IEEE TRANSACTIONS ON SYSTEMS, MAN, AND CYBERNETICS, VOL. SMC-13, NO.

5, SEPTEMBER/OCTOBER 1983

1010

the time it reaches the tree's periphery at = 2, not much is left

of the high-frequency components. For example, between = 2
and 2.5 the impulse peak response is attenuated by a factor of
0.49, but between = 3.5 and 4 the attenuation is only 0.55, thus
approaching the dc value of 0.61. The conclusion, therefore, is
that the dc analysis is approximately applicable to the impulse
response. The dc analysis showed that a single input suffers a
two-to-one loss of voltage at each bifurcation, as it propagates to
the right, in addition to the normal cable attenuation. This rule
has been applied to a single PSP peripheral input, as shown in
Fig. 1. Starting with a peak amplitude of 100 mV, the signal
arrives at the soma with a peak amplitude of 7.5/16, or 0.4625
mV. It is also assumed, since shunt capacitance has only a
secondary effect, that the leading and trailing edges of the ERP,
for a single peripheral input, are the same as for 16 simultaneous
inputs.
How many nodes must be simultaneously active at a particular
level, in the absence of other inputs, to trigger the neuron? The
values for a single input yield the following answers. At the
= 3.5 level, a single action-potential input is sufficient. At
the = 3 level, four nodes exist; two of them must be simulta
neously stimulated to trigger the neuron. At the = 2.5 level
eight nodes exist; five simultaneously active nodes are required.
At the periphery, at = 2, all 16 terminals must be simulta
neously excited. As a logic element, if the neuron has 10 000
inputs, it is mainly an OR input device, but one should remember
the very important role of inhibitory junctions on or near the
soma.
REFERENCES
[1]
[2]
[3]
[4]

[5]
[6]

W. Rail, "Theoretical significance of dendritic trees for neuronal inputoutput relations" in Neural Theory and Modeling, R. F. Reiss, Ed. Stan
ford Ca: Stanford Univ. Press, 1964, pp. 73-97.
A. Pellionisz and R. Llinas, "A computer model of cerebellar Purkinje
cells," Neurosci., vol. 2, pp. 37-48, 1977.
E. W. Pottala, T. R. Colburn, and D. R. Humphrey, "A dendritic com
partment model neuron," IEEE Trans. Biomed. Eng., vol BME-20, pp.
132-139, Mar. 1973.
H. D. Patton, "Spinal reflexes and synaptic transmission," in Neurophysi
ology, T. C. Ruch et al., Eds. Philadelphia, PA: Saunders, 1965, pp.
153-180.
A. M. Gordon and J. W. Woodbury, "Action potential: properties of
excitable membranes (appendix)," in Neurophysiology, T. C. Ruch et al.,
Eds. Philadelphia, PA: Saunders, 1965, pp. 58-72.
G. A. Campbell and R. M. Foster, "Fourier integrals for practical applica
tions," Monograph B-584, Bell Telephone Syst., 1942, Eq. 819.

I.

