science journal.pdf

Neuro Quantology is an international, interdisciplinary, open-access, peer-reviewed journal that publishes original research and review articles on the interface between quantum physics and neuroscience. The journal focuses on the exploration of the neural mechanisms underlying consciousness, cognition, perception, and behavior from a quantum perspective. Neuro Quantology is published monthly

NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
50
Original article1
Controlling Synchronization of Modified
FitzHugh-Nagumo Neurons Under External
Electrical Stimulation
Deepak Mishra, Abhishek Yadav, Sudipta Ray and Prem K. Kalra
Abstract
We report control of synchronization between pair of coupled neurons under
external electrical stimulation. A nonlinear controlling mechanism is proposed for
keeping the coupled system in synchronized state. We studied transitions between
synchrony and asynchrony because of variation in coupling strength. We discuss the
dynamical analysis for the Modified FitzHugh-Nagumo neuron model in detail. This
work focuses the application of control system theory for understanding possible
synchronization phenomena in a pair of biological neuron models.
Key Words: modified FitzHugh-Nagumo, nonlinear controller, synchronization,
coupled neurons
NeuroQuantology 2006; 1: 50-67
Introduction
Determining the dynamical behavior of an ensemble of coupled neurons is an important
problem in computational neuroscience. Commonly used models for the study of individual
neuron which display spiking behavior include (a) Integrate-and-Fire neuron model and its
variants (b) FitzHugh-Nagumo model (c) Hodgkin-Huxley model and (d) Morris-Lecar model
(Gerstner, 2002; FitzHugh, 1969; Nagumo, 1962; Hodgkin, 1952; Koch, 1999; Abbott, 2001).
From the very beginning of the research in the field of computational neuroscience, people
deal with single neuron and its behavior. Present trends of research include investigation of
Corresponding authors: Department of Electrical Engineering, Indian Institute of Technology Kanpur, India,
e-mail: dkmishra@iitk.ac.in, ayadav.iitk@gmail.com, sray@iiita.ac.in, kalra@iitk.ac.in
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
51
the behavior of neurons considered in a network and their way to fire synchronously. It is
assumed that the activities in the brain are synchronous and underlying interests for
synchronization of nonlinear oscillators in physical and biological systems range from novel
communication strategies to understand how large and small neural assemblies efficiently
and sensitively achieve desired functional goal (Pinto, 2000).
The dynamics of many neural ensembles such as central pattern generators or
thalamo-cortical circuits poses questions related to the cooperative behavior of neurons.
Each neuron independently may show irregular behavior while ensembles of different
neurons can synchronize in order to process biological information or produce regular,
rhythmic activity (Elson, 1999). How do the dissimilar neurons synchronize? How do they
inhibit noise and intrinsic fluctuations? What are the parameters responsible for such
synchronization and regularization? Answers to these and similar questions may be found
through simulations and experiments that enable one to follow qualitatively the cooperative
dynamics of neurons as intrinsic synaptic parameters are varied (Elson, 1999). However,
these problems did not receive many opportunities for extensive study. Many cells are
linked together by specialized inter-cellular pathways known as gap junction. There are two
types of possible couplings among neurons namely weak coupling and strong coupling,
defined on the basis of the magnitude of coupling strength. In my paper (Mishra, 2004), the
effect of coupling strength on dynamics of coupled neurons is studied.
In recent years, there has been tremendous interest for the study of the
synchronization of chaotic systems. The synchronous and asynchronous behavior of
neurons is one of the important research topics (Jiang, 2004; Thompson, 1999). Application
of nonlinear active controller for maintaining synchronism among neurons is one of the
issues addressed in (Ucar, 2004). The phenomenon of synchronism gives rise to different
dynamical behaviors such as chaotic synchronization etc. In (Mishra, 2004; Mishra, 2005),
nonlinear dynamical analysis on single and coupled modified FitzHugh-Nagumo model under
steady current stimulation is carried out. Also the effect of parameter variation on its
behavior is investigated.
In many papers (Pinto, 2000; Ucar, 2004; Rinzel, 1987; Elson, 1999) dynamical
analysis on various neuron models is carried out under steady current input. The variations
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
52
in the external stimulus may bring the system to unstable state from a stable one. However,
biological rhythms, such as, cardiac and circadian rhythms arise from activity of multiple
oscillators with dispersed intrinsic frequencies (Chang, 2000). Variety of complex dynamical
behavior including phase locked limit cycles, quasi-periodicity, intermittency and chaos are
observed in literature (Thompson, 1999) for sinusoidal external fields. Chang et.al. (Chang,
2000), investigated the stability of the output rhythm of these sympathetic oscillators for a
periodic driving force.
In this paper, a nonlinear controller has been designed to synchronize a coupled
modified FitzHugh-Nagumo model. Dynamical characteristics of modified FitzHugh-Nagumo
neuron model under external stimulation are discussed first. With the variation of the
stimulation and the initial condition, the complex behavior is revealed. The response of a
model of two neurons coupled with a gap junction is investigated and the significance of
coupling coefficient is studied next. We propose a nonlinear active controller for the
synchronization of a pair of coupled neurons. Numerical results in support of our findings
are also presented. At last, we conclude our work.
Dynamics of Modified FitzHugh-Nagumo Neuron Model
The modified FitzHugh-Nagumo equations are a set of three coupled differential equations
which exhibit the qualitative behavior observed in neurons, viz quiescence, excitability and
periodicity (Rinzel, 1987). The system can be represented as
)
cos(
)
/
(
)
(
,
)
(
)
(
)
(
3
/
.
.
3
.
t
A
t
F
Where
dy
c
x
y
bw
a
x
w
t
F
y
w
x
x
x
Ω
Ω
=
−
+
−
=
−
+
=
+
+
−
−
=
ε
φ
(1)
The function F(t) represents the external stimulus. The variable x represents the
potential difference between the dendritic spine head and its surrounding medium, w is
recovery variable and y represents the slowly moving current in the dendrite. In this
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
53
model, x and w together make up a fast subsystem relative to y . The Jacobian at
equilibrium point (x*, w*, y*) is found to be










