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A comparison of two boundary conditions used with the bidomain

model of cardiac tissue

Article  in  Annals of Biomedical Engineering · February 1991

DOI: 10.1007/BF02368075 · Source: PubMed

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Annals of BiomeclicalEngineering, Vol. 19, pp. 669-678, 1991 0090-6964/91 $3.00 + .00
Printed in the USA. All rights reserved. 1991 PergamonPress pie

A Comparison of Two Boundary Conditions Used

with the Bidomain Model of Cardiac Tissue

Bradley J. Roth
Biomedical Engineering and Instrumentation Program
Building 13, Room 3W13
National Institutes of Health
Bethesda, MD
(Received 12/7/89; Revised 4/15/90)

In the bidomain model, two alternative sets o f boundary conditions at the inter-
face between cardiac tissue and a saline bath have been used. It is shown that these
boundary conditions are equivalent i f the length constant o f the tissue in the direc-
tion transverse to the fibers is much larger than the radius o f the individual cardiac
cells. I f this is not the case, the relative merits o f the two boundary conditions are
closely related to the question o f the applicability o f a continuum model, such as the
bidomain model, to describe a discrete multicellular tissue.

Keywords--Bidomain model, Cardiac tissue, Boundary conditions.

INTRODUCTION

The electrical properties o f cardiac muscle are complicated because o f the coupling
o f cells through intercellular junctions, the effect o f the interstitial space between cells,
and anisotropy. Yet, experimental evidence indicates that these factors are important
for understanding action potential propagation in cardiac tissue (1,8,17,19). It would
be useful to have a mathematical t h e o r y that explains these data. One such theory,
the b i d o m a i n model, has been applied successfully to cardiac muscle (4,6,7,11,13).
It is a c o n t i n u u m model, m e a n i n g that it describes the m a c r o s c o p i c electrical prop-
erties o f cardiac tissue averaged over m a n y cells. The continuum approach is attractive
because otherwise each cell would have to be treated individually, making calculations
o f electrical behavior numerically intractable. O f course, a c o n t i n u u m model is not
valid unless the replacement o f the microscopic cellular structure by macroscopic elec-
trical properties is p e r f o r m e d correctly.
Although there is general agreement on how to relate m a n y o f the macroscopic pa-
rameters in the bidomain model to the microscopic structure, there remains some con-

Acknowledgment--The suggestions and comments from Dr. Peter Basser are greatly appreciated.
Address correspondence to Dr. Bradley J. Roth, Biomedical Engineering and Instrumentation Program,
Building 13, Room 3W13, National Institutes of Health, Bethesda, MD 20892.
669
670 B.J. Roth

troversy over the correct macroscopic boundary conditions at the interface between
cardiac tissue and a saline bath. Two sets of boundary conditions have been proposed
(9,10,20). Until this controversy is resolved, there remains some uncertainty in how
to properly apply the bidomain model to cardiac tissue.
In this paper, the question of boundary conditions in the bidomain model is reex-
amined. An elementary calculation is performed for steady-state, one-dimensional
current flow through a slab of cardiac tissue lying in a saline bath. This example is
chosen because of its simplicity; it yields an analytic solution for the potential and
clearly illustrates the physical behavior. The results are used to compare the bound-
ary conditions proposed by Tung (20) to those proposed by Peskoff (9) and Plonsey
(10). When the length scale of the potential variations is large compared to the radius
o f a single cell, the two sets of boundary conditions are equivalent. The boundary
conditions introduced by Roth and Wikswo (16) for the case when the transmembrane
potential is given are also discussed.

METHODS

Consider a slab of cardiac tissue of thickness h, bathed on both sides by saline of

conductivity ~r and centered between two large flat electrodes connected to a cur-
rent source, so that the electrodes pass a current density J (Fig. 1). If the area of each
electrode is large compared to their separation, then current flows only in the direc-
tion perpendicular to the electrodes, the z-direction, and the problem is one-dimen-
sional. This assumption simplifies the bidomain equations, so that they can be solved
analytically. In this case the bidomain model resembles the one-dimensional cable
model studied by Weidmann (21), except that he considered current flow in the di-
rection parallel to the individual cardiac cells, whereas here the current flows perpen-
dicular to the cells.

