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1. Biomrchtics.

Vol. 3. pp. 583-592.

Pergamon Press. 1970.

Printed in Great Britain



Department of Zoology, University of Durham, England

three-component model of the muscle is used in which the components change
their values when the muscle is stimulated. In particular the elastic components change not only
their moduli of elasticity but the unstretched lengths decrease when the muscle is in the active
state. When the model is extended to the intrafusal muscle fibres of the mammalian muscle
spindle it can reproduce some of the observed responses to mechanical stretch and fusimotor


large increase in the viscosity compared with

the increase in elasticity.
However, the model had the defect that the
postulated changes in viscosity and elasticity
could not reproduce the behaviour of the
spindle when it changed from a passive state
in zero tension-where
the elastic parts are
not extended- to the active state where tension is generated in the contractile parts of
the intrafusal fibre.
In the present model it is postulated that
upon stimulation not only are the moduli of
elasticity of the elastic components and the
coefficient of viscosity of the viscous component changed, but the unstretched lengths
of the elastic components are reduced. The
behaviour of the model is compared to skeletal
muscle when it is stimulated isometrically and
given controlled mechanical stretches in the
active and passive states. The model is then
incorporated into the muscle spindle to overcome the above-mentioned
defect with the
previous model.

GENERALLY the mammalian muscle spindle

contains two histologically distinct kinds of
intrafusal fibre (nuclear-bag
and nuclearchain tibres), both of which are encircled by
branches of the primary afferent nerve ending
1962: Boyd, 1962; Cooper and
Daniel, 1963). The motor nerve fibres to the
spindle are functionally distinguishable into
two kinds (static and dynamic fusimotor
fibres) according to their effects on the
of the primary ending during
mechanical stretch (Matthews, 1962; Crowe
and Matthews, 1964a, b).
In a recently developed model of the mammalian muscle spindle (Crowe, 1968) many of
its properties could be reproduced in a model
in which the primary ending lies on a serieselastic component which is attached to the
rest of the fibre which consists of a viscous
component in parallel with a second elastic
component. In particular, stimulation of the
spindle by fusimotor nerves produces effects
which are accountable by way of changes in
the visco-elastic properties of the contractile
parts of the intrafusal fibres. It was shown that
the effects produced by stimulation of a
dynamic fusimotor fibre during mechanical
stretch could be reproduced by a relatively
*ReceivedI I


The model of the muscle is shown in Fig. 1.
of two elastic components. The
series elastic component has an unstretched
length L, and elasticity E, and the parallel
It consists



It is thus possible to set up a differential

equation which relates values of F(t) to the
imposed changes of length X. The analysis is,
however, performed more easily by using the
Laplace transform
the theory of which,
together with its application to biological
systems, has been dealt with by Grodins
(1963). In the notation of the Laplace transform, equations (I), (2) and (3) take the form


X(s) = X,(S) +x,(S)


F(s) = E,X, (s)


= E2X2(s)fI/sX,(s).

We can eliminate X,(S) and X2(s) from the
above equations and obtain

Fig. 1. Simple three-component
of the muscle. The two elastic components
are represented
by springs
having unstretched lengths L, and L,,
moduli of elasticity E, and E,. and are
extended by amounts X, and X,. The
viscous component is represented by a
dashpot having a viscosity V2.

elastic component has an unstretched length

& and elasticity Ez.The viscous component
has a viscosity Vz.
If the system is stretched by an amount X
then the two elastic components
will be
stretched by amounts X1 and X2 so that

E,+E2+ V,s

The expression
in the { ) brackets is
the transfer function relating a change in
length of the muscle to the resulting tension
The pattern of stretch that is applied to the
model is the ramp shown in Fig. 2. It consists
of two infinite ramps of slope l/T the first
of which starts at time t = 0. From this is
subtracted the second ramp which starts at
1!= T. The Laplace transform of the whole
ramp of unit height is


Where (X2) is the rate of increase

reckoned positive with increase in X?.