−
−
−
−
−
=
d
b
x
J
ε
ε
φ
φ
0
0
1
1
1 2
(2)
If at a neighborhood of a particular value µ0 of the parameter µ, there exists a
pair of eigenvalues of J(µ) of the form α(µ) ± iβ(µ) such that α(µ) = 0, β(µ) ≠ 0, then
no other eigenvalue of J(µ0) will be an integral multiple of iβ(µ0). Thus J(µ0) has a pair
of pure imaginary eigenvalues. This helps in understanding the dynamics of the model at
the equilibrium point.
Dynamics of Single Uncoupled Modified FitzHugh-Nagumo Neuron Model
The dynamical set of equations of a single uncoupled modified FitzHugh-Nagumo system is
given in equations (1). The system parameters used for simulations are a = 0.7, b = 0.8, c =
-0.775, φ = 0.08, ε = 0.0001 and d = 1.0. The calculated equilibrium point for the system at
F(t) = 0 is: (x*, w*, y*) = (-1.0292, -0.4115, 0.2542). Eigenvalues at these points are: (λ1,
λ2, λ3) = (-0.0002, -0.061+j0.283, -0.061+j0.283).
We found that the set of equations are asymptotically stable around the
equilibrium points at F(t) = 0. The variations in the external stimulus bring the system to
unstable state (periodic oscillation). We analyze the response of the model by subjecting it
under the following electrical stimulation
)
cos(
)
/
(
)
( t
A
t
F Ω
Ω
= (3)
Here, A represents the magnitude of the stimulus and Ω refers to the frequency
of given stimulus. The stimulus frequency is varied while keeping the magnitude at a fixed
value of A = 0.71, since at this particular value of A, modified FitzHugh-Nagumo neuron
model gives periodic spiking. Simulation results at different stimulus frequencies are shown
in Figure 1 and Figure 2. Time response for the neuron at Ω = 0.07 is shown in Figure 1(a)
and phase portrait is drawn in Figure 1(b). Similar responses for Ω = 0.127 are shown in
Figure 2. It is observed that with the variation in stimulus frequency, the neuron shows
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
54
complex chaotic behavior. Hence the stimulus frequency can be considered as a significant
parameter that affects the behavior of neuron.
Fig.1 Time responses and phase portrait for modified FitzHugh-Nagumo model at stimulus frequency Ω =
0.07 (a) Time response (b) phase portrait.
Fig.2 Time responses and phase portrait for modified FitzHugh-Nagumo model at stimulus frequency Ω =
0.07 (a) Time response (b) phase portrait.
Bifurcation analysis with Ω as the parameter
We have investigated behavioral change in the dynamics of modified FitzHugh-Nagumo
model with respect to Ω by plotting leading Lyapunov exponents, and bifurcation diagram in
Figure 3. It is observed that modified FitzHugh-Nagumo model exhibits stable, periodic and
chaotic behavior for different value of Ω. Thus the frequency of injected stimulus plays
important role and its variation alters the dynamics of model. The Lyapunov exponent is
positive for Ω = 0.127.
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
55
Fig.3 Plots of Leading Lyapunov exponent and bifurcation diagram with Ω as bifurcation parameter. (a) Leading
Lyapunov exponent; (b) Bifurcation diagram.
Dynamics of Coupled Modified FitzHugh-Nagumo Neuron Model
We studied the characteristics of an uncoupled modified FitzHugh-Nagumo neuron in the
previous section. In this section, we extend our analysis for coupled neuron models. A
system of two coupled neurons can be expressed as:
j
i
j
i
X
c
X
f
dt
dX
j
i
i
≠
=
+
=
2
,
1
,
)
(
arctan
)
(
(4)
where Xij ∈ Rn (xi or xj) represents state variable of the two oscillating neurons,
function f: Rn →Rn defines the dynamics of a single neuron in the absence of coupling,
and c is the coupling matrix. Complete synchronization occurs when the coupled chaotic
oscillators asymptotically exhibit identical behaviors, i.e., when || X1(t)-X2(t)|| →0 as t →∞,
for any initial condition. The synchronization is dependent on the coupling matrix c. The
dynamical equations for the coupled modified FitzHugh-Nagumo neuron model are given in
equations (5).
The two systems are coupled with different coupling parameters, say gc and g’c,
with rest of the parameter values kept identical.
(a) (b)
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
56
)
(
,
)
(
)
2
cos(
)
2
/
(
)
arctan(
'
)
(
3
/
)
(
),
(
)
2
cos(
)
2
/
(
)
arctan(
)
(
3
/
2
2
.
2
2
2
.
2
1
2
2
3
2
2
.
2
1
1
.
1
1
1
.
1
2
1
1
3
1
1
.
1
dy
c
x
y
bw
a
x
w
t
A
x
g
t
F
y
w
x
x
x
dy
c
x
y
bw
a
x
w
t
A
x
g
t
F
y
w
x
x
x
c
c
−
+
−
=
−
+
=
Ω
Ω
+
+
+
+
−
−
=
−
+
−
=
−
+
=
Ω
Ω
+
+
+
+
−
−
=
ε
φ
π
π
ε
φ
π
π
(5)
We have carried out the analysis in the presence of external electrical stimulus of
magnitude A = 0.7 and frequency Ω = 0.127, the values for which the model exhibits
complex chaotic response.
The results for strongly coupled neuron models are shown in Figure 4. The
coupling strengths are: gc = 0.9 and g’c = 0.9. The coupled modified FitzHugh-Nagumo
neurons are synchronous, but the response is chaotic. Time courses for the variables x1 and
x2 are shown in Figure 4(a). The synchronism among the neurons is evident from the plot
between x1 and x2, which is almost a straight line as shown in Figure 4(b).
We analyze a loosely coupled neural system, where the values for coupling
coefficient are kept as gc = 0.009 and g’c = 0.009. The responses of coupled neurons are
asynchronous. The firing of one neuron is out of phase with the other neuron. The time
courses for x1 and x2, when system is loosely coupled, are shown in Figure 5(a). Figure 5(b)
shows the plot between x1 and x2.
The coupling among neurons can be weak and strong, so we have taken effect of
unequal (Weak-Strong) coupling. This is done by keeping one of the neuron in strongly
coupled state and other in weakly coupled state i.e. by keeping gc = 0.9 and g’c = 0.009,.
The response with these values of coupling strengths is shown in Figure 6. The time courses
for variables x1 and x2 are plotted in Figure 6(a). The responses of the variable x1 and x2 are
not in complete synchronism but they are trying to achieve a synchronous state. The same
can be observed from phase portrait of x1 and x2 drawn in Figure 6(b). In this case, neurons
try to maintain synchronization, but they are not in exact synchronism. In order to bring
this coupled system in synchronism, we need an active controller. In the next section, a
control mechanism is explained which keeps the coupled neurons in exact synchronism by
applying a control input to one of the pairs of neurons.
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
57
Fig.4 Response of coupled modified FitzHugh-Nagumo neuron models (equations 5) with coupling strengths
gc= 0.9 and g’c= 0.9. (a) The time courses for variables x1 and x2 (b) Phase portrait of the components of
oscillations.
Fig.5 Response of coupled modified FitzHugh-Nagumo neuron models (equations 5) with coupling strengths gc
= 0.9 and g’c = 0.009. (a) The time courses for variables x1 and x2 (b) Phase portrait of the components of
oscillations.
The findings in the analysis of coupling strength effects support the hebbian
hypothesis. According to Donald Hebb, if input from neuron A often contributes to the
firing of neuron B, then the synapse from A to B should be strengthened (Dyan, 2001). Thus
it can be stated that the coupling between the pair of neuron is one of the important
parameter to be studied for exploring the intricacies of the coupled system.
Nonlinear Active Controller for a Pair of Coupled Modified FitzHugh-Nagumo System
It is found in previous section that because of unequal coupling strength we observe
asynchrony among pair of neurons. In this section, we propose a control mechanism which
can bring the two systems into exact synchronism. The schematic diagram for two coupled
neurons is shown in Figure 7. The method is based on the Lyapunov stability theory.
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
58
Fig.6 Response for coupled modified FitzHugh-Nagumo neuron model (equations 5) with coupling strengths gc
= 0.009 and g’c = 0.009. (a) The time courses for variable x1 and x2 (b) Phase portrait of the components of
oscillations.
Fig. 7 Schematic diagram of two coupled neurons controlled by an active controller.
Responses for Uncontrolled Pair of Neurons
To begin with, we show the results for two uncontrolled coupled pairs of neurons whose
dynamical equations can be given by the following set of equations.
)
(
,
)
(
)
2
cos(
)
2
/
(
)
arctan(
'
)
(
3
/
)
(
),
(
)
2
cos(
)
2
/
(
)
arctan(
)
(
3
/
2
2
.
2
2
2
.
2
1
2
2
3
2
2
.
2
1
1
.
1
1
1
.
1
2
1
1
3
1
1
.
1
dy
c
x
y
bw
a
x
w
t
A
x
g
t
F
y
w
x
x
x
dy
c
x
y
bw
a
x
w
t
A
x
g
t
F
y
w
x
x
x
c
c
−
+
−
=
−
+
=
Ω
Ω
+
+
+
+
−
−
=
−
+
−
=
−
+
=
Ω
Ω
+
+
+
+
−
−
=
ε
φ
π
π
ε
φ
π
π
(6)
)
(
),
(
)
2
cos(
)
2
/
(
)
arctan(
'
)
(
3
/
)
(
),
(
)
2
cos(
)
2
/
(
)
arctan(
)
(
3
/
4
4
.
4
4
4
.
4
3
4
4
3
4
4
.
4
3
3
.
3
3
3
.
3
4
3
3
3
3
3
.
3
dy
c
x
y
bw
a
x
w
t
A
x
n
t
F
y
w
x
x
x
dy
c
x
y
bw
a
x
w
t
A
x
n
t
F
y
w
x
x
x
c
c
−
+
−
=
−
+
=
Ω
Ω
+
+
+
+
−
−
=
−
+
−
=
−
+
=
Ω
Ω
+
+
+
+
−
−
=
ε
φ
π
π
ε
φ
π
π
(7)
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
59
The parameters used for the uncontrolled coupled pair of neurons are same as used for
earlier analysis. The only changes are in the values of coupling coefficients. The coefficient