I Z
I
- electrode

Jl '
I saline

z = h/2

I z =- h/2
I saline
I

+ electrode

FIGURE 1. A slab of cardiac tissue of thickness h, bathed in a saline bath between two flat, paral-
lel electrodes passing a current density J. The z-axis is perpendicular to the tissue surface and the
fiber direction is parallel to the surface.
Bidomain Boundary Conditions 671

In a passive bidomain the intracellular potential, 4~t, and interstitial potential, ~bo,
are governed by two coupled partial differential equations (10). For steady currents
in one dimension, these equations reduce to

02r 3 (~i--~o) (1)

Oiz OZ2 R---m
h h
--- <Z< -- 9
2 2
02 4~o 3
- (q~i - 0o) (2)
a~ OZ2 Rm

The parameters aiz and Ooz are the intracellular and interstitial conductivities in the
z-direction (transverse to the cells), and/3 is the ratio of the membrane surface area
to tissue volume. All three quantities are macroscopic parameters derived by averag-
ing over a volume containing many cells (13). R m is the membrane resistance times
unit area.
The potentials t~i and ~bo can be replaced by t~m and xI,:

t~m = ~i -- t~o (3)

XI't = ~ i + ~oz ~o (4)

w h e r e t~m is the transmembrane potential. The physical interpretation of xI, is dis-

cussed by Roth (13). When the bidomain equations (Eqs. 1 and 2) are written in terms
o f Om and xI,, they uncouple, yielding

02~m 1
OZ 2 -- ~k2 t~m
(5)

and h <Z< h
--
2 2
02XIt
- 0 (6)
az 2

where k is the length constant of the tissue transverse to the fiber direction

=
Rmoizaoz (7)
( tIiz + tYoz)

The potential in the saline bath, q~e, obeys Laplace's equation

0:~e _ 0 IZl > h

0Z 2 , ~ . (8)

If the origin of the z-axis is at the center of the slab, then symmetry requires that the
potentials are odd functions of z. The solutions for ~m, xI', and Oe are thus
672 B.J. Roth

~bm=Asinh(~) , -- h < z < -h (9)

2 2

h h
qI=Bz , 2 <z< 2 (10)

and

Cz+D z> h
' 2
(11)
G= h
Cz-D , z< -~

The constants A, B, C, and D remain to be determined; one depends on the current

passed by the electrodes and the other three are determined by the boundary condi-
tions at the tissue-bath surface. Once ~m and xI, are known, Eqs. 3 and 4 can be in-
verted to obtain ~i and ~o; typical results are shown in Fig. 2.
Because the problem is one-dimensional, the current density passed by the elec-
trode, J, must equal the current density in the bath, --~reO~e/OZ. Using Eq. 11, this
condition determines the constant C:

J
C- (12)
(7e

Potential

- h / ~ m
~ h/2 z

D
~iz
' ~ . + Goz B
~_
2

(C 2h-+D)

FIGURE 2. The intracellular potential, ~i, interstitial potential, ~o, t r a n s m e m b r a n e potential, ~,,, and
bath potential, ~e, as functions o f z. The t w o alternative b o u n d a r y conditions compared in this paper
d e t e r m i n e if t h e ~i c u r v e has zero or n o n z e r o slope at z = +_hi2.
Bidomain Boundary Conditions 673

The other three unknowns, A, B, and D, are determined by three boundary condi-
tions at the tissue surface (z = +h/2). Two of these conditions, generally accepted
as correct, are: the bath and interstitial potentials are continuous

~e = 4~o (13)

and, in the direction perpendicular to the surface, the sum of the intracellular and in-
terstitial current densities equals the current density in the bath

aiz ~ + Ooz Oz - ae O~ (14)

The second condition follows from the continuity of current, and in this example im-
plies that

J
B - (15)
a&

The first condition is true because there is no resistive barrier between the interstitial
space and the saline bath, and it produces an equation relating the two remaining un-
knowns, A and D:

D = J ~ aiz + Ooz
) aiz + aoz
,16,

The third boundary condition, which determines A and D individually, is the sub-
ject of controversy. In his original formulation of the bidomain model, Tung (20)
claimed that the intracellular current density vanishes at the tissue surface

0(~ i
--Oiz ~ = 0 . (17)

This condition has recently been used by Henriquez and Plonsey (6,7), Colli Franzone
et al. (2), and Roth (14) in calculations of propagating action potentials in cardiac tis-
sue. In Fig. 2, this condition implies that at z = + h / 2 the slope of the (~i curve is
zero. Application of this boundary condition results in