The van der Pol equation and FitzHugh-Nagumo equations

are two systems of differential equations with important applica
bility to problems of oscillations in biology. The van der Pol
equation [28] is one of the simplest known limit-cycle oscillators
and is discussed in most differential equations texts.
The FitzHugh-Nagumo equations (sometimes called the
Bonhoffer-van der Pol equations) are a generalization of the van
der Pol equations that are used to model the behavior of excitable
media. They were introduced by FitzHugh [4] as a simplification
of the Hodgkin-Huxley equations of electrical activity in squid
axon [12].
Since these systems of equations are models of electrical phe
nomena, it is natural to build an analog device. In the past [21],
[27] the van der Pol equation was described as modeling a
vacuum tube device, but vacuum tubes are no longer commonly
used or understood items. More recently, tunnel diodes have been
used in analog circuits [13], [6], [22], but tunnel diodes are also
obsolete as well as hard to work with and expensive [14].
The goal of this correspondence is to describe an analog of an
excitable medium that is reliable, simple to use, inexpensive to
build, and makes use of integrated circuits. Numerous investiga
tors [6]-[8], [10], [19], [22], [26], [29] have used analog devices, to
model neuronal electrical activity such as those described by the
Hodgkin-Huxley equations. The advantages of the circuit that
we present here are as follows.
1) The circuit is inexpensive and easy to build and operate.
2) It is an "exact" analog of a well-known model equation that
retains physiological significance.
3) The circuit can be modeled using Kirchoff circuit laws.
This circuit was built with two goals in mind. We wanted a
device to use with students for demonstration and teaching
purposes. We also hoped to have a device that was sufficiently
sophisticated to be useful as a research tool to investigate the
behavior of excitable media. With this analog we feel that we
have realized both of these goals.
In the sections that follow, we first motivate the circuit analog
that we use (Section II). In Sections III and IV we show how
operational amplifiers can be used to build a nonlinear current
device with an "N-shaped" / - V characteristic and to simulate an
inductor. In Section V we give a brief analysis of the resulting
circuit equations to motivate the choice of specific parameter
values and briefly discuss some of the ways this device can be
used to study more complicated problems. Our presentation
assumes no previous knowledge of operational amplifiers (opamps) in the hope that nonexperts will be able to build and
understand this circuit.
II.

Analog Circuitry for the van der Pol and

FitzHugh-Nagumo Equations
JAMES P. KEENER

INTRODUCTION

THE FITZHUGH-NAGUMO

EQUATIONS

The FitzHugh-Nagumo equations are an idealization of the

Hodgkin-Huxley equations of electrical activity in an excitable
membrane. An excitable membrane is a semipermeable mem
brane whose permeability to certain ions is functionally related to
the voltage potential across the membrane.
The total current / across the membrane is the sum of
capacitive currents and ionic currents / ,
0

AbstractAn analog circuit for the FitzHugh-Nagumo equations is

given that uses readily available integrated circuitry. The mathematical
model for this circuit is derived, and simple analysis is given, to show how
the circuit works. Specifications for a reliable and easily built analog
neuron are given with components that cost only a few dollars. The circuit
is useful as a research and educational device.

ion

where is the transmembrane potential, and C is the resting

membrane capacitance. The ionic currents / consist of currents
of sodium and potassium ions and other less important currents.
The sodium current / is a "fast" current and is modeled as
being instantaneously related to the transmembrane potential
i o n

N a

Manuscript received August 12, 1982; revised April 1, 1983.

The author is with the Department of Mathematics, University of Utah, Salt
Lake City, Utah 84112.

OO18-9472/83/09OO-1010$01.00 1983 IEEE

'Na=/(0

(2)

IEEE TRANSACTIONS ON SYSTEMS, MAN, AND CYBERNETICS, VOL. SMC-13, NO. 5, SEPTEMBER/OCTOBER

1983

1011

out

Fig. 3. Schematic diagram of operational amplifier.

III.

OPERATIONAL AMPLIFIERS: THE FAST SODIUM

CURRENT

Fig. 1. Fast sodium current.

From Fig. 2 it is apparent how to build an analog circuit for

(4), at least in principle. The main difficulty lies in constructing a
suitable sodium current device. Previous devices that used vacuum
tubes or tunnel diodes are now obsolete. In this section we show
how to use operational amplifiers, a popular integrated circuit
chip that has been used in numerous amplifier applications [14].
The schematic diagram for an op-amp is shown in Fig. 3. There
are five leads, two of which are not shown in most circuit
diagrams since their necessity is assumed to be obvious. These
two, labeled V and V_ supply power to operate the op-amp.
One attractive feature of op-amps is that one can use nearly any
type of power supply, from inexpensive penlight batteries to
expensive well-regulated power supplies, in a wide range of
voltage levels.
All op-amps use three pins for their main operations. These are
labeled i> , , v and are called the output, invert input, and
noninvert inputs, respectively. Op-maps are designed to perform
one basic function, which is to give a reliable output voltage that
depends solely on the difference of the input voltages,
+

out

= g(v
Fig. 2. Equivalent circuit for (4).