values used are: gc = g’c = 0.6 and nc = n’c = 0.02. Simulation results for this model are
drawn in Figure 8. The time evolutions of the variables x1 and x3 are shown in Figure 8(a).
The corresponding phase portrait between x1 and x3 is plotted in Figure 8(b). Error curves
for uncontrolled system are plotted in Figure 9. It is evident from these figures that the pairs
of neurons are in asynchronous state.
Fig.8 Responses of pair of coupled neurons (equations 6 and 7) used in the absence of nonlinear active
controller at different coupling strengths gc = 0.6 and nc= 0.02. (a) Time courses for variables x1 and x3 (b)
Phase portrait of the components of oscillations
(b)
(a)
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
60
Responses for controlled pair of neurons
In order to bring the synchronism among these neurons we proposed a control law. The
equations given in (7) are replaced by the set of coupled system given by equations (8),
which incorporates the control input. Thus,
Fig. 9 The error curves for the variables in modified FitzHugh-Nagumo system (equations 6 and 7) at coupling
strengths gc = 0.6 and g’c = 0.02. (a) Error signals e1, e2 and e3 (b) Error signals e4, e5 and e6.
(a)
(b)
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
61
)
(
)
(
),
(
)
(
)
(
)
2
cos(
)
2
/
(
)
arctan(
)
(
3
/
3
3
.
3
3
3
.
3
4
3
3
3
3
3
.
3
t
dy
c
x
y
t
bw
a
x
w
t
t
A
x
n
t
F
y
w
x
x
x
c
b
a
c
µ
ε
µ
φ
µ
π
π
+
−
+
−
=
+
−
+
=
+
Ω
Ω
+
+
+
+
−
−
=
)
(
)
(
),
(
)
(
)
(
)
2
cos(
)
2
/
(
)
arctan(
'
)
(
3
/
4
4
.
4
4
4
.
4
3
4
4
3
4
4
.
4
t
dy
c
x
y
t
bw
a
x
w
t
t
A
x
n
t
F
y
w
x
x
x
f
e
d
c
µ
ε
µ
φ
µ
π
π
+
−
+
−
=
+
−
+
=
+
Ω
Ω
+
+
+
+
−
−
=
(8)
Errors between the variables are calculated as
2
4
6
2
4
5
2
4
4
1
3
3
1
3
2
1
3
1
,
,
,
,
y
y
e
w
w
e
x
x
e
y
y
e
w
w
e
x
x
e
−
=
−
=
−
=
−
=
−
=
−
=
(9)
Ideally, the rate of change of error must be zero in order to achieve exact synchronism.
Derivative of the error signals are given by
2
.
4
.
6
.
2
.
4
.
5
.
2
.
4
.
4
.
1
.
3
3
.
1
.
3
.
2
.
1
.
.
3
1
.
,
,
,
,
y
y
e
w
w
e
x
x
e
y
y
e
w
w
e
x
x
e
−
=
−
=
−
=
−
=
−
=
−
=
⋅
(10)
The calculated error signal for the system is given by following equations
f
e
d
c
c
c
b
a
c
c
de
e
e
be
e
e
x
g
x
n
x
x
e
e
e
e
de
e
e
be
e
e
x
g
x
n
x
x
e
e
e
e
µ
ε
µ
φ
µ
µ
ε
µ
φ
µ
+
−
−
=
+
−
=
+
−
+
+
−
+
−
=
+
−
−
=
+
−
=
+
−
+
+
−
+
−
=
)
(
,
)
(
)
arctan(
'
)
arctan(
'
3
/
3
/
)
(
,
)
(
)
arctan(
)
arctan(
3
/
3
/
6
4
6
.
5
4
5
.
1
3
3
2
3
4
6
5
4
4
.
2
1
3
.
3
1
.
2
2
4
3
1
3
3
2
3
1
.
1
(11)
We proposed the control law for µa, µb, µc, µd and µf in equations (12). They are
expressed as in equation (12).
1
1
2
4
3
1
3
3
3
2
1
,
)
arctan(
)
arctan(
3
/
3
/
de
be
x
g
x
n
x
x
e
e
Ke
c
b
c
c
a
ε
µ
φ
µ
µ
=
−
=
+
−
−
+
−
+
−
=
6
5
1
3
3
2
3
4
6
5
4
1
,
)
arctan(
'
)
arctan(
'
3
/
3
/
de
be
x
g
x
n
x
x
e
e
e
K
f
e
c
c
d
ε
µ
φ
µ
µ
=
−
=
+
−
−
+
−
+
−
=
(12)
The systems given in (6) and (8) will approach synchronization for any initial conditions by
the control law given by (12). We construct the Lyapunov function
)
)(
2
/
1
( 2
6
2
5
2
4
2
3
2
2
2
1 e
e
e
e
e
e
V +
+
+
+
+
= (13)
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
62
The differential of the Lyapunov function along the trajectory of system (11) is
6
.
6
5
.
5
4
.
4
3
.
3
2
.
2
1
.
1 e
e
e
e
e
e
e
e
e
e
e
e
V +
+
+
+
+
= (14)
Substituting above into (14) results in
0
)
( 2
6
2
5
2
4
2
3
2
2
2
1
.
<
−
−
−
−
−
−
= e
e
e
e
e
e
V (15)
which gives asymptotic stability of the system by Lyapunov stability theory. This means that
the coupled systems (6) and (8) are synchronized for any initial conditions.
Results of the controlled pair of coupled modified FitzHugh-Nagumo neurons are
shown in Figure 10. The time evolutions of variables x1 and x3 are shown in Figure 10(a).
Phase portrait for variables x1 and x3 is plotted in Figure 10(b). It is evident that the set of
coupled neurons is now in exact synchronism. The control signal profile is shown in Figure
11. This shows the time evolution of controller activity. The error profile drawn for the
system is shown in Figure 12. The system is operated without any controller till t=250 msec
and it is switched to controlling mode after this time instant. It is observed from the error
profile that, as soon as the controller comes into action, system achieves complete
synchronism.
The description of a nonlinear controller for maintaining synchronism is given. We
compared the results with a nonlinear coupled neuron model in the absence of controlling
mechanism. It is found that the application of active controller for maintaining synchronism
in nonlinear systems is very effective and can be used in real life applications.
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
63
Fig. 10 Responses of pair of coupled neurons (equations 6 and 8) with nonlinear active controller. The
responses are generated at different coupling strengths i.e. gc = 0.6 and nc = .02. (a) Time courses for variables
x1 and x3 (b) Phase portrait of the components of oscillations.
(a)
(b)
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
64
Fig. 11 Responses of pair of coupled neuron used with nonlinear active controller at different coupling
strengths gc = 0.6 and nc = 0.02. (a) Control signals (equations 11) µa, µb and µc (b) Control signals (equations
11) µd, µe and µf for keeping the system in synchronism.
(b)
(a)
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
65
Fig. 12 Responses for pair of coupled neuron used with nonlinear active controller at different coupling
strengths gc = 0.6 and nc = 0.02. (a) Error signals (equations 9) e1, e2 and e3 (b) Error signals (equations 9) e4,
e5 and e6.
(b)
(a)
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
66
Conclusion
In this paper, the characteristics of three dimensional modified FitzHugh-Nagumo neuron
model is studied. Dynamical behavior of the modified FitzHugh-Nagumo system under
external electrical stimulation is presented and it is verified that the introduction of periodic
stimulation modifies the dynamics of biological system by presenting the dynamical behavior
for the modified FitzHugh-Nagumo system under external electrical stimulation. The
responses of the system for different stimulus frequencies are shown. The synchronization
of two coupled neurons subjected to external electrical stimulation is studied. The behavior
of coupled neurons with the variation in coupling strength is also studied. A nonlinear active
controller description is provided at the end. It is shown that this controller can maintain
the synchronous behavior among strongly-weakly coupled neurons. The methodology for
determining control law is presented. We compared these results with the response of a
nonlinear coupled neuron model in the absence of controlling mechanism. It is found that
the application of active controller for maintaining synchronism in nonlinear system is very
effective and can be used in real life applications.
NeuroQuantology 2006|Issue 1|Page 50-67
Mishra et al. FitzHugh-Nagumo Neurons
ISSN 1303 5150 www.neuroquantology.com
67
References
Gerstner W and Kistler WM. Spiking Neuron Models, Single Neurons, Populations, Plasticity, Cambridge
University Press. 2002.
Pinto RD, Varona P, Volkovskii AR et al. Synchronous behavior of two coupled electronic neurons. Physical
Review E 2000;62:2644-2655.
Ucar A, Lonngren KE, Bai WE. Synchronous of the Coupled FitzHugh-Nagumo System. Chaos, Solitons and
Fractals 2004;20:1085-1090.
Mishra D, Yadav A, Ray S, Kalra PK. Nonlinear Dynamical Analysis on Coupled Modified FitzHugh-Nagumo
Neuron Model. ISNN 2005, LNCS 3496, 2005;95-101.
Mishra D, Yadav A, Ray S, Kalra PK. Bifurcation analysis in modified Fitzhugh Nagumo neuronal model. NCCDS
2005.
Jiang W, Bin D, Tsang KM. Chaotic synchronization of neurons coupled with gap junction under external
electrical stimulation. Chaos, Solitons and Fractals 2004; 22:469-476.
Thompson CJ, Bardos DC, Yang YS, Joyner KH. Nonlinear cable models for cells exposed to electric fields I.
General Theory and Space-clamped Solutions. Chaos, Solitons and Fractlas 1999;10(11):1825-1842.
Hodgkin A and Huxley A. A quantitative description of membrane current and its application to conduction and
excitation in nerve. Journal of Physiology, London, 1952;117:500-544.
Nagumo J, Arimoto S and Yosizawa S. An active pulse transmission line simulating nerve axon. Proc IRE, 1962;50.
FitzHugh R. Mathematical models for excitation and propagation in nerve. Biological Engineering 1969.
Koch C. Biophysics of computation. Oxford University Press, 1999.
Dyan P and Abbott LF. Theoretical neuroscience: computational and mathematical modeling of neural systems.
The MIT Press, Massachusetts. 2001.
Elson RC, Selverston A, Huerta R, Rulkov NF, Rabinovich M, Abarbanel HDI. Synchronous behavior of two
coupled biological neurons. Physical Review Letters 1999; 81: 5692-5695.
Rinzel J. A formal classification of bursting mechanisms in excitable systems, in mathematical topics in population
biology, morphogenesis and neuroscience. Lecture notes in Biomathematics. Springer-Verlag, New York,
1987; 71: 267-281.
Chang HS, Staras K, Gilbey MP. Multiple Oscillators Provide Metastability in Rhythm Generation. The Journal of
Neuroscience 2000; 20(13): 5135-5143.