- ,, sech( ) (18)

and

hi1 , oiz 2 tanh( )]) 19,

D = J ~ aiz + aoz aoz h
674 B.J. Roth

An alternative boundary condition, proposed by Peskoff (9) and Plonsey (10), is that
the intracellular current density at the tissue surface is equal to the membrane cur-
rent density 1
OOi ~m
-agz -- - (20)
OZ Rm

implying that

sech( )
A = (21)

and

D=jh[ 1
oozh
-aiz - "~- O~ 1 + 1 (22)
2 o~ 1 +

The two results for the constants A and D (Eqs. 18 and 19 vs. Eqs. 21 and 22) allow
the implications of the two sets of boundary conditions to be compared.

RESULTS
The two boundary conditions give identical results when

<< 1 . (23)

/
If the slab of tissue is thick, so that h / 2 >> X, then coth (h/2X) is approximately equal
to one, and the two results are equivalent if the product of the length constant and
the surface-to-volume ratio is much greater than one, k/3 >> 1. If the slab is not thick,
then coth ( h / 2 k ) is large and the restriction that k/3 >> 1 can be weakened and still
have the two boundary conditions give similar results. This is not surprising, since in
a thin slab, current redistribution into the intracellular space would be minimal.
The product X/3 measures the ratio of the cell membrane area facing the intersti-
tial space (internal membrane) in the volume where the potential gradients are signif-
icant to the membrane area facing the saline bath (surface membrane). Thus, the
condition X/3 >> 1 implies that for the two boundary conditions to be equivalent the

lPlonsey (10) left out a minus sign when he proposed this boundary condition.
Bidomain Boundary Conditions 675

area of the surface m e m b r a n e should be small, relative to the area of the internal
membrane. This conclusion is similar to the suggestion by Plonsey (10) that the intra-
cellular current at the strand surface is negligible because the ratio of the surface
m e m b r a n e to internal m e m b r a n e in a 1 m m radius cylindrical strand of cardiac tis-
sue is about 1~ However, it is not the internal membrane area in the volume of the
entire tissue, but instead the internal membrane area in the volume over which there
are large potential gradients that is important. If potential gradients are restricted to
a thin later on the surface of the strand, as predicted by Henriquez et al. (4), then the
ratio of internal to surface membrane area m a y be smaller than Plonsey (10) suggested.
If the individual cardiac cells are modeled as cylinders with radius a, packed in the
tissue with an intracellular volume fraction f , then the surface-to-volume ratio,/3, is
equal to 2 f / a (13). In cardiac ventricular muscle, the radius of a cell is approximately
10 ~m. If f = 0.7, R m = 0.91 fl m 2 (21), aiz = 0.019 S / m and aoz = 0.24 S / m (1), then
/3 = 0.14 ~m -1 and X = 340 ~m. Thus, X/3 is approximately equal to 50, which is
fairly large compared to 1. However, when the current is changing in time with a fre-
quency u much greater than the reciprocal o f the membrane time constant, the mem-
brane resistance must be replaced by the m e m b r a n e impedance, which at high
frequencies is approximately 1/27ruCm, where Cm is the m e m b r a n e capacitance per
unit area. With ~ -- 1 kHz and Cm = 0.01 F / m 2, the length constant is about 45 ~m
and the product X/3 is 6. Therefore, for dc currents the two b o u n d a r y conditions re-
sult in potentials differing by only a few percent, but for ac currents at 1 kHz the dif-
ference can be 10 to 2 0 % 2. Differences o f this magnitude have been observed in
calculations of propagating action potentials in cylindrical strands of cardiac muscle
using both boundary conditions (14).
Since 2 f is on the order of 1 for cardiac muscle, 13 is approximately equal to 1/a.
Thus, the condition for the two boundary conditions to be equivalent can be ex-
pressed as X >> a, the length constant is much greater than the cell radius. If X is not
much greater than a, which of the two sets of boundary conditions is correct? This
is a difficult question, because when the length scale of the potential gradients is not
large compared to the cell size, the validity of the bidomain model is suspect. The bi-
domain model is a continuum model, and therefore is based on the assumption that
the length scale of the potential gradients is large compared to the size of the individ-
ual cells, X >> a. Thus, the question of which boundary condition is correct is closely
connected to the question of the validity of a continuum model for a discrete tissue.
I f X/a is only 6, then errors introduced by using the bidomain model to represent a
discrete tissue m a y be as large as the differences between the two boundary condi-
tions. It seems that the only ways to access the relative merits of the two boundary
conditions when X/3 is not much greater than 1 are by experiments or a careful, de-
tailed study of the limiting procedure in replacing a discrete tissue by a continuum.
It may be that neither boundary condition is correct, but instead each may represent
a different approximation to the actual microscopic behavior.
In some applications of the bidomain model, the t r a n s m e m b r a n e potential is as-
sumed to be known and the bidomain equations are used to determine the extracel-
lular potential (4,5,11,13,15,16). Usually the transmembrane potential is assumed to

