm; even separations
mitochondria, sarcoplasmic reticulum and sarcolemma form signalling of up to 1 µm may still allow neuromuscular transmission to take place,
microdomains. although more slowly. The nerve ending is packed with vesicles but the
adjacent area of the muscle cell is not structurally differentiated from
that of non-junctional regions, i.e. there is no distinct synapse.
NEUROVASCULAR SUPPLY OF SMOOTH MUSCLE Intramuscular afferent nerves are the peripheral processes of small
sensory neurones in the dorsal root ganglia. Since they are unmyelin-
Vascular supply ated, contain axonal vesicles and have a beaded appearance, they are
difficult to distinguish from efferent fibres, except by differential stain-
ing for neurotransmitters.
The blood supply of smooth muscle is less extensive than that of stri-
ated muscle. Where the tissue is not too densely packed, afferent and


efferent vessels gain access via connective tissue septa, and capillaries STRUCTURAL BASIS OF CONTRACTION
run in the connective tissue between small fascicles. However, unlike
striated muscle, capillaries are not found in relation to individual cells.
Although electron microscopy revealed the presence of filaments in
smooth muscle some years ago, this observation alone provided little
Innervation
insight into their mode of function because of the lack of any obvious
organization of the filaments. More recent work, using high-resolution
Smooth muscle may contract in response to nervous or hormonal immunocytochemistry, has revealed further details of the internal archi-
stimulation, or electrical depolarization transferred from neighbouring tecture of the cell and suggests a structural basis for contractile function.
cells. Some muscles receive a dense innervation to all cells; these are The model, which is illustrated in Figure 6.3, depends on the mutual
often referred to as multi-unit smooth muscles, and most blood vessels interaction of two systems of filaments, one forming the cytoskeleton
are of this type. Such innervation can precisely define contractile activ- and the other the contractile apparatus.
ity; e.g. in the iris, specific nervous control can produce either pupillary Excluding the perinuclear region, the cytoplasm of a smooth muscle
constriction or dilation. Other muscles are more sparsely innervated. cell effectively consists of two structural domains. The cytoskeleton
They tend to display myogenic activity, initiated spontaneously or in forms a structural framework that maintains the spindle-like form of
response to stretch, which may be markedly influenced by hormones. the cell and provides an internal scaffold with which other elements
In these muscles, which include those in the walls of the gastrointestinal can interact. Its major structural component is the intermediate fila-
tract, urinary bladder, ureter, uterus and uterine tube, innervation tends ment desmin, with the addition of vimentin (which may also be present
to exert a more global influence on the rate and force of intrinsically alone) in vascular smooth muscle. The intermediate filaments are
generated contractions. These muscles have been referred to as unitary arranged mainly in longitudinal bundles, but some filaments intercon-
smooth muscles. The terms multi-unit and unitary smooth muscles are nect the bundles with each other and with the sarcolemma to form a


widely used, but in practice such distinctions are better regarded as the three-dimensional network. The bundles of intermediate filaments
extremes of a continuous spectrum. insert into focal, electron-dense bodies, approximately 0.1 µm in diam-
Smooth muscles are innervated by unmyelinated axons whose cell eter, which are distributed uniformly throughout the cytoplasm and
bodies are located in autonomic ganglia, either in the sympathetic chain also attach to dense plaques underlying the plasma membrane (see Fig.
or, in the case of parasympathetic fibres, closer to the point of innerva- 6.3A). The cytoplasmic dense bodies and submembraneous dense
tion (Fig. 6.5). They ramify extensively, spreading over a large area of plaques are equivalent to the Z-discs of striated muscle cells. They
the muscle and sending branches into the muscle fasciculi. The terminal contain the actin-binding protein α-actinin and thus also anchor the
portion of each axonal branch is beaded and consists of expanded por- actin filaments of the contractile apparatus. These form a lattice of
tions, varicosities, packed with vesicles and mitochondria, separated by obliquely arranged bundles throughout the cytoplasm, which transmit
thin, intervaricose portions. Each varicosity is regarded as a transmitter force to the plasma membrane and thus the basal lamina and extracel-
release site and may be considered as a nerve ending in the functional lular matrix via dense plaques. These are associated with a highly struc-
sense. In this way the axonal arborization of a single autonomic neurone tured arrangement of ancillary proteins, including vinculin and talin,