If this expression replaces X(S) in equation

(7) then the Laplace transform of the resultant
tension in the system is given by





In order to produce this stretch a force

F(t) must be applied to the muscle such that
F(t) = E,XI


in X2

E,(E,+ v,s)(l --ems)

(E,+E,+V,s)TsZ .

The inverse Laplace transform

over the two parts of the ramp:


is considered



Tension ?

Lenqf h





: phosei


Fig. 2. Theoretical records of tension development in response to

ramp stretches. Arbitrary values of the components have been
chosen but in records rl and B the value of (E, + E,)irl is five times
that for records C and D.

(a) The dynamic phase T, 2 t 2 0

Over this interval the inverse
transform yields:

E, 2I:,

F(t)= T(E,ElVz


In particular, if T is large, the tension at the
end of the dynamic phase is


F(t) =




x (exp [(v)T]_/_

E, E2

The first term on the right hand side is

dependent upon the viscosity and the slope
of the ramp as well as the moduli of elasticity.
The second term arises purely from the
moduli of elasticity.
(b) The staticphase t > T
For this interval we obtain:






For large values of t the first term on the

right hand side will decay to zero and the
tension in the steady state will depend only
upon the moduli of elasticity:

= iEEyEi, i .
1 1


Thus during the static part of the ramp the

tension in the muscle decays exponentially
to a steady value. The amount by which it
decays, for large values of T, is given by
F (viscous)

T(E, f E.,_ ) .




The pattern of the tension response

ramp stretch is shown in Fig. 2.

to a

The terms in X, can be eliminated from equation (3) so that we obtain



Consider a muscle in the resting state

and at zero tension. If it is stimulated isometrically a tension is developed.
In the
excited state the elasticity increases since
a greater force is now required to extend the
muscle by a specified amount. But increases
in the values of the moduli of elasticity alone
cannot account for the tension produced in the
excited muscle that was previously at zero
tension because the values of X, and X, are
zero. In the present model, not only does
stimulation produce increases in elasticity
and viscosity, but the unstretched lengths of
the elastic components are reduced as well.
It is assumed, as a simplification, that the
changes take place abruptly at the onset of
stimulation and that the components of the
system immediately revert to their original
values at the cessation of stimulation. In the
passive state the elastic components have
unstretched lengths Lluand & respectively
(Fig. 3A), but immediately upon stimulation
these values change to L,8and LzJso that the
elastic components are initially extended by
amounts X,O and Xzo (Fig. 3B), and the tension will immediately rise to the value EISXIo,
where E,S is the elasticity of the series elastic
component of the muscle in the excited state.
The subsequent values of the tension are
given by the equations (2) and (3) except that
E2"and VzS,the component values of the
system in the excited state, are inserted in
place of E, , .% and vz.
If the muscle is held at constant length then
X = X, +X, = constant


where X1 and X,, which are time-dependent,

are the amounts by which the elastic parts of
the system are extended.
We differentiate equation (15) to obtain
(Xi) = - (X2).


= E,"X-X,(E,"+E,"). (17)

Integration of this equation yields

- E1S:kz8 In ( E1f;XE? - Xi) = f + constant,
but at t = 0, Xi = XI0 so we can determine the
constant of integration and obtain the following equation in X, as a function of time:

The tension of the system is given by
F(t) = EldX,.


We now consider two cases:


> E2*X20.

From equations ( 19) and (20) we may write

F(t) =A+Bexp




B = E,g(E,dX,o-E~SX20)

v*o .


At the onset of stimulation the tension will

rise immediately to the value A + B and will
subsequently decay to the steady value A.





Fig. 3. Postulated changes produced in the model as a result of

stimulation. (A) Model in the unstimulated state at zero tension,
i.e. the elastic components, are at their unstretched lengths. (B)
State of the model immediately upon the onset of stimulation. (C)
Steady state of the excited muscle if E,X,O > E,X,. (D) Steady
state of the excited muscle if E,*X,
> E,tY,o.