Recomendados

Analyzing the Factors and Issues Related to Empowerment of Women using Bi-Dir... por
Analyzing the Factors and Issues Related to Empowerment of Women using Bi-Dir...Analyzing the Factors and Issues Related to Empowerment of Women using Bi-Dir...
Analyzing the Factors and Issues Related to Empowerment of Women using Bi-Dir...ijcnes
5 visualizações3 slides
neural pacemaker por
neural pacemakerneural pacemaker
neural pacemakerSteven Yoon
170 visualizações8 slides
Modeling Stochasticity and Gap Junction Dynamics: Integrate and Fire Model por
Modeling Stochasticity and Gap Junction Dynamics: Integrate and Fire ModelModeling Stochasticity and Gap Junction Dynamics: Integrate and Fire Model
Modeling Stochasticity and Gap Junction Dynamics: Integrate and Fire Modeldharmakarma
1K visualizações17 slides
Essay About Beh 225 Brain Response Of Behavior por
Essay About Beh 225 Brain Response Of BehaviorEssay About Beh 225 Brain Response Of Behavior
Essay About Beh 225 Brain Response Of BehaviorMegan Espinoza
2 visualizações82 slides
Thesis por
ThesisThesis
ThesisJean Fecteau
166 visualizações40 slides
Computational neuropharmacology drug designing por
Computational neuropharmacology drug designingComputational neuropharmacology drug designing
Computational neuropharmacology drug designingRevathi Boyina
147 visualizações38 slides

Mais conteúdo relacionado

Similar a science journal.pdf

fazowemetodybadaniamozguver10en.pdf por
fazowemetodybadaniamozguver10en.pdffazowemetodybadaniamozguver10en.pdf
fazowemetodybadaniamozguver10en.pdfJerzyAchimowicz2
2 visualizações20 slides
Tognoli & Kelso, Society for Neuroscience 2009, diversity of 10Hz rhythms in ... por
Tognoli & Kelso, Society for Neuroscience 2009, diversity of 10Hz rhythms in ...Tognoli & Kelso, Society for Neuroscience 2009, diversity of 10Hz rhythms in ...
Tognoli & Kelso, Society for Neuroscience 2009, diversity of 10Hz rhythms in ...EmmanuelleTognoli
59 visualizações22 slides
Edgardo Arroyo CV por
Edgardo Arroyo CVEdgardo Arroyo CV
Edgardo Arroyo CVEdgardo J. Arroyo
145 visualizações5 slides
nature17435 por
nature17435nature17435
nature17435davidjgiles
342 visualizações13 slides
An Efficient Implementation Of A Realistic Spiking Neuron Model On An FPGA por
An Efficient Implementation Of A Realistic Spiking Neuron Model On An FPGAAn Efficient Implementation Of A Realistic Spiking Neuron Model On An FPGA
An Efficient Implementation Of A Realistic Spiking Neuron Model On An FPGARobin Beregovska
3 visualizações6 slides
INHIBITION AND SET-SHIFTING TASKS IN CENTRAL EXECUTIVE FUNCTION OF WORKING ME... por
INHIBITION AND SET-SHIFTING TASKS IN CENTRAL EXECUTIVE FUNCTION OF WORKING ME...INHIBITION AND SET-SHIFTING TASKS IN CENTRAL EXECUTIVE FUNCTION OF WORKING ME...
INHIBITION AND SET-SHIFTING TASKS IN CENTRAL EXECUTIVE FUNCTION OF WORKING ME...sipij
634 visualizações10 slides

Similar a science journal.pdf(20)

fazowemetodybadaniamozguver10en.pdf por JerzyAchimowicz2
fazowemetodybadaniamozguver10en.pdffazowemetodybadaniamozguver10en.pdf
fazowemetodybadaniamozguver10en.pdf
JerzyAchimowicz22 visualizações
Tognoli & Kelso, Society for Neuroscience 2009, diversity of 10Hz rhythms in ... por EmmanuelleTognoli
Tognoli & Kelso, Society for Neuroscience 2009, diversity of 10Hz rhythms in ...Tognoli & Kelso, Society for Neuroscience 2009, diversity of 10Hz rhythms in ...
Tognoli & Kelso, Society for Neuroscience 2009, diversity of 10Hz rhythms in ...
EmmanuelleTognoli59 visualizações
Edgardo Arroyo CV por Edgardo J. Arroyo
Edgardo Arroyo CVEdgardo Arroyo CV
Edgardo Arroyo CV
Edgardo J. Arroyo145 visualizações
nature17435 por davidjgiles
nature17435nature17435
nature17435
davidjgiles342 visualizações
An Efficient Implementation Of A Realistic Spiking Neuron Model On An FPGA por Robin Beregovska
An Efficient Implementation Of A Realistic Spiking Neuron Model On An FPGAAn Efficient Implementation Of A Realistic Spiking Neuron Model On An FPGA
An Efficient Implementation Of A Realistic Spiking Neuron Model On An FPGA
Robin Beregovska3 visualizações
INHIBITION AND SET-SHIFTING TASKS IN CENTRAL EXECUTIVE FUNCTION OF WORKING ME... por sipij
INHIBITION AND SET-SHIFTING TASKS IN CENTRAL EXECUTIVE FUNCTION OF WORKING ME...INHIBITION AND SET-SHIFTING TASKS IN CENTRAL EXECUTIVE FUNCTION OF WORKING ME...
INHIBITION AND SET-SHIFTING TASKS IN CENTRAL EXECUTIVE FUNCTION OF WORKING ME...
sipij634 visualizações
Eeg time series data analysis in focal cerebral ischemic rat model por ijbesjournal
Eeg time series data analysis in focal cerebral ischemic rat modelEeg time series data analysis in focal cerebral ischemic rat model
Eeg time series data analysis in focal cerebral ischemic rat model
ijbesjournal183 visualizações
Eeg seminar por DrRAVIKANTKUMAR
Eeg seminarEeg seminar
Eeg seminar
DrRAVIKANTKUMAR500 visualizações
Neuromuscular Junction Formation por Qilong Wu
Neuromuscular Junction FormationNeuromuscular Junction Formation
Neuromuscular Junction Formation
Qilong Wu124 visualizações
Journalcompneuro por Khalifa Bakkar
JournalcompneuroJournalcompneuro
Journalcompneuro
Khalifa Bakkar306 visualizações
A Novel Approach to Study the Effects of Anesthesia on Respiratory Signals by... por IJECEIAES
A Novel Approach to Study the Effects of Anesthesia on Respiratory Signals by...A Novel Approach to Study the Effects of Anesthesia on Respiratory Signals by...
A Novel Approach to Study the Effects of Anesthesia on Respiratory Signals by...
IJECEIAES6 visualizações
6. 9588 1-pb por IAESIJEECS
6. 9588 1-pb6. 9588 1-pb
6. 9588 1-pb
IAESIJEECS12 visualizações
JAISTサマースクール2016「脳を知るための理論」講義03 Network Dynamics por hirokazutanaka
JAISTサマースクール2016「脳を知るための理論」講義03 Network DynamicsJAISTサマースクール2016「脳を知るための理論」講義03 Network Dynamics
JAISTサマースクール2016「脳を知るための理論」講義03 Network Dynamics
hirokazutanaka665 visualizações
Meller et al (2012) Single Unit Firing Rates In Macaque SI (In Review) por David
Meller et al (2012)  Single Unit Firing Rates In Macaque SI (In Review)Meller et al (2012)  Single Unit Firing Rates In Macaque SI (In Review)
Meller et al (2012) Single Unit Firing Rates In Macaque SI (In Review)
David 278 visualizações
Trent&Lopez.FinalSwimmyDraft por Erin Trent
Trent&Lopez.FinalSwimmyDraftTrent&Lopez.FinalSwimmyDraft
Trent&Lopez.FinalSwimmyDraft
Erin Trent1.6K visualizações
Gastrointestinal Smooth Muscle Report por Jenny Richardson
Gastrointestinal Smooth Muscle ReportGastrointestinal Smooth Muscle Report
Gastrointestinal Smooth Muscle Report
Jenny Richardson2 visualizações
Electromyography Analysis for Person Identification por CSCJournals
Electromyography Analysis for Person IdentificationElectromyography Analysis for Person Identification
Electromyography Analysis for Person Identification
CSCJournals222 visualizações
A Novel Approach For Detection of Neurological Disorders through Electrical P... por IJECEIAES
A Novel Approach For Detection of Neurological Disorders through Electrical P...A Novel Approach For Detection of Neurological Disorders through Electrical P...
A Novel Approach For Detection of Neurological Disorders through Electrical P...
IJECEIAES12 visualizações
Neuron based time optimal controller of horizontal saccadic eye movements por Alireza Ghahari
Neuron based time optimal controller of horizontal saccadic eye movementsNeuron based time optimal controller of horizontal saccadic eye movements
Neuron based time optimal controller of horizontal saccadic eye movements
Alireza Ghahari135 visualizações
Senses Pre-Lab Report por Becki Roy
Senses Pre-Lab ReportSenses Pre-Lab Report
Senses Pre-Lab Report
Becki Roy3 visualizações