(6)

where g is a step function between two voltage levels V and

V . The voltage levels V and V are close, but not equal to,
the supply voltages V+ and K_, respectively. An ideal op-amp
draws no current (infinite input impedance), provides as much
current as necessary to maintain the requisite output voltage
(zero output impedance), and responds instantaneously to changes
in v - Vi.
In reality, of course, there is a small amount of current drawn
through v and v only finite currents can flow through i; ,
response is not instantaneous, and the response curve is not a
perfect step function. However, for most purposes, one can
model op-amps as ideal; the deviation from ideal is generally too
small to notice and is well within the standard tolerances of
electronic devices.
To get a better idea of how op-amps are used we suppose that
there is a small internal capacitance and resistance so that the
output voltage satisfies
R+

where f(v) is some "]V-shaped" nonlinear function such as de

picted in Fig. 1. The potassium current i is assumed to satisfy
K

Ri

' dt

(3)

where v is the resting potassium potential in the membrane. All

other ionic currents are neglected. Combining (1), (2), and (3), we
have the well-known FitzHugh-Nagumo equations
0

L-jj = + v 0

RI,

(4)

Although this is but a crude approximation to the HodgkinHuxley model, it is a very useful simplification that retains many
of its important features. One further advantage of (4) is that
there is an obvious circuit analog shown in Fig. 2, consisting of a
resistor, capacitor, inductor, and a nonlinear device with an
A/-shaped current-voltage characteristic.
The exact form of the current-voltage characteristic f(v) does
not seem to be very important. Some people [4] have suggested
that f(v) be a cubic polynomial. Others [18], [20] have suggested
that/(t;) be piecewise linear. We will take / to be piecewise linear
since one can actually solve the piecewise linear system, and, as
we shall see, it is easy to build an electronic device with a
piecewise linear / - V characteristic.
The van der Pol equation results from (4) by setting R = 0 and
ehminating /. We find
+

(5)

which is the van der Pol equation when / is a cubic polynomial.

Apparently, this equation does not have an exact electrical analog
since R can never be exactly zero.

R+

l9

out

dv
dt
m

= g(v

V )-O
x

(7)

where g is the step function

> 0
v = 0.

(8)

v<0
The parameter c ~ is called the slew rate and is typically on the
order of 10 V / s . In most cases c is sufficiently small so that v
can be viewed as responding instantaneously to changes in g.
The main application of an op-amp is with negative feedback.
For example, the circuit in Fig. 4 has negative feedback, and
from Kirkhoff s laws, must satisfy
1

out

dun,

dt

^ R ^ T

V
2

^ )

(9)

1012

IEEE TRANSACTIONS ON SYSTEMS, MAN, AND CYBERNETICS, VOL. SMC-13, NO. 5, SEPTEMBER/OCTOBER 1983

Vout

Fig. 4.

Basic amplifier circuit.

v,

I I I W V
Hz
1,

Fig. 7.

Circuit diagram for an actual inductor-capacitor circuit.

Fig. 5.

Nonlinear current device.

Fig. 8.
Fig. 6.

It follows that

Simulated inductor circuit.

/ - V characteristic for nonlinear current device.

o u t

The motivation for our simulated inductor is that a parallel

capacitor-inductor circuit is more accurately modeled by includ
ing series and parallel resistances R and R as shown in Fig. 7. If
one end of this circuit has a fixed voltage then it can be
simulated by using an op-amp as shown in Fig. 8. To see that this
is true, we write Kirkhoffs law for the i current in Fig. 7 as

equilibrates rapidly to the function

R VR

dh
L-r
+ Ri
dt
r

s5 2

V*-

In fig. 8, the op-amp device holds v

out

"2 " " o u t

R

v -h(v )
R
2

-fM

(11)

sketched in Fig. 6. This I- V characteristic is the desired piecewise

linear response curve, suggested earlier, that we use to simulate
the fast sodium current. To within the standard tolerances of
normal electronic components, this response is a true piecewise
linear function.

(13)

R,

(10)
In the region * < ; < K*, the device is a linear amplifier.
This amplifier circuit can easily be made into a nonlinear
current device by connecting terminals v and v with a resistor,
depicted in Fig. 5. It follows from Kirkhoffs laws that the
current equilibrates rapidly to

= v so that i satisfies

oul

v-

(12)

v.

