Hill’s Model for Muscle Physiology and Biomechanics

Affiliation

Jakob von Morgenland

Undergraduate Interdepartmental Program for Neuroscience
University of California, Los Angeles
Los Angeles, CA, United States of America
[email protected]

Sharmila Venugopal, Ph.D.

Department of Integrative Biology and Physiology
University of California, Los Angeles
Los Angeles, CA, United States of America
[email protected]
(310) 206-0332

corresponding author(s): Sharmila Venugopal ([email protected])

Synonyms
Muscle, Hill’s model, MATLAB

Definition
Computational models of muscles serve as important tools to understand the
musculoskeletal physiology and biomechanics. Such models have been widely
implemented in a variety of simulation platforms and incorporate varying degrees of
physiological details. This article summarizes a simplified two-component biomechanical
muscle model, first described by A. V. Hill in 1938, popularly known as the “Hill’s Muscle
Model”. The Hill’s model provides thermodynamically constrained quantitative
relationships between muscle length, shortening velocity, force and heat released during
a muscle contraction. The model description, simulations and MATLAB script provided
here highlight the computational features of the Hill’s muscle model.
Detailed Description
1. Biomechanical components of muscle force generation

Muscle cells contract to produce movement. During a contraction, the shortening

of a muscle cell results in tension or force production. The basic structural components
involved in force production consist of a series elastic element and a contractile element.
The series elastic element is composed of tendons and aponeurosis. Tendons are tough
extensions of the muscles and aponeurosis are thin sheets of tissue that attach the
muscle to the bone. The contractile element is composed of sarcomeres which consist of
thin actin filaments and thick myosin filaments. The sarcomeres form subunits called
myofibrils which are long filaments bundled into muscle fibers (see Fig. 1). The myosin
heads of the thick filament form cross-bridges with the adenosine triphosphate (ATP)
binding sites on the thin actin filaments. To produce force in the muscle cell, the filaments
slide past each other when bound to ATP. More details on muscle biology, molecular
mechanisms and dynamics of force generation can be found in [1].

Figure 1 – Structural components of a muscle. Schematic illustrating the main

structural components of a muscle.

In his seminal paper (1938), A.V.Hill details his extensive experiments measuring
the length, velocity, force and the energy released during muscle contractions [2]. Based
on such physiological measures, Hill proposed a mathematical relationship between
energy, force and velocity of muscle shortening/lengthening (also see [3]). It is noted that
the details of muscle biology were unknown at that time.
2. Model Description
a) A two-component biomechanical model for force production
A highly simplified biomechanical muscle model conceived by A.V. Hill consists of
series elastic and contractile elements as shown in Fig. 2.

Figure 2 – Biomechanical components of a muscle. A schematic showing the

biomechanical equivalence of the structural components of a muscle.

The series elastic element is assumed to be a spring-like structure with length, 𝐿𝑠𝑒
and the length of the contractile element is given by 𝐿𝑐𝑒 such that, the total muscle length,
𝐿 is:
𝐿 = 𝐿𝑐𝑒 + 𝐿𝑠𝑒

During an isometric contraction, the 𝐿𝑐𝑒 gradually reduces to mimic shortening of the
contractile element. In parallel, the 𝐿𝑠𝑒 gradually increases (muscle stretch), to account
for the constant muscle length. The contraction force of 𝐿𝑐𝑒 is exactly the same as the
stretching force of 𝐿𝑠𝑒 . Such a force, 𝑃 is assumed to be proportional to the stretch in 𝐿𝑠𝑒
(Hooke’s Law) as given below (also see [4]):

𝑃 = 𝛼(𝐿𝑠𝑒 − 𝐿𝑠𝑒 (0))

where, 𝛼 is the spring contant and 𝐿𝑠𝑒 (0) is the length of the series elastic element before
the contraction. The rate of change in 𝐿 is therefore:

𝑑𝐿 𝑑𝐿𝑐𝑒 𝑑𝐿𝑠𝑒 𝑑𝐿𝑠𝑒

= + = 𝑣𝑐𝑒 +
𝑑𝑡 𝑑𝑡 𝑑𝑡 𝑑𝑡

where, 𝑣𝑐𝑒 is the shortening velocity of the contractile element. Similarly, the rate of
change of 𝑃 is given by:

𝑑𝑃 𝑑𝐿𝑠𝑒
=𝛼
𝑑𝑡 𝑑𝑡

From the above, it is noted that during length changes, the force 𝑃 responds to length
change primarily in 𝐿𝑠𝑒 . For isometric contractions, in which the total muscle length is held
constant, the contractile element subsequently readjusts to restore the 𝐿𝑠𝑒 and therefore
the force, 𝑃.

b) Heat released and force-velocity relationship

The original formulation for the force-velocity relationship given by A.V.Hill, was based
on the measurements of heat released during muscle shortening. The heat released
depends on the distance ( 𝑥 ) and velocity ( 𝑣 ) of shortening. To measure these
relationships, Hill’s experiments consisted of testing the effect of different shortening
velocities on the heat released during shortening. To achieve a consistent initial condition,
he began at the tetanic force, 𝑃0 during an isometric contraction and subsequently
measured the heat released during muscle shortening for varying loads (𝑃) (also see
Figs. 4 - 6). The heat released during muscle shortening is given as 𝑎𝑥, g.cm, where 𝑎
was experimentally determined to be a constant and has the unit of force. Next, if 𝑃 g of
load is lifted by the muscle, the work done is given as 𝑃𝑥, g.cm.