Mais de nareshkotra

ugc carelist journals 22nov.pdf por
ugc carelist journals 22nov.pdfugc carelist journals 22nov.pdf
ugc carelist journals 22nov.pdfnareshkotra
4 visualizações7 slides
scientific report journal 22 nov.pdf por
scientific report journal 22  nov.pdfscientific report journal 22  nov.pdf
scientific report journal 22 nov.pdfnareshkotra
3 visualizações6 slides
materials science journal 21 nov.pdf por
materials science journal 21 nov.pdfmaterials science journal 21 nov.pdf
materials science journal 21 nov.pdfnareshkotra
3 visualizações4 slides
international research journal of engineering and technology20nov.pdf por
international research journal of engineering and technology20nov.pdfinternational research journal of engineering and technology20nov.pdf
international research journal of engineering and technology20nov.pdfnareshkotra
4 visualizações12 slides
journal of applied science and engineering 2nov.pdf por
journal of applied science and engineering 2nov.pdfjournal of applied science and engineering 2nov.pdf
journal of applied science and engineering 2nov.pdfnareshkotra
2 visualizações11 slides
ugc carelist 17 nov.pdf por
ugc carelist 17 nov.pdfugc carelist 17 nov.pdf
ugc carelist 17 nov.pdfnareshkotra
3 visualizações6 slides

Mais de nareshkotra(20)

ugc carelist journals 22nov.pdf por nareshkotra
ugc carelist journals 22nov.pdfugc carelist journals 22nov.pdf
ugc carelist journals 22nov.pdf
nareshkotra4 visualizações
scientific report journal 22 nov.pdf por nareshkotra
scientific report journal 22  nov.pdfscientific report journal 22  nov.pdf
scientific report journal 22 nov.pdf
nareshkotra3 visualizações
materials science journal 21 nov.pdf por nareshkotra
materials science journal 21 nov.pdfmaterials science journal 21 nov.pdf
materials science journal 21 nov.pdf
nareshkotra3 visualizações
international research journal of engineering and technology20nov.pdf por nareshkotra
international research journal of engineering and technology20nov.pdfinternational research journal of engineering and technology20nov.pdf
international research journal of engineering and technology20nov.pdf
nareshkotra4 visualizações
journal of applied science and engineering 2nov.pdf por nareshkotra
journal of applied science and engineering 2nov.pdfjournal of applied science and engineering 2nov.pdf
journal of applied science and engineering 2nov.pdf
nareshkotra2 visualizações
ugc carelist 17 nov.pdf por nareshkotra
ugc carelist 17 nov.pdfugc carelist 17 nov.pdf
ugc carelist 17 nov.pdf
nareshkotra3 visualizações
top journals 16nov.pdf por nareshkotra
top journals 16nov.pdftop journals 16nov.pdf
top journals 16nov.pdf
nareshkotra3 visualizações
journal papers 16 nov.pdf por nareshkotra
journal papers 16 nov.pdfjournal papers 16 nov.pdf
journal papers 16 nov.pdf
nareshkotra4 visualizações
science research journal 15 nov.pdf por nareshkotra
science research journal 15 nov.pdfscience research journal 15 nov.pdf
science research journal 15 nov.pdf
nareshkotra3 visualizações
medical scopus journals 15 nov.pdf por nareshkotra
medical scopus journals 15 nov.pdfmedical scopus journals 15 nov.pdf
medical scopus journals 15 nov.pdf
nareshkotra7 visualizações
advanced materials journal .pdf por nareshkotra
advanced materials journal .pdfadvanced materials journal .pdf
advanced materials journal .pdf
nareshkotra4 visualizações
international research journal of engineering and technology 11.pdf por nareshkotra
international research journal of engineering and technology 11.pdfinternational research journal of engineering and technology 11.pdf
international research journal of engineering and technology 11.pdf
nareshkotra5 visualizações
scopus database journal 11 n.pdf por nareshkotra
scopus database journal 11 n.pdfscopus database journal 11 n.pdf
scopus database journal 11 n.pdf
nareshkotra6 visualizações
journal of engineering and applied science 10.pdf por nareshkotra
journal of engineering and applied science 10.pdfjournal of engineering and applied science 10.pdf
journal of engineering and applied science 10.pdf
nareshkotra5 visualizações
science research journal10 .pdf por nareshkotra
science research journal10 .pdfscience research journal10 .pdf
science research journal10 .pdf
nareshkotra4 visualizações
scientific report journal 09.pdf por nareshkotra
scientific report journal     09.pdfscientific report journal     09.pdf
scientific report journal 09.pdf
nareshkotra7 visualizações
top journals 08.pdf por nareshkotra
top journals 08.pdftop journals 08.pdf
top journals 08.pdf
nareshkotra3 visualizações
journal of applied science and engineering 08 .pdf por nareshkotra
journal of applied science and engineering 08 .pdfjournal of applied science and engineering 08 .pdf
journal of applied science and engineering 08 .pdf
nareshkotra3 visualizações
scopu s 07.pdf por nareshkotra
scopu s 07.pdfscopu s 07.pdf
scopu s 07.pdf
nareshkotra4 visualizações
ugc carelist 07 nov.pdf por nareshkotra
ugc carelist 07 nov.pdfugc carelist 07 nov.pdf
ugc carelist 07 nov.pdf
nareshkotra2 visualizações

Último

Web3 Lending.pptx por
Web3 Lending.pptxWeb3 Lending.pptx
Web3 Lending.pptxStrike Finance
6 visualizações4 slides
Hotel GDS por
Hotel GDSHotel GDS
Hotel GDSaishukri
5 visualizações10 slides
independent chandigarh escorts.pdf por
independent chandigarh escorts.pdfindependent chandigarh escorts.pdf
independent chandigarh escorts.pdfMonali Escorts
9 visualizações23 slides
Community Compassion The Vital Role of Charity Organizations in Singapore por
Community Compassion The Vital Role of Charity Organizations in SingaporeCommunity Compassion The Vital Role of Charity Organizations in Singapore
Community Compassion The Vital Role of Charity Organizations in SingaporeWorldVision5
8 visualizações6 slides
Colorful Illustrated Infographic.pdf por
Colorful Illustrated Infographic.pdfColorful Illustrated Infographic.pdf
Colorful Illustrated Infographic.pdfRichestSoft
5 visualizações1 slide
Get Best TimberTech deck builder Dripping in Springs TX por
Get Best TimberTech deck builder Dripping in Springs TXGet Best TimberTech deck builder Dripping in Springs TX
Get Best TimberTech deck builder Dripping in Springs TXAccent Deck Design
7 visualizações5 slides

Último(16)