(The amplifier in Fig. 4 with R = 0, R = oo is called a voltage

follower and maintains v = v within the operating range of the
op-amp.) Since
x

out

(14)

dt

we have that
CR,R

di
~dt

(15)

which is the same equation as (13) when L = CR R .

Equation
(14) for is the same in both circuits since (ideally) the op-amp
draws no current from i .
We can now assemble our full circuit; the circuit diagram is
shown in Fig. 9. It is not hard, using Kirkhoffs laws and the
properties of ideal op-amps, to find the circuit equations.
s

IV.

OPERATIONAL AMPLIFIERS; INDUCTORS AND THE

POTASSIUM CURRENT

Inductors are somewhat difficult to construct, at least with

predictable values of inductance, and for large values of induc
tance they require large cores and can be dangerous. In this
section we show how to use an op-amp to simulate an inductor
with the added feature that large values of L are easily obtained.
In fact, our simulated inductor is more accurately modeled by the
linear law = L di/dt than standard iron-core inductors.

CRR^
2

+ Ri

3 2

v-v

i (l-R /R )
2

R*

(16)

IEEE TRANSACTIONS ON SYSTEMS, MAN, AND CYBERNETICS, VOL. SMC-13, NO. 5, SEPTEMBER/OCTOBER 1983

1013

/i=o

'c-L
rVW

v=o\

Fig. 10. Phase portrait for system (19).

Fig. 9. Circuit diagram for analog of (4).

By introducing the dimensionless variables (we take V = R

V =

V R*

/ =

'

CR
2

c =

V)
R

R )C
A

R>

0_

s = R + R*
d

(17)
T =

l n

R )i -v ),

(, +

((/? -

in Fig. 10. With 0 < s < we either have a stable rest point or a
stable limit cycle, depending on the value of F . In terms of
actual resistor values, the requirement 0 < s < is equivalent to
R>

R.

(20)

The remaining parameter choices determine the period and

shape of the limit cycle. If c <c 1 the oscillation is of relaxation
type while for c - 1 the oscillation is nearly sinusoidal. The
period of oscillation can be found exactly since the equations are
piecewise linear. However, in the range c <c 1, the period can be
accurately estimated using singular perturbation methods. Fol
lowing standard arguments [2], we find the nondimensional period

, [( ~ K )( + 1) + s(fi + 1)][( + V )(s + 1) + 3( + 1)]

0

l ( ~ Vo)(* + 1) " *( + ! ) ] [ ( * + V )(s + 1) - *(/* + 1)] '

(21)

l C }

we arrive at the system of equations

provided V is in the range |K | < ( - s)/(l + s). In the sym

metric case V = 0, which is as close to a van der Pol oscillator as
we can come, we find
0

d I

= - I - V

dV

(18)

G(V)

where

v,

-G(V)-{

5+1

sV,
-1 -

V,

1
s + 1
1
s + 1

+ 1

(19)

T =

0 + 1

fi(s + l) +*(
- s

To actually construct this system one must choose values to use

for all the resistors, capacitors and power supplies. In this section
we show how one might choose such values and give the values
that we use.
First, note that the power supplies V for all op-amps are
chosen so that K_= V+. Second, the power supply voltage
levels for the inductor circuit must be larger than for the sodium
current device, since the TV-shaped I-V characteristic requires
that the op-amp reach its saturation level V at a voltage at
which the inductor is below its own saturation. In our circuit, we
use 12 V for the sodium current and 15 V for the potassium
current.
We learn how to choose the remaining parameters by an
analysis of (18). The phase plane portrait of this system is shown

+ *(c).

! = 2.4:,

= 100:

= 1:,

/* = 10:

C = 0.01 j*F,

C - 0.5

PARAMETER SELECTION

+ 1)

(22)

Using (22) we can pick parameter values to get a wide range of

periods of oscillation.
The specific components that we have found practical are three
LM741 op-amps (National Semiconductor)

The equations in (18) are a nondimensional version of the system

of equations in (4).
V.

ln

50 kti potentiometer.