The total energy in excess of the isometric contraction is given as:

ℎ = (𝑃 + 𝑎)𝑥, in g.cm

The rate of change in energy is therefore written as:

𝑑ℎ 𝑑𝑥
= (𝑃 + 𝑎) = (𝑃 + 𝑎)𝑣
𝑑𝑡 𝑑𝑡

Experimentally, Hill found that this rate of change of energy release increased linearly as
the load, 𝑃 diminished such that, it was zero when 𝑃 = 𝑃0 . This relationship is known as
the famous Hill equation and relates the rate of heat released during muscle shortening
to the corresponding load/force, as given below:

(𝑃 + 𝑎)𝑣 = 𝑏(𝑃 − 𝑃0 )

where, 𝑏 is the slope of the above linear relationship. The constant 𝑏 is defined as the
absolute rate of energy liberation.

3. Model Simulations
Figure 3 illustrates a flow diagram of the computational steps of the two-component
biomechanical muscle model. The changes in muscle length (𝐿) is translated into force
(𝑃) and heat production (𝐻). The model reproduces known physiological relationships
between these quantities. The description here is restricted to isometric conditions where,
the muscle length is held constant to generate a corresponding steady-state force.

Figure 3 – A flow chart of the computational steps of Hill model. The model input is
the assumed muscle length (L) and outputs include lengths of the series elastic and
contractile elements, velocity, force and heat released. The ovals indicate computational
steps.
a) Force-Length Relationship

Figure 4 illustrates the force generation during an isometric contraction. In this

simulation experiment, the initial length 𝐿𝑠𝑒 is set 30% of the total length 𝐿 at rest, such
that the 𝐿𝑐𝑒 is at 70% of 𝐿; note that the force is zero. To mimic muscle shortening during
an isometric contraction, the value of 𝐿𝑐𝑒 is reduced to 60% of 𝐿. Note that this change in
length is not instantaneous but has an initial transitory phase as 𝐿𝑐𝑒 shortens and 𝐿𝑠𝑒
increases to ensure 𝐿 is constant. Correspondingly, the force, 𝑃 increases. After
stabilization of 𝐿𝑐𝑒 and 𝐿𝑠𝑒 , the force 𝑃 saturates at the steady-state value of the isometric
contraction. A white noise was added to the force function in these simulations to match
realistic conditions.

Figure 4 – Force-Length Relationship. In the above simulation, 𝐿𝑠𝑒 was set to 30% of
the total muscle length, 𝐿 . The simulation included motor noise in order to more
realistically model physiological force production.

b) Force-Velocity Relationship
Hill empirically demonstrated that when held at the tetanic condition during an
isometric contraction, subsequent increases in muscle load, 𝑃, decreased the shortening
velocity, 𝑣 of the muscle over a distance, 𝑥, cm. Such experiments can be simulated in
the model to reproduce this force-velocity relationship. As shown in Fig. 5, beginning at
an isometric force of 150 mN, the shortening velocity, 𝑣 mm/s was changed from a value
zero to 1 in repeated simulations to compute the resulting steady-state force. This inverse
force-velocity relationship is summarized by an exponential regression fit as shown in the
figure.

Figure 5 – Relationship between force and shortening velocity. Red circles show the
steady-state force for different values for shortening velocity in individual simulations. The
blue line shows a regression fit highlighting an inverse force-velocity relationship.

c) Length-Heat Relationship
Hill demonstrated that the heat released during muscle shortening is independent
of the shortening velocity. This critical aspect on the thermodynamics of isometric
contraction is illustrated by the simulations in Fig. 6. The muscle model was released
from an isometric tetanus at 2 s, and was subject to different shortening velocities as
shown in Fig. 6A. The corresponding heat liberated as shown in Fig. 6B depends only
on the shortening distance, 𝑥 (here, 𝑥 = 0.5 mm) and not on the shortening velocity.
Specifically the total amount of heat released due to muscle shortening was the same
across all of the simulations, despite varying shortening velocities. These results
demonstrate that the shortening distance 𝑥 is a crucial determinant of the energy released
by the muscle. When held in completely isometric conditions, the energy released is zero
because there is no change in distance.
Figure 6 – Force-Velocity and Length-Heat Relationships. A. The muscle was held in
isometric tetanus for 2 seconds, after which it was subject to different shortening
velocities. From right to left, the shortening velocities shown are 1 mm/s, 0.50 mm/s, 0.33
mm/s, 0.25 mm/s, 0.20 mm/s, and 0.17 mm/s. After undergoing a period of shortening,
all of the simulations ended at the same final length, which was ½ of the original length
of the muscle at isometric tetanus. B. The heat released by the muscle for the different
shortening velocities in A are plotted (heat responses are color matched with traces in
A). Over shorter periods of shortening, the rate of energy released is higher or reaches
the maximal level more quickly; for this simulation, the end length was the same and note
that the energy released at the end of shortening is the same across all trials.