Web3 Lending.pptx por Strike Finance
Web3 Lending.pptxWeb3 Lending.pptx
Web3 Lending.pptx
Strike Finance6 visualizações
Hotel GDS por aishukri
Hotel GDSHotel GDS
Hotel GDS
aishukri5 visualizações
independent chandigarh escorts.pdf por Monali Escorts
independent chandigarh escorts.pdfindependent chandigarh escorts.pdf
independent chandigarh escorts.pdf
Monali Escorts9 visualizações
Community Compassion The Vital Role of Charity Organizations in Singapore por WorldVision5
Community Compassion The Vital Role of Charity Organizations in SingaporeCommunity Compassion The Vital Role of Charity Organizations in Singapore
Community Compassion The Vital Role of Charity Organizations in Singapore
WorldVision58 visualizações
Colorful Illustrated Infographic.pdf por RichestSoft
Colorful Illustrated Infographic.pdfColorful Illustrated Infographic.pdf
Colorful Illustrated Infographic.pdf
RichestSoft5 visualizações
Get Best TimberTech deck builder Dripping in Springs TX por Accent Deck Design
Get Best TimberTech deck builder Dripping in Springs TXGet Best TimberTech deck builder Dripping in Springs TX
Get Best TimberTech deck builder Dripping in Springs TX
Accent Deck Design7 visualizações
Biography of Bert Boksen.pdf por Bert Boksen
Biography of Bert Boksen.pdfBiography of Bert Boksen.pdf
Biography of Bert Boksen.pdf
Bert Boksen7 visualizações
How Does The Sage Accounting System Help Companies Gain Financial Viability? por BrianElis
How Does The Sage Accounting System Help Companies Gain Financial Viability?How Does The Sage Accounting System Help Companies Gain Financial Viability?
How Does The Sage Accounting System Help Companies Gain Financial Viability?
BrianElis6 visualizações
How furniture rental service work - RentMacha por Rent Macha
How furniture rental service work - RentMachaHow furniture rental service work - RentMacha
How furniture rental service work - RentMacha
Rent Macha6 visualizações
The Importance of Engraved Gifts in Celebrations.pptx por Engraversworld Ltd
The Importance of Engraved Gifts in Celebrations.pptxThe Importance of Engraved Gifts in Celebrations.pptx
The Importance of Engraved Gifts in Celebrations.pptx
Engraversworld Ltd12 visualizações
amil baba kala jadu manpasand shadi ka taveez,wazifa,istikhara love marrige l... por amil baba
amil baba kala jadu manpasand shadi ka taveez,wazifa,istikhara love marrige l...amil baba kala jadu manpasand shadi ka taveez,wazifa,istikhara love marrige l...
amil baba kala jadu manpasand shadi ka taveez,wazifa,istikhara love marrige l...
amil baba5 visualizações
Experience the Speed of Tomorrow, Today! por jettglobal36
Experience the Speed of Tomorrow, Today!Experience the Speed of Tomorrow, Today!
Experience the Speed of Tomorrow, Today!
jettglobal365 visualizações
Quality Translations and Interpreting Empowering Houston’s Diverse Landscape por 24 Hour Translation
Quality Translations and Interpreting Empowering Houston’s Diverse LandscapeQuality Translations and Interpreting Empowering Houston’s Diverse Landscape
Quality Translations and Interpreting Empowering Houston’s Diverse Landscape
24 Hour Translation13 visualizações
Arrive in style with Jett Cabs Sedan service! por jettglobal36
Arrive in style with Jett Cabs Sedan service!Arrive in style with Jett Cabs Sedan service!
Arrive in style with Jett Cabs Sedan service!
jettglobal367 visualizações
Bosch Refrigerator Repair.pptx por 24x7servicecentre123
Bosch Refrigerator Repair.pptxBosch Refrigerator Repair.pptx
Bosch Refrigerator Repair.pptx
24x7servicecentre1235 visualizações
A Guide to Prevent Common Dog Problems in Dogs! por David Carter
A Guide to Prevent Common Dog Problems in Dogs!A Guide to Prevent Common Dog Problems in Dogs!
A Guide to Prevent Common Dog Problems in Dogs!
David Carter6 visualizações