At the cessation of stimulation the series

elastic component is at less than the unstretched length Llu and, assuming that it
exerts no compressional force, the tension in
the muscle will drop immediately to zero. The

parallel elastic component will still be extended, although its unstretched length will
have increased, but it will pull on the viscous
until both elastic components
reach their unstretched lengths. The pattern



of the tension during and after a period of

stimulation is shown in Fig. 4a.
In this case the expression

for the tension is






E18+ E,


At the onset of stimulation the tension rises

immediately to the value A-B
and then
increases to attain the final steady level A.
At the cessation of stimulation the component values will change. There will be a
sudden drop in tension to the value EIUXIU,
where X, is the initial value of X, at the
cessation of stimulation. The parallel elastic
component will have a length below that of its
unstretched length kU and, if we assume that
it exerts no compressional
force, only the
series elastic element will pull upon the
viscous part. The tension will decay exponentially to zero. The value of the time constant
will depend upon the component values V,
and E,. The pattern of the tension during
and after a period of excitation is shown in
Fig. 4B.

4.1 Tension

with experimental

and single musclejibres


in whole


of directly
stimulated single muscle fibres have been
studied by Lannergren
and Smith (1966).
Their records for fast fibres of toad skeletal
muscle are reproduced here (Fig. 5). Quite
clearly in any mechanical system, an instantaneous abrupt change in tension is not
possible and therefore could not be expected
in muscle tissue even if the biochemical
activities which bring about the tension were

Fig. 4. Theoretical records of the isometric tension in

muscle during and after a period of stimulation (indicated
by the horizontal bar beneath each record). (A) E,fY,O >
E2*Xzo. In this case the tension overshoots and then
decays to a steady level. (B) E2Xzo > E,X,O. In this
case the tension rises gradually to the steady level after
an initial immediate rise. At the cessation of excitation
the tension drops suddenly to a new value but subsequently decays exponentially to zero. In each record
arbitrary values of the constants have been chosen.

immediate in their action. Therefore

it is
that the observed changes in
tension occupy a small interval of time.
Records B, C, E, F, H and I (Fig. 5) show
fairly steep rises in tension at the onset of
stimulation and records E and H show a rapid
fall in tension at the cessation of stimulus.
The records E, F, H and I are of the type in
which E,X,O > EzSX20. Records B and C do
not follow the theoretical
model in their
behaviour during the stimulation. but Lannergren and Smith suggest that the decline in
tension is due to fatigue. The records E and
H are more rounded at the peak levels of
tension than those of records F and I but
account must be taken of the differences in
the time scales.
Similar records to those of E and F were
obtained from a whole muscle (cat tibialis)
preparation by Brown and Burns (1949).
Tension development
in slow muscle is
shown in Figs. 6 and 7. The cat soleus muscle









I set


50 mq







Fig. 5. Isometric
responses of directlystimulated single muscle fibres.A, D and G responses to
a single stimulus. B, E and H responses to stimulation at
the fusion frequencies indicated. C. F and I responses to
stimulation at 30 set-. Note the rapid rise in tension and,
in the case of records E and H. the rapid fall in tension on
cessation of stimulation.
Records reproduced
Lannergren and Smith C1966).

Fig. 6. The effect on the tension in the soleus muscle of

the anaesthetized cat of stretching while it was contracting
tetanically. The muscle was activated by stimulating a
portion of the S I ventral root at 50 set-. The muscle was
stretched 6 mm at the velocity indicated. The tension
produced by the same stretch when the muscle was not
stimulated was less than 60g. wt. Time scale expanded
during the dynamic phase of stetching. Record obtained
in collaboration with Dr. M. C. Brown and Dr. P. B. C.
Matthews and reproduced from Brown and klatthews