(23)

All of these components are readily available at electronics

supply stores for a few dollars. With the parameters listed in (23),
the predicted period is
T~ 5.035 X 1 0 " s .
The measured period in our circuit is
3

- 5.1 X 1 0 " s .
Such agreement (1.4 percent error) is much better than should be
expected, given the usual five to ten percent tolerances of stan
dard electronic components.
Many authors [1], [5], [17], [18] have studied the sinusoidally
forced van der Pol equation, and others have studied systems of
coupled van der Pol equations [6], [7], [9], [15], [19]. There is also
much interest in a transmission line [3], [11], [21]-[25] of active
elements. All of these systems are easily constructed using our
3

IEEE TRANSACTIONS ON SYSTEMS, MAN, AND CYBERNETICS, VOL. SMC-13, NO. 5, SEPTEMBER/OCTOBER 1983

1014

REFERENCES
[I]

M. L. Cartwright and J. E. Littlewood, "On nonlinear differential equa

tions of the second order: Part I, The equation > ' - A : ( l - > ' ) j > + > ' =
b\kcos(\t
+ a), k large," J. London Math. Soc, vol. 20, pp. 180-189,
1945.
J. D. Cole, Perturbation Methods in Applied Mathematics. Waltham, MA:
Blaisdell, 1968.
J. A. Feroe, "Existence and stability of multiple impulse solutions of a
nerve equation," SIAMJ. Appl. Math., vol. 42, pp. 235-246, 1982.
R. FitzHugh, "Impulses and physiological states in models of nerve
membrane," Biophys. J., vol. 1, pp. 445-466, 1961.
J. Flaherty and F. C. Hoppensteadt, "Frequency entrainment of a forced
van der Pol oscillator " Stud. Appl. Math., vol. 58, pp. 5-15, 1978.
J. P. Gollub, T. O. Brunner, and B. G. Danley, "Periodicity and chaos in
coupled nonlinear oscillators," Sci., vol. 200, pp. 48-50, 1978.
J. P. Gollub, E. J. Romer, and J. E. Socolar, "Trajectory divergence for
coupled relaxation oscillators: measurements and models,"/. Stat. Phvs.,
vol. 23, pp. 321-333, 1980.
R. P. Grant, "The mechanism of A- V arrhythmias with an electronic
analogue of the human A-V node," Am. J. Med., vol. 20, pp. 334-344,
1956.
J. Grasmann and M. J. W. Jansen, "Mutually synchronized relaxation
oscillators as prototypes of oscillatory systems in biology," J. Math.
BioL, vol. 7, pp. 171-197, 1979.
L. D. Harmon, "Studies with artificial Neuron, Part I: Properties and
functions of an artificial neuron," Kypernetik, vol. 1, pp. 89-101, 1963.
S. P. Hastings, "Single and multiple pulse waves for the
FitzHugh-Nagumo equations," SIAM J. Appl. Math., vol. 42, pp.
247-260, 1982.
A. L. Hodgkin and A. F. Huxley, "A qualitative description of mem
brane current and its application to conduction and excitation in nerve,"
J. Physics, vol. 177, pp. 500-544, 1952.
F. C. Hoppensteadt, "Electrical models of neurons," Lect. Appl. Math.,
vol. 19, pp. 327-344, 1981.
P. Horowitz and W. Hill, The Art of Electronics. Cambridge, MA:
Cambridge Press, 1980.
C. R. Katholi, F. Urthaler, J. Macy Jr., and . N. James, "A mathemati
cal model of automaticity in the sinus node and AV junction based on
weakly coupled relaxation oscillators," Comp. Biomed. Res., vol. 10, pp.
529-543, 1977.
J. P. Keener, "Chaotic cardiac dynamics," Lect. Appl. Math., vol. 19, pp.
299-325, 1981.
M. Levi, "Qualitative analysis of the periodically forced relaxation oscil
lators," Mem. Am. Math. Soc, vol. 32, 1981.
N. Levinson, "A second order differential equation with singular solu
tions," Ann. Math., vol. 50, pp. 127-153, 1949.
D. A. Linkens, S. J. Rimmer, and S. P. Datardina, "Spectral analysis of
coupled nonlinear oscillators under modulation conditions with reference
to intestinal modellings," Comp. BioL Med., vol. 8, pp. 125-137, 1978.
H. P. McKean, "Nagumo's equation," Adv. Math., vol. 4, pp. 209-223,
1970.
N. Minorsky, Nonlinear Oscillations. Princeton, NJ: Van Nostrand,
1962.
J. Nagumo, S. Arimoto, and S. Yoshizawa, "An active pulse transmission
line simulating nerve axon," Proc IRE, vol. 50, pp. 2061-2070, 1964.
R. H. Rand and P. J. Holmes, "Bifurcation of periodic motions in two
weakly coupled van der Pol oscillators," Int. J. Nonlinear Mech., vol. 15,
pp. 387-399, 1980.
J. Rinzel and J. B. Keller, "Travelling wave solutions of a nerve conduc
tion equation," Biophys. J., vol. 13, pp. 1313-1337, 1973.
A. C. Scott, Neurophysics. New York: Wiley, 1977.
D. A. Sideris and S. P. Moulopoulos, "Mechanism of atrioventricular
conduction: Study on an analogue,"/. Electrocardiol., vol. 10, pp. 51-58,
1977.
J. J. Stoker, Nonlinear Vibrations. New York: Interscience, 1950.
B. van der Pol and J. van der Mark, "The heartbeat considered as a
relaxation oscillation, and an electrical model of the heart," Phil. Mag.,
vol. 6, pp. 763-775, 1928.
D. L. Ypey, W. P. M. Von Meerwijk, E. Ince, and G. Groos, "Mutual
entrainment of two pacemaker cells; a study with an electronic parallel
conductance model," / . Theor. BioL, vol. 86, pp. 731-755, 1980.
2