2The electrical behavior at high frequency is actually more complicatedthan described here because of
the phase shifts between membrane current and potential.
676 B.J. Roth

be constant in the direction perpendicular to the tissue surface. This assumption is

made primarily to simplify the mathematics, with little or no physical justification.
In the example presented above, the analogous assumption is that the transmembrane
potential is not a function of z. Instead, it is a constant which can be taken as zero.
This assumption is obviously not true, but holds fairly well in thick slabs ( h / 2 >> k)
except within a few length constants of the tissue surface. With t~m given, only two
functions are unknown and therefore only two boundary conditions need be speci-
fied at the tissue surface. Generally the continuity of potential and current, Eqs. 13
and 14, are used. 3 If the bidomain equations are solved for this case (A = 0 by as-
sumption), the constants B and C are the same as calculated previously, and D is

D = j h_[ 1 1 ] (24)
2 ~7e tTiz q- tToz

If the slab is thick ( h / 2 >> ~,) or the intracellular conductivity is small compared
to the interstitial conductivity (aiz << aoz), then this approximate calculation gives the
same extracellular potential as is obtained when both the extracellular and transmem-
brane potentials are calculated from the bidomain equations. This is surprising, since it
means that the extracellular potential can be calculated correctly using a poor approx-
imation to the transmembrane potential and without knowledge of the surface-to volume
ratio. In fact, ventricular muscle aiz is small relative to aoz (1), so this approximation
should have a wide range of validity. However, for tightly packed cells, such as those
found in some Purkinje fibers (18), aoz may be small compared to aiz, in which case
Eq. 24 is seriously in error.
Although the calculated extracellular potential may be reasonable, the assumption
that the transmembrane potential is independent of depth leads to incorrect results
when current density is considered. In this case the intracellular current density is
equal t o JtTiz/(tTiz -1- aoz ) everywhere within the tissue. Clearly the third boundary
condition, as proposed by Tung (20) or Peskoff (9) and Plonsey (10), is not obeyed.
Moreover, since the current is continuous at the tissue-bath boundary, the intracel-
lular current must leave the tissue to enter the bath by crossing the cell membrane at
z = +_h/2. Thus, the membrane current density is discontinuous and equal to zero ev-
erywhere except at the tissue surface, where it jumps to a large value. Thus, there is
a paradox: the membrane at the surface behaves differently than the membrane just
below the surface. This paradox, plus the fact that the third boundary condition gov-
erning the intracellular current density is not obeyed, forces the conclusion that in re-
ality a transmembrane potential, independent o f the depth into the tissue, cannot
occur (6). Under some conditions this approximation may be a useful device for de-
termining the extracellular potential, but it does not adequately describe the current
near the tissue surface, and certainly should not be used during calculations o f the
propagating transmembrane potential.

3plonsey and Barr (11) used another set of boundary conditions for calculating the extracellular po-
tential produced by a uniform plane wavefront propagating through an infinitely thick slab of tissue. Roth
(12) and Henriquez (3) have noted that Plonsey and Barr's calculation is not consistent with continuity of
current (Eq. 14).
Bidomain Boundary Conditions 677