science journal.pdf

  • 1. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 50 Original article1 Controlling Synchronization of Modified FitzHugh-Nagumo Neurons Under External Electrical Stimulation Deepak Mishra, Abhishek Yadav, Sudipta Ray and Prem K. Kalra Abstract We report control of synchronization between pair of coupled neurons under external electrical stimulation. A nonlinear controlling mechanism is proposed for keeping the coupled system in synchronized state. We studied transitions between synchrony and asynchrony because of variation in coupling strength. We discuss the dynamical analysis for the Modified FitzHugh-Nagumo neuron model in detail. This work focuses the application of control system theory for understanding possible synchronization phenomena in a pair of biological neuron models. Key Words: modified FitzHugh-Nagumo, nonlinear controller, synchronization, coupled neurons NeuroQuantology 2006; 1: 50-67 Introduction Determining the dynamical behavior of an ensemble of coupled neurons is an important problem in computational neuroscience. Commonly used models for the study of individual neuron which display spiking behavior include (a) Integrate-and-Fire neuron model and its variants (b) FitzHugh-Nagumo model (c) Hodgkin-Huxley model and (d) Morris-Lecar model (Gerstner, 2002; FitzHugh, 1969; Nagumo, 1962; Hodgkin, 1952; Koch, 1999; Abbott, 2001). From the very beginning of the research in the field of computational neuroscience, people deal with single neuron and its behavior. Present trends of research include investigation of Corresponding authors: Department of Electrical Engineering, Indian Institute of Technology Kanpur, India, e-mail: dkmishra@iitk.ac.in, ayadav.iitk@gmail.com, sray@iiita.ac.in, kalra@iitk.ac.in
  • 2. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 51 the behavior of neurons considered in a network and their way to fire synchronously. It is assumed that the activities in the brain are synchronous and underlying interests for synchronization of nonlinear oscillators in physical and biological systems range from novel communication strategies to understand how large and small neural assemblies efficiently and sensitively achieve desired functional goal (Pinto, 2000). The dynamics of many neural ensembles such as central pattern generators or thalamo-cortical circuits poses questions related to the cooperative behavior of neurons. Each neuron independently may show irregular behavior while ensembles of different neurons can synchronize in order to process biological information or produce regular, rhythmic activity (Elson, 1999). How do the dissimilar neurons synchronize? How do they inhibit noise and intrinsic fluctuations? What are the parameters responsible for such synchronization and regularization? Answers to these and similar questions may be found through simulations and experiments that enable one to follow qualitatively the cooperative dynamics of neurons as intrinsic synaptic parameters are varied (Elson, 1999). However, these problems did not receive many opportunities for extensive study. Many cells are linked together by specialized inter-cellular pathways known as gap junction. There are two types of possible couplings among neurons namely weak coupling and strong coupling, defined on the basis of the magnitude of coupling strength. In my paper (Mishra, 2004), the effect of coupling strength on dynamics of coupled neurons is studied. In recent years, there has been tremendous interest for the study of the synchronization of chaotic systems. The synchronous and asynchronous behavior of neurons is one of the important research topics (Jiang, 2004; Thompson, 1999). Application of nonlinear active controller for maintaining synchronism among neurons is one of the issues addressed in (Ucar, 2004). The phenomenon of synchronism gives rise to different dynamical behaviors such as chaotic synchronization etc. In (Mishra, 2004; Mishra, 2005), nonlinear dynamical analysis on single and coupled modified FitzHugh-Nagumo model under steady current stimulation is carried out. Also the effect of parameter variation on its behavior is investigated. In many papers (Pinto, 2000; Ucar, 2004; Rinzel, 1987; Elson, 1999) dynamical analysis on various neuron models is carried out under steady current input. The variations
  • 3. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 52 in the external stimulus may bring the system to unstable state from a stable one. However, biological rhythms, such as, cardiac and circadian rhythms arise from activity of multiple oscillators with dispersed intrinsic frequencies (Chang, 2000). Variety of complex dynamical behavior including phase locked limit cycles, quasi-periodicity, intermittency and chaos are observed in literature (Thompson, 1999) for sinusoidal external fields. Chang et.al. (Chang, 2000), investigated the stability of the output rhythm of these sympathetic oscillators for a periodic driving force. In this paper, a nonlinear controller has been designed to synchronize a coupled modified FitzHugh-Nagumo model. Dynamical characteristics of modified FitzHugh-Nagumo neuron model under external stimulation are discussed first. With the variation of the stimulation and the initial condition, the complex behavior is revealed. The response of a model of two neurons coupled with a gap junction is investigated and the significance of coupling coefficient is studied next. We propose a nonlinear active controller for the synchronization of a pair of coupled neurons. Numerical results in support of our findings are also presented. At last, we conclude our work. Dynamics of Modified FitzHugh-Nagumo Neuron Model The modified FitzHugh-Nagumo equations are a set of three coupled differential equations which exhibit the qualitative behavior observed in neurons, viz quiescence, excitability and periodicity (Rinzel, 1987). The system can be represented as ) cos( ) / ( ) ( , ) ( ) ( ) ( 3 / . . 3 . t A t F Where dy c x y bw a x w t F y w x x x Ω Ω = − + − = − + = + + − − = ε φ (1) The function F(t) represents the external stimulus. The variable x represents the potential difference between the dendritic spine head and its surrounding medium, w is recovery variable and y represents the slowly moving current in the dendrite. In this
  • 4. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 53 model, x and w together make up a fast subsystem relative to y . The Jacobian at equilibrium point (x*, w*, y*) is found to be           − − − − − = d b x J ε ε φ φ 0 0 1 1 1 2 (2) If at a neighborhood of a particular value µ0 of the parameter µ, there exists a pair of eigenvalues of J(µ) of the form α(µ) ± iβ(µ) such that α(µ) = 0, β(µ) ≠ 0, then no other eigenvalue of J(µ0) will be an integral multiple of iβ(µ0). Thus J(µ0) has a pair of pure imaginary eigenvalues. This helps in understanding the dynamics of the model at the equilibrium point. Dynamics of Single Uncoupled Modified FitzHugh-Nagumo Neuron Model The dynamical set of equations of a single uncoupled modified FitzHugh-Nagumo system is given in equations (1). The system parameters used for simulations are a = 0.7, b = 0.8, c = -0.775, φ = 0.08, ε = 0.0001 and d = 1.0. The calculated equilibrium point for the system at F(t) = 0 is: (x*, w*, y*) = (-1.0292, -0.4115, 0.2542). Eigenvalues at these points are: (λ1, λ2, λ3) = (-0.0002, -0.061+j0.283, -0.061+j0.283). We found that the set of equations are asymptotically stable around the equilibrium points at F(t) = 0. The variations in the external stimulus bring the system to unstable state (periodic oscillation). We analyze the response of the model by subjecting it under the following electrical stimulation ) cos( ) / ( ) ( t A t F Ω Ω = (3) Here, A represents the magnitude of the stimulus and Ω refers to the frequency of given stimulus. The stimulus frequency is varied while keeping the magnitude at a fixed value of A = 0.71, since at this particular value of A, modified FitzHugh-Nagumo neuron model gives periodic spiking. Simulation results at different stimulus frequencies are shown in Figure 1 and Figure 2. Time response for the neuron at Ω = 0.07 is shown in Figure 1(a) and phase portrait is drawn in Figure 1(b). Similar responses for Ω = 0.127 are shown in Figure 2. It is observed that with the variation in stimulus frequency, the neuron shows
  • 5. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 54 complex chaotic behavior. Hence the stimulus frequency can be considered as a significant parameter that affects the behavior of neuron. Fig.1 Time responses and phase portrait for modified FitzHugh-Nagumo model at stimulus frequency Ω = 0.07 (a) Time response (b) phase portrait. Fig.2 Time responses and phase portrait for modified FitzHugh-Nagumo model at stimulus frequency Ω = 0.07 (a) Time response (b) phase portrait. Bifurcation analysis with Ω as the parameter We have investigated behavioral change in the dynamics of modified FitzHugh-Nagumo model with respect to Ω by plotting leading Lyapunov exponents, and bifurcation diagram in Figure 3. It is observed that modified FitzHugh-Nagumo model exhibits stable, periodic and chaotic behavior for different value of Ω. Thus the frequency of injected stimulus plays important role and its variation alters the dynamics of model. The Lyapunov exponent is positive for Ω = 0.127.
  • 6. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 55 Fig.3 Plots of Leading Lyapunov exponent and bifurcation diagram with Ω as bifurcation parameter. (a) Leading Lyapunov exponent; (b) Bifurcation diagram. Dynamics of Coupled Modified FitzHugh-Nagumo Neuron Model We studied the characteristics of an uncoupled modified FitzHugh-Nagumo neuron in the previous section. In this section, we extend our analysis for coupled neuron models. A system of two coupled neurons can be expressed as: j i j i X c X f dt dX j i i ≠ = + = 2 , 1 , ) ( arctan ) ( (4) where Xij ∈ Rn (xi or xj) represents state variable of the two oscillating neurons, function f: Rn →Rn defines the dynamics of a single neuron in the absence of coupling, and c is the coupling matrix. Complete synchronization occurs when the coupled chaotic oscillators asymptotically exhibit identical behaviors, i.e., when || X1(t)-X2(t)|| →0 as t →∞, for any initial condition. The synchronization is dependent on the coupling matrix c. The dynamical equations for the coupled modified FitzHugh-Nagumo neuron model are given in equations (5). The two systems are coupled with different coupling parameters, say gc and g’c, with rest of the parameter values kept identical. (a) (b)
  • 7. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 56 ) ( , ) ( ) 2 cos( ) 2 / ( ) arctan( ' ) ( 3 / ) ( ), ( ) 2 cos( ) 2 / ( ) arctan( ) ( 3 / 2 2 . 2 2 2 . 2 1 2 2 3 2 2 . 2 1 1 . 1 1 1 . 1 2 1 1 3 1 1 . 1 dy c x y bw a x w t A x g t F y w x x x dy c x y bw a x w t A x g t F y w x x x c c − + − = − + = Ω Ω + + + + − − = − + − = − + = Ω Ω + + + + − − = ε φ π π ε φ π π (5) We have carried out the analysis in the presence of external electrical stimulus of magnitude A = 0.7 and frequency Ω = 0.127, the values for which the model exhibits complex chaotic response. The results for strongly coupled neuron models are shown in Figure 4. The coupling strengths are: gc = 0.9 and g’c = 0.9. The coupled modified FitzHugh-Nagumo neurons are synchronous, but the response is chaotic. Time courses for the variables x1 and x2 are shown in Figure 4(a). The synchronism among the neurons is evident from the plot between x1 and x2, which is almost a straight line as shown in Figure 4(b). We analyze a loosely coupled neural system, where the values for coupling coefficient are kept as gc = 0.009 and g’c = 0.009. The responses of coupled neurons are asynchronous. The firing of one neuron is out of phase with the other neuron. The time courses for x1 and x2, when system is loosely coupled, are shown in Figure 5(a). Figure 5(b) shows the plot between x1 and x2. The coupling among neurons can be weak and strong, so we have taken effect of unequal (Weak-Strong) coupling. This is done by keeping one of the neuron in strongly coupled state and other in weakly coupled state i.e. by keeping gc = 0.9 and g’c = 0.009,. The response with these values of coupling strengths is shown in Figure 6. The time courses for variables x1 and x2 are plotted in Figure 6(a). The responses of the variable x1 and x2 are not in complete synchronism but they are trying to achieve a synchronous state. The same can be observed from phase portrait of x1 and x2 drawn in Figure 6(b). In this case, neurons try to maintain synchronization, but they are not in exact synchronism. In order to bring this coupled system in synchronism, we need an active controller. In the next section, a control mechanism is explained which keeps the coupled neurons in exact synchronism by applying a control input to one of the pairs of neurons.