(Fig. 6) is held at zero tension and then stimulated isometrically. Initially there is a sudden
rise in tension and then the rise to the steady
tension is more gradual. This is therefore a
muscle in which E2sX20> E,X,O.
A situation in which the series elastic component does not seem to change its unstretched length is indicated in Fig. 7 which
shows a record for tortoise gastrocnemius
muscle. In this case there is no sudden rise
in tension at the onset of stimulation. The
record also shows the pattern of decay of
tension at the cessation of stimuiation. This
decay follows a roughly exponential course.
It would appear that differences between
fast and slow muscle produce differences in
the value of E,X,O- E,SX,o. The fast muscles
will have a larger value than the slow muscles.
This does not necessarily mean that all fast
muscles will have a positive value. It could be
negative but less negative than for the slow
muscles. For instance, the records of Bulier

Tension _


Fig. 7. The effect on the tension in the tortoise gastrocnemius muscle of stretching while it was contracting (top
record) and in the passive state (middle record). The
isolated nerve-muscle preparation was subjected to a
I mm ramp stretch (bottom record). The tension scale
also applies to the middle record. Record obtained in
collaboration with Dr. A. H. M. F. Ragab.

and Lewis (1962) show isometric tetanic

of flexor
(F.D.L.) and soleus muscle. In both cases
E,$X,- E2sX20 is negative. but for F.D.L. it
is less negative than for soleus.
Figures 6 and 7 also show the effect upon
the tension of a ramp stretch. In the case of
the cat soleus muscle it is seen that the



F (viscous) component -as indicated by the

difference in tension at the end of the dynamic
part of the ramp and the steady level during
the static part- is dependent upon the speed
at which the muscle is stretched. The oscillation on the tension record at the beginning and
end of the dynamic part of the ramp when the
muscle is stretched at 30 mm set-r is probably
due to inertial effects.
The records for the tortoise muscle (Fig. 7)
show the differences between stimulated and
passive muscle in the development of tension
during a ramp stretch. The difference between
the tension just before the start of the ramp
and the steady tension during the static part is
greater in the stimulated muscle. In other
E E,
F (elastic) = E, ; kz
is increased when the muscle is stimulated.
Such an increase is brought about if either or
both E, and E2 increase.
Likewise, it is seen that the contribution to
the tension due to the viscous component


also increases. This expression increases with

increase in Vz or E, but increase in the value
of E2 tends to reduce its value. Therefore
the increases in E, and Vz must be large
enough to outweigh the increase in E2 if, as
is seen in Fig. 7, stretch of the muscle produces
an increase in the F (viscous) term.
The time-course of the decay of tension
during the static phase of the ramp arises
from the term

contained in expression (12). If excitation of
the muscle produces a reduction of the term
(E, + E2)/V, then the tension will decay more

slowly to the steady level. In order to achieve

this, not only must V, increase but it must do
so by a sufficient amount to offset the increase
in value of (El + E2). Thus an increase in Vz
may not necessarily result in a reduction in
the (E, + Eo)/V, term. However, from visual
inspection of records A and B (Fig. 7). it does
appear that, even though (E, + E2) has been
increased upon stimulation of the muscle,
the increase in V2 is sufficient to produce a
slower return to the steady level of tension.
4.2 The behaviour of the muscle spindle
during fusimotor stimulation
A model which has properties similar to
those of the mammalian spindle has been set
up (Crowe, 1968). In particular, stimulation
of the spindle by fusimotor fibres and by
mechanical stretch produces effects that are
accountable by way of changes in the viscoelastic properties of the intrafusal fibres, but
this model could not account for the following
(a) A previously inactive spindle would fire
when its fusimotor fibres were stimulated.
(b) Crowe and Matthews (1964a) noticed
that in general the effects of stimulation of
static fusimotor fibres started and stopped
more abruptly than those of stimulation of
dynamic fusimotor fibres, thus suggesting
that the speeds of contraction of the intrafusal muscle fibre supplied by the two kinds of
fusimotor fibre are different. The static fusimotor fibres generally caused the discharge
of the ending to rise more abruptly at the
beginning of repetitive stimulation and fall
more abruptly with cessation. Sometimes on
beginning to stimulate a static fusimotor
fibre with the muscle at constant length the
discharge of the primary ending overshot its
later steady value (Fig. 8A). This effect was
not seen on stimulating dynamic fusimotor
fibres. Instead, the final steady level was
reached after a gradual rise (Fig. 8B).
The earlier model of the spindle can be
modified so that the contractile parts of the
intrafusal fibre consist of the system shown in