[2]
[3]
[4]
[5]
[6]
Fig. 11.

Voltage and current traces from self-oscillatory circuit.

[7]

[8]

[9]
[10]
[II]
[12]

Fig. 12.

Voltage response of excitable circuit (first trace) to slowly oscillating

input voltage (second trace).

[13]
[14]
[15]

[16]
[17]
[18]
[19]

[20]
[21]
Fig. 13.

Voltage response of excitable circuit (first trace) to more rapidly

oscillating input voltage (second trace).

[22]
[23]

circuit as the basic building block, and a wide variety of response

patterns are readily observed.
In Figs. 11-13 we show typical oscilloscope output from our
circuit. In Fig. 11 the voltage and potassium current are shown as
a function of time when the circuit is self-oscillatory. In Figs. 12
and 13 are shown the voltage response of an excitable neuron
(not self-oscillatory) to sinusoidal forcing. In Fig. 12 the forcing
is low frequency and we see a 3 : 1 bursting pattern. In Fig. 13,
the forcing is at a higher frequency and the response pattern is
4 : 5 (Wenkebach pattern). There are numerous other interesting
response patterns, including apparently chaotic patterns, that are
readily observed with this circuit.
The study of larger coupled systems is still in progress and will
be reported later. However, it is already quite apparent that with
this analog circuit we are able to perform experiments and search
parameter space for interesting phenomena much more quickly
than the corresponding analysis or numerical computations can
be done. We believe that this device will prove valuable in the
study of one- and two-dimensional excitable media.
ACKNOWLEDGMENT

The author gratefully acknowledges the hard work of Jeff

McGough in helping with the development of this device.

[24]
[25]
[26]
[27]
[28]
[29]

The Neural Path Probabilistic Delay Model

CAROL A. NIZNIK, SENIOR MEMBER, IEEE
AbstractThe neural path probabilistic delay (NPPD) algorithm models
the neural network in a discrete time manner analogous to the computer
network. The four stages of the basic neuron cell component, i.e., neuron
Manuscript received August 12, 1982; revised April 4, 1983.
The author is with the Department of Electrical Engineering, University of
Pittsburgh, Pittsburgh, PA 15261; her present address is 36 Panorama Trail,
Rochester, NY 14625.

0018-9472/83/0900-1014$01.00 1983 IEEE