REFERENCES

1. Clerc, L. Directional differences of impulse spread in trabecular muscle from mammalian heart. J~
Physiol. 255:335-346; 1976.
2. Colli Franzone, P.; Guerri, L.; Rovida, S. Wavefront propagation in an activation model of the an-
isotropic cardiac tissue: Asymptotic analysis and numerical simulations. J. Math. Biol. 28:121-176;
1990.
3. Henriquez, C.S. Structure and volume conduction effects on propagation in cardiac tissue. Durham,
NC: Duke University; 1988. Dissertation.
4. Henriquez, C.S.; Trayanova, N.; Plonsey, R. Potential and current distributions in a cylindrical bun-
dle of cardiac tissue. Biophys. J. 53:907-918; 1988.
5. Henriquez, C.S.; Trayanova, N.; Plonsey, R. A planar slab bidomain model for cardiac tissue. Ann.
Biomed. Eng. 18:367-376; 1990.
6. Henriquez, C.S.; Plonsey, R. Simulation of propagation along a bundle of cardiac tissue. I. Mathe-
matical formulation. IEEE Trans. Biomed. Eng. 37:850-860; 1990.
7. Henriquez, C.S. Plonsey, R. Simulation of propagation along a bundle of cardiac tissue. II. Results
of simulation. IEEE Trans. Biomed. Eng. 37:861-875; 1990.
8. Kleber, A.G.; Riegger, C.B. Electrical constants of arterially perfused rabbit papillary muscle. J. Phys-
iol. 385:307-324; 1986.
9. Peskoff, A. Electric potential in three-dimensional electrically syncytial tissues. Bull. Math. Biol.
41:163-181; 1979.
10. Plonsey, R. Bioelectric sources arising in excitable fibers. Ann. Biomed. Eng. 16:519-546; 1988.
11. Plonsey, R.; Barr, R.C. Interstitial potentials and their change with depth into cardiac tissue. Biophys.
J. 51:547-555; 1987.
12. Roth, B.J. Longitudinal resistance in strands of cardiac muscle. Nashville, TN: Vanderbilt University;
1987. Dissertation.
13. Roth, B.J. The electrical potential produced by a strand of cardiac muscle: A bidomain analysis. Ann.
Biomed. Eng. 16:609-637; 1988.
14. Roth, B.J. Action potential propagation in a thick strand of cardiac muscle. Circ. Res. 68:162-163;
1991.
15. Roth, B.J.; Guo, W.-Q.; Wikswo, J.P., Jr. The effects of spiral anisotropy on the electric potential
and the magnetic field at the apex of the heart. Math. Biosci. 88:159-189; 1988.
16. Roth, B.J.; Wikswo, J.P., Jr. A bidomain model for the extracellular potential and magnetic field of
cardiac tissue. IEEE Trans. Biomed. Eng. 33:467-469; 1986.
17. Spach, M.S.; Miller, W.T., III; Geselowitz, D.B.; Barr, R.C.; Kootsey, J.M.; Johnson, E.A. The dis-
continuous nature of propagation in normal canine cardiac muscle. Evidence for recurrent disconti-
nuities of intracellular resistance that affect the membrane currents. Circ. Res. 48:39-54; 1981.
18. Sommer, J.R. Implications of structure and geometry on cardiac electrical activity. Ann. Biomed. Eng.
11:149-157; 1983.
19. Suenson, M. Interaction between ventricular cells during the early part of excitation in the ferret heart.
Acta. Physiol. Scand. 125:81-90; 1985.
20. Tung, L. A bi-domain model for describing ischemic myocardial dc potentials. Cambridge, MA: Mas-
sachusetts Institute of Technology; 1978. Dissertation.
21. Weidmann, S. Electrical constants of trabecular muscle from mammalian heart. J. Physiol. 210:1041-
1054; 1970.

NOMENCLATURE
a = radius of cardiac cells (m)
A , D = constants determined by the boundary conditions (V)
B,C = constants determined by the boundary conditions ( V / m )
Cm = membrane capacitance per unit area ( F / m 2)
h = thickness o f tissue slab (m)
Rm = membrane resistance times unit area (tim 2)
Z = distance perpendicular to the tissue surface (m)
 678 B.J. Roth

= s u r f a c e - t o - v o l u m e ratio o f the tissue ( l / m )

p = f r e q u e n c y (Hz)
k = length c o n s t a n t in the z-direction (m)
xI, = p o t e n t i a l d e f i n e d in Eq. 4 ( V )
~be = p o t e n t i a l i n the saline b a t h ( V )
~5i = intracellular potential (V)
~bm = transmembrane potential (V)
~bo = interstitial p o t e n t i a l ( V )
ae = c o n d u c t i v i t y o f the saline b a t h ( S / m )
aiz = i n t r a c e l l u l a r c o n d u c t i v i t y in the z direction ( S / m )
Ooz = interstitial c o n d u c t i v i t y in the z direction ( S / m )

LIST OF SYMBOLS

th = phi
k = lambda
= psi
u = nu
~o = o m e g a
fl = u p p e r case o m e g a
o = sigma
7r = p i

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