Fig. 1 to which the elastic region which contains the primary ending is attached in series.
In such a model, changes in unstretched
length at stimulation will cause a previously
passive spindle to start discharging. Also, the
different patterns of response, depending upon
whether a static or dynamic fusimotor fibre is
stimulated when the spindle is held at constant
length, can be explained if it is assumed that
the firing frequency is proportional to the
tension exerted by the muscle. The pattern of
firing will therefore depend upon whether
E1?sXzois greater than or less than E,X,O. As
Crowe and Matthews
(1964a) suggested,
stimulation of a static fusimotor fibre produces
a more rapid contraction than stimulation of
the dynamic fusimotor fibres. If, as has been
suggested above, stimulation of a fast fibre
produces a situation where E,SX,o > Ez8Xzo
then the calculated tension response is as
shown in Fig. 4A, and if stimulation of a slow
fibre produces a situation where E.3sX,o >
E,X,O then the calculated tension response is
as shown in Fig. 4B. If the pattern of firing is
proportional to the tension, then effects similar
to those shown in Fig. 8 will be produced.











mechanical properties of a wide variety of

types of resting muscle may be described in
terms of conceptual models which incorporate
viscous elements and series and parallel
elastic components. Such models are usually
inadequate to describe the change from rest to
the active state. Changes in the values of the
elasticity and viscosity are not sufficient to
produce a tension in a muscle which is at zero
tension prior to stimulation. Houk (1963)
introduces a force generator to replace the
parallel elastic component in his model. No
force generator is included in the present
model but a similar effect is produced by
postulating that the unstretched lengths of the
elastic components are reduced as a result of
The present model suffers from the defects
inherent in many models of muscle in the
active state. Firstly, it does not meet the
of Fenn (1924) that when a
muscle shortens it gives out more total energy
than in the isometric state. Secondly, there is
no irreversible
element in the system to
account for the discontinuity
in the forcevelocity relationship
by Aubert
(1956). In addition a study of the mechanical
properties of muscle in order to determine the
constants of elasticity and viscosity would be







Fig. 8. Records showing the discharge of the primary ending of a muscle spindle during a ramp stretch and during
stimulation at 100 set- of a static fusimotor fibre (record A) and at 90 set- of a dynamic fusimotor fibre (record B)
over the periods indicated by the horizontal bars. The records have been chosen to illustrate the patterns of firing
produced at the onset of stimulation of the two types of fusimotor fibre. Records taken from Crowe and Matthews
( 1964a).




limited because of the restrictions upon the

linearity of the specimen.
the model is a reasonable
analogue of the mechanical properties
muscle because it can reproduce at least
the tensions observed
either skeletal muscle or intrafusal rIIUS&
fibres of the spindle are subjected to isometric contraction or mechanical stretch in
the active and passive state.
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Brown. G. L. and Bums, B. D. (1949) Fatigue and
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stimulation of static and dynamic fusimotor fibres
on the response to stretching of the primary endings
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studies of static and dynamic fusimotor fibres. J.
Physiol., Lund. 174. l32- I5 I.
Fenn. W. 0. (I 924) A quantitative comparison between
the energy liberated and the work performed by the
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Grodins. F. S. (1963). Conrrol Theory and Biological
Sysrems. Columbia University Press, New York.
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reflex in human muscle systems. MS. thesis, Massachusetts Institute of Technology, Cambridge, 1963.
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Controi Theory to Pkysiofogical Syste&.
Lannergren, J. and Smith, R. S. (I 966). Types of muscle
fibres in toad skeletal muscle. Acra physiol. stand. 68,
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of fusimoto0ibre by their effects on the dynamic response of muscle spindle primary endings. Q. J1 exp.
Pkysiol. 47.324-33X
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