  • 8. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 57 Fig.4 Response of coupled modified FitzHugh-Nagumo neuron models (equations 5) with coupling strengths gc= 0.9 and g’c= 0.9. (a) The time courses for variables x1 and x2 (b) Phase portrait of the components of oscillations. Fig.5 Response of coupled modified FitzHugh-Nagumo neuron models (equations 5) with coupling strengths gc = 0.9 and g’c = 0.009. (a) The time courses for variables x1 and x2 (b) Phase portrait of the components of oscillations. The findings in the analysis of coupling strength effects support the hebbian hypothesis. According to Donald Hebb, if input from neuron A often contributes to the firing of neuron B, then the synapse from A to B should be strengthened (Dyan, 2001). Thus it can be stated that the coupling between the pair of neuron is one of the important parameter to be studied for exploring the intricacies of the coupled system. Nonlinear Active Controller for a Pair of Coupled Modified FitzHugh-Nagumo System It is found in previous section that because of unequal coupling strength we observe asynchrony among pair of neurons. In this section, we propose a control mechanism which can bring the two systems into exact synchronism. The schematic diagram for two coupled neurons is shown in Figure 7. The method is based on the Lyapunov stability theory.
  • 9. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 58 Fig.6 Response for coupled modified FitzHugh-Nagumo neuron model (equations 5) with coupling strengths gc = 0.009 and g’c = 0.009. (a) The time courses for variable x1 and x2 (b) Phase portrait of the components of oscillations. Fig. 7 Schematic diagram of two coupled neurons controlled by an active controller. Responses for Uncontrolled Pair of Neurons To begin with, we show the results for two uncontrolled coupled pairs of neurons whose dynamical equations can be given by the following set of equations. ) ( , ) ( ) 2 cos( ) 2 / ( ) arctan( ' ) ( 3 / ) ( ), ( ) 2 cos( ) 2 / ( ) arctan( ) ( 3 / 2 2 . 2 2 2 . 2 1 2 2 3 2 2 . 2 1 1 . 1 1 1 . 1 2 1 1 3 1 1 . 1 dy c x y bw a x w t A x g t F y w x x x dy c x y bw a x w t A x g t F y w x x x c c − + − = − + = Ω Ω + + + + − − = − + − = − + = Ω Ω + + + + − − = ε φ π π ε φ π π (6) ) ( ), ( ) 2 cos( ) 2 / ( ) arctan( ' ) ( 3 / ) ( ), ( ) 2 cos( ) 2 / ( ) arctan( ) ( 3 / 4 4 . 4 4 4 . 4 3 4 4 3 4 4 . 4 3 3 . 3 3 3 . 3 4 3 3 3 3 3 . 3 dy c x y bw a x w t A x n t F y w x x x dy c x y bw a x w t A x n t F y w x x x c c − + − = − + = Ω Ω + + + + − − = − + − = − + = Ω Ω + + + + − − = ε φ π π ε φ π π (7)
  • 10. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 59 The parameters used for the uncontrolled coupled pair of neurons are same as used for earlier analysis. The only changes are in the values of coupling coefficients. The coefficient values used are: gc = g’c = 0.6 and nc = n’c = 0.02. Simulation results for this model are drawn in Figure 8. The time evolutions of the variables x1 and x3 are shown in Figure 8(a). The corresponding phase portrait between x1 and x3 is plotted in Figure 8(b). Error curves for uncontrolled system are plotted in Figure 9. It is evident from these figures that the pairs of neurons are in asynchronous state. Fig.8 Responses of pair of coupled neurons (equations 6 and 7) used in the absence of nonlinear active controller at different coupling strengths gc = 0.6 and nc= 0.02. (a) Time courses for variables x1 and x3 (b) Phase portrait of the components of oscillations (b) (a)
  • 11. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 60 Responses for controlled pair of neurons In order to bring the synchronism among these neurons we proposed a control law. The equations given in (7) are replaced by the set of coupled system given by equations (8), which incorporates the control input. Thus, Fig. 9 The error curves for the variables in modified FitzHugh-Nagumo system (equations 6 and 7) at coupling strengths gc = 0.6 and g’c = 0.02. (a) Error signals e1, e2 and e3 (b) Error signals e4, e5 and e6. (a) (b)
  • 12. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 61 ) ( ) ( ), ( ) ( ) ( ) 2 cos( ) 2 / ( ) arctan( ) ( 3 / 3 3 . 3 3 3 . 3 4 3 3 3 3 3 . 3 t dy c x y t bw a x w t t A x n t F y w x x x c b a c µ ε µ φ µ π π + − + − = + − + = + Ω Ω + + + + − − = ) ( ) ( ), ( ) ( ) ( ) 2 cos( ) 2 / ( ) arctan( ' ) ( 3 / 4 4 . 4 4 4 . 4 3 4 4 3 4 4 . 4 t dy c x y t bw a x w t t A x n t F y w x x x f e d c µ ε µ φ µ π π + − + − = + − + = + Ω Ω + + + + − − = (8) Errors between the variables are calculated as 2 4 6 2 4 5 2 4 4 1 3 3 1 3 2 1 3 1 , , , , y y e w w e x x e y y e w w e x x e − = − = − = − = − = − = (9) Ideally, the rate of change of error must be zero in order to achieve exact synchronism. Derivative of the error signals are given by 2 . 4 . 6 . 2 . 4 . 5 . 2 . 4 . 4 . 1 . 3 3 . 1 . 3 . 2 . 1 . . 3 1 . , , , , y y e w w e x x e y y e w w e x x e − = − = − = − = − = − = ⋅ (10) The calculated error signal for the system is given by following equations f e d c c c b a c c de e e be e e x g x n x x e e e e de e e be e e x g x n x x e e e e µ ε µ φ µ µ ε µ φ µ + − − = + − = + − + + − + − = + − − = + − = + − + + − + − = ) ( , ) ( ) arctan( ' ) arctan( ' 3 / 3 / ) ( , ) ( ) arctan( ) arctan( 3 / 3 / 6 4 6 . 5 4 5 . 1 3 3 2 3 4 6 5 4 4 . 2 1 3 . 3 1 . 2 2 4 3 1 3 3 2 3 1 . 1 (11) We proposed the control law for µa, µb, µc, µd and µf in equations (12). They are expressed as in equation (12). 1 1 2 4 3 1 3 3 3 2 1 , ) arctan( ) arctan( 3 / 3 / de be x g x n x x e e Ke c b c c a ε µ φ µ µ = − = + − − + − + − = 6 5 1 3 3 2 3 4 6 5 4 1 , ) arctan( ' ) arctan( ' 3 / 3 / de be x g x n x x e e e K f e c c d ε µ φ µ µ = − = + − − + − + − = (12) The systems given in (6) and (8) will approach synchronization for any initial conditions by the control law given by (12). We construct the Lyapunov function ) )( 2 / 1 ( 2 6 2 5 2 4 2 3 2 2 2 1 e e e e e e V + + + + + = (13)
  • 13. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 62 The differential of the Lyapunov function along the trajectory of system (11) is 6 . 6 5 . 5 4 . 4 3 . 3 2 . 2 1 . 1 e e e e e e e e e e e e V + + + + + = (14) Substituting above into (14) results in 0 ) ( 2 6 2 5 2 4 2 3 2 2 2 1 . < − − − − − − = e e e e e e V (15) which gives asymptotic stability of the system by Lyapunov stability theory. This means that the coupled systems (6) and (8) are synchronized for any initial conditions. Results of the controlled pair of coupled modified FitzHugh-Nagumo neurons are shown in Figure 10. The time evolutions of variables x1 and x3 are shown in Figure 10(a). Phase portrait for variables x1 and x3 is plotted in Figure 10(b). It is evident that the set of coupled neurons is now in exact synchronism. The control signal profile is shown in Figure 11. This shows the time evolution of controller activity. The error profile drawn for the system is shown in Figure 12. The system is operated without any controller till t=250 msec and it is switched to controlling mode after this time instant. It is observed from the error profile that, as soon as the controller comes into action, system achieves complete synchronism. The description of a nonlinear controller for maintaining synchronism is given. We compared the results with a nonlinear coupled neuron model in the absence of controlling mechanism. It is found that the application of active controller for maintaining synchronism in nonlinear systems is very effective and can be used in real life applications.
  • 14. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 63 Fig. 10 Responses of pair of coupled neurons (equations 6 and 8) with nonlinear active controller. The responses are generated at different coupling strengths i.e. gc = 0.6 and nc = .02. (a) Time courses for variables x1 and x3 (b) Phase portrait of the components of oscillations. (a) (b)
  • 15. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 64 Fig. 11 Responses of pair of coupled neuron used with nonlinear active controller at different coupling strengths gc = 0.6 and nc = 0.02. (a) Control signals (equations 11) µa, µb and µc (b) Control signals (equations 11) µd, µe and µf for keeping the system in synchronism. (b) (a)
  • 16. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 65 Fig. 12 Responses for pair of coupled neuron used with nonlinear active controller at different coupling strengths gc = 0.6 and nc = 0.02. (a) Error signals (equations 9) e1, e2 and e3 (b) Error signals (equations 9) e4, e5 and e6. (b) (a)
  • 17. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 66 Conclusion In this paper, the characteristics of three dimensional modified FitzHugh-Nagumo neuron model is studied. Dynamical behavior of the modified FitzHugh-Nagumo system under external electrical stimulation is presented and it is verified that the introduction of periodic stimulation modifies the dynamics of biological system by presenting the dynamical behavior for the modified FitzHugh-Nagumo system under external electrical stimulation. The responses of the system for different stimulus frequencies are shown. The synchronization of two coupled neurons subjected to external electrical stimulation is studied. The behavior of coupled neurons with the variation in coupling strength is also studied. A nonlinear active controller description is provided at the end. It is shown that this controller can maintain the synchronous behavior among strongly-weakly coupled neurons. The methodology for determining control law is presented. We compared these results with the response of a nonlinear coupled neuron model in the absence of controlling mechanism. It is found that the application of active controller for maintaining synchronism in nonlinear system is very effective and can be used in real life applications.
  • 18. NeuroQuantology 2006|Issue 1|Page 50-67 Mishra et al. FitzHugh-Nagumo Neurons ISSN 1303 5150 www.neuroquantology.com 67 References Gerstner W and Kistler WM. Spiking Neuron Models, Single Neurons, Populations, Plasticity, Cambridge University Press. 2002. Pinto RD, Varona P, Volkovskii AR et al. Synchronous behavior of two coupled electronic neurons. Physical Review E 2000;62:2644-2655. Ucar A, Lonngren KE, Bai WE. Synchronous of the Coupled FitzHugh-Nagumo System. Chaos, Solitons and Fractals 2004;20:1085-1090. Mishra D, Yadav A, Ray S, Kalra PK. Nonlinear Dynamical Analysis on Coupled Modified FitzHugh-Nagumo Neuron Model. ISNN 2005, LNCS 3496, 2005;95-101. Mishra D, Yadav A, Ray S, Kalra PK. Bifurcation analysis in modified Fitzhugh Nagumo neuronal model. NCCDS 2005. Jiang W, Bin D, Tsang KM. Chaotic synchronization of neurons coupled with gap junction under external electrical stimulation. Chaos, Solitons and Fractals 2004; 22:469-476. Thompson CJ, Bardos DC, Yang YS, Joyner KH. Nonlinear cable models for cells exposed to electric fields I. General Theory and Space-clamped Solutions. Chaos, Solitons and Fractlas 1999;10(11):1825-1842. Hodgkin A and Huxley A. A quantitative description of membrane current and its application to conduction and excitation in nerve. Journal of Physiology, London, 1952;117:500-544. Nagumo J, Arimoto S and Yosizawa S. An active pulse transmission line simulating nerve axon. Proc IRE, 1962;50. FitzHugh R. Mathematical models for excitation and propagation in nerve. Biological Engineering 1969. Koch C. Biophysics of computation. Oxford University Press, 1999. Dyan P and Abbott LF. Theoretical neuroscience: computational and mathematical modeling of neural systems. The MIT Press, Massachusetts. 2001. Elson RC, Selverston A, Huerta R, Rulkov NF, Rabinovich M, Abarbanel HDI. Synchronous behavior of two coupled biological neurons. Physical Review Letters 1999; 81: 5692-5695. Rinzel J. A formal classification of bursting mechanisms in excitable systems, in mathematical topics in population biology, morphogenesis and neuroscience. Lecture notes in Biomathematics. Springer-Verlag, New York, 1987; 71: 267-281. Chang HS, Staras K, Gilbey MP. Multiple Oscillators Provide Metastability in Rhythm Generation. The Journal of Neuroscience 2000; 20(13): 5135-5143.