Conclusion
Computational models of muscles help explain the principles of muscle physiology
and force generation. The Hill model described here offers insights into the relationships
between muscle length, force, velocity, and heat released based on the classic
experiments by A. V. Hill (1938). The model is useful to begin understanding the
quantitative aspects of muscle physiology and biomechanics.
Cross-References
Tsianos GA, Loeb GE (2013), Muscle Physiology and Modeling. In: Nature Springer
Encyclopedia of Computational Neuroscience.

References
1. Enoka, R.M. and K.G. Pearson, The motor unit and muscle action, in Principles of
Neural Science, E.R. Kandel, et al., Editors. 2013, McGraw-Hill Companies: U.S.A. p.
768-788.
2. Hill, A.V. The heat of shortening and the dynamic constants of muscle. in Proceedings of
the Royal Society of London. 1938.
3. Holmes, J.W., Teaching from classic papers: Hill's model of muscle contraction. Adv
Physiol Educ, 2006. 30(2): p. 67-72.
4. Loiselle, D.S., et al., Energetic consequences of mechanical loads. Prog Biophys Mol
Biol, 2008. 97(2-3): p. 348-66.

Further Reading
Nature-Springer Encyclopedia of Neuroscience
Appendix
Model Implementation using MATLAB
%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%
%%%%% Hill Muscle Model %%%%%
%%%%% Jakob von Morgenland %%%%%
%%%%% The Hill Muscle Model and its Implementation (JVM and SV) %%%%%
%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%%

Preparing inputs for the Hill function

t=0:0.001:5;
% time from 0 to 5 seconds with 0.001 time step
L=ones(length(t),1);
% initializing length of muscle to 1
L2=ones(length(t),1);
m=[-1,-0.5,-1/3,-0.25,-0.2,-1/6]
% theoretical slopes for linear velocity equations
yint=[3,2,1.66,1.5,1.4,1.32]
% calculated y-intercepts for linear velocity equations
vel=[1,0.5,1/3,0.25,0.2,1/6,0]
% theoretical velocity values derived from slope calculations
% not used in rest of simulation, included for reference for force-velocity graph
force=[7.437,34.51,52.68,65.71,75.52,83.16,144.9]
% calculated force values derived from simulations using theoretical velocity values

Input-Output relationship for Hill Model

[P,H,Lse,Lce] = hill(L,t);

% Inputs = muscle length (L) and time (t)

% Outputs = force (P), heat (H), and the individual element lengths (Lce and Lse)

For loop to determine force-velocity relationship

for j = 1:length(m)
for i = 1:length(t)-1
if t(i)<2
L2(i)=1;
else
if t(i)>= 2
L2(i)=yint(j)+m(j)*t(i);
end
end
if L2(i) < 0.5
L2(i)=0.5;
i=length(t);
end
 end
[P2,H2,Lse2,Lce2] = hill(L2,t);
Pss(j)=P2(length(t)-1);
end

Hill function

function [P,H,Lse,Lce] = hill(L,t)

Model parameters

a = (380*.098); % shortening and heat excess proportionality constant

b = 0.325; % excess energy and steady-state force proportionality constant
P0 = a/0.257; % initial force in isometric contraction
alpha = P0/0.1; % spring constant for series elastic element
Lse0 = 0.3; % initial length of the series elastic element
k = a/25; % heat production constant

Initialize arrays for outputs

Lse = zeros(length(t),1);
Lce = zeros(length(t),1);
Lse(1,:) = Lse0;
Lce(1,:) = 1-Lse0;
H = zeros(length(t),1);
P = zeros(length(t),1);

Solver for length input into Hill model

for j = 2:(length(t))
dt = (t(j)-t(j-1));
dL = (L(j)-L(j-1));
dP = alpha*((dL/dt)+b*((P0-P(j-1))/(a+P(j-1))))*dt;
P(j) = P(j-1)+dP;
H(j) = H(j-1)+(k+a*b*((P0-P(j-1))/(a+P(j-1))))*dt;
Lse(j) = Lse0+P(j-1)/alpha;
Lce(j) = L(j)-Lse(j);
end

Creates noise for more realistic output

for i = 1: length(H)
H(i) = H(i)+(k/10)*randn(1);
P(i) = P(i)+(P0/100)*randn(1);
end
end