Dynamical Systems, Differential

Equations and Applications

AIMS Proceedings, 2015

doi:10.3934/proc.2015.0195
pp. 195203

STOCHASTIC MODELING OF THE FIRING ACTIVITY OF COUPLED

NEURONS PERIODICALLY DRIVEN

Maria Francesca Carfora

Istituto per le Applicazioni del Calcolo CNR
Napoli, Italy

Enrica Pirozzi
Dipartimento di Matematica e Applicazioni
Universit`
a di Napoli Federico II
Napoli, Italy

Abstract. A stochastic model for describing the firing activity of a couple of interacting
neurons subject to time-dependent stimuli is proposed. Two stochastic differential equations suitably coupled and including periodic terms to represent stimuli imposed to one
or both neurons are considered to describe the problem. We investigate the first passage
time densities through specified firing thresholds for the involved time non-homogeneous
Gauss-Markov processes. We provide simulation results and numerical approximations
of the firing densities. Asymptotic behaviors of the first passage times are also given.

1. Introduction. The study of the dynamics of couples of interacting neurons is an essential step towards the modeling of more complex dynamics. Indeed, in literature the
number of papers on little and large networks of neurons (see, for example,[13, 16, 17]) is
rapidly growing. In particular, in the framework of stochastic modeling the investigations
essentially proceed along the following directions: the use of the Stein equations [7, 8],
the jump-diffusion processes [16] or the Gaussian processes [1] subject to Poissonian inputs
originated by others neurons; more recently models of copulas [14] have been proposed.
Motivated by our studies related to the first passage time problem for certain classes of
stochastic processes [3, 6, 9], we built some models of single neuron activity and we gave
evaluations of firing densities. In the last two years, combining our previous investigations
about neuronal Leaky Integrate-and-Fire (LIF) models, first passage time (FPT) problems,
Gaussian-Markovian (GM) processes and coupled dynamics, we carried out specific stochastic models for the dynamics of coupled neurons [2, 4]. Our models are based on the use
of two stochastic differential equations (SDE) of LIF type. They are coupled by means
of a stochastic function which affects the firing activity of a neuron only when the other
one fires. Specifically, we include a synaptic current conveying all external stimuli and, by
adding a stochastic term in that current, we model the interconnection between the two
neurons. Appropriate regularity conditions on the involved functions allow us to determine
the Gauss-Diffusion processes solving the considered equations. We use such processes to
model the stochastic time evolution of the potential of neuronal membranes of the two neurons and FPT are investigated to obtain estimates of the firing activity of each interacting
neuron. In particular, by applying an average operator, we obtain an expression for the
mean functions of the above processes that involves the stochastic coupling functions. We
are able to investigate the FPT of such processes through firing thresholds by numerical and
2010 Mathematics Subject Classification. Primary: 60J70; Secondary: 9208.
Key words and phrases. LIF neuronal model, first passage time, GaussMarkov processes, periodic stimulus, asymptotic regime.

195

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MARIA FRANCESCA CARFORA AND ENRICA PIROZZI

simulative techniques. Moreover, in the asymptotic regime we use the available analytical
expressions for the firing densities to provide the mean functions in closed form.
In the present paper we extend our model by adding a periodic function (periodic stimulus) in the coupled dynamics. In [11] a wide discussion on the motivations for considering
periodic stimuli based on the grounds of neuro-physiological evidences is reported. More
recently, the LIF model in the presence of a periodic stimulus has been considered in [5] and
[15]. Identifying the neurons as Neuron 1 and Neuron 2, we firstly focus our attention on the
firing activity of Neuron 2 when only Neuron 1 is subject to a periodic signal. The numerical
approximations of both firing activities are then obtained by solving two Volterra integral
equations via numerical quadrature. Comparisons with simulation results are given. An
asymptotic approximation is also given and suitably used. Finally, the mutual interaction
between two neurons is also investigated providing corresponding results for excitatory and
inhibitory coupling functions.
2. The model. The model proposed in [2], [4] for two interacting neurons is here generalized to include the effects of a periodic signal, acting on one of the neurons, during coupled
dynamics. Denoting by Vi (t) the sub-threshold membrane potential time course of Neuron i
(i = 1, 2), we consider the following stochastic differential equations:
q


(1)
dVi (t) = ai (t)Vi (t) + Bi,3i (t) dt + i2 (t)dWi (t) (i = 1, 2; t 0).
We assume that a spike of Neuron i occurs when its membrane potential Vi (t) attains a
constant firing threshold Si ; then, the dynamics restarts from the reset value of Vi (t) after
the spike that we set as Vi (0) := v0i < Si . In Eqs. (1), {W1 (t) : t 0} and {W2 (t) : t 0}
are two independent standard Brownian motions. In the sequel, in order to describe the time
evolution of the membrane potential of two interacting neurons, we consider the generalized
Leaky Integrate-and-Fire (LIF) model for a single neuron, characterized by the following
functions:
1
i + i i
ai (t) := , Bi,3i (t) :=
+ bi (t) + Ii,3i (t), i2 (t) := i2 (i = 1, 2). (2)
i
i
For Neuron i, the parameters i > 0, i and i represent the membrane decay time constant, the membrane resting potential and a constant current (due to the overall effect of
the interaction with the surrounding environment and/or to a constant external stimulus),
respectively. The function bi (t) can represent a periodic signal acting on one of the two
neurons; specifically, we consider in the following
b1 (t) = cos(t + ),

b2 (t) = 0.

Finally, let (i) be the time of the first spike of Neuron i; referring to the dynamics of
the neuronal membrane potential during the time interval [0, (i) ], the additional synaptic
currents Ii,3i (t) for i = 1, 2 are such that
h
i
Ii,3i (t) = i0i et/i + ki 1 et/i H3i (t)
(3)
where the stochastic function H3i (t) is defined as
(
0, if t < (3i) ,
H3i (t) :=
1, if t (3i)
with (3i) being the first firing instant (if any) of Neuron 3 i occurring in the interval
[0, (i) ]. The effect of this random component on the dynamics of Neuron i is a jump
of amplitude ki in the synaptic current Ii,3i at each spike of the other neuron, followed
by an exponential decay with time constant i . Then ki represents the intensity of the
excitatory (ki > 0) or inhibitory (ki < 0) contribution of Neuron i activity to the dynamics

STOCHASTIC MODELING OF COUPLED NEURONS PERIODICALLY DRIVEN

197

of Neuron 3 i. We note that in such a model just after a spike time (i) all functions
involved in Neuron i dynamics are reset to their initial values.
2.1. Previous work. In previous investigations [2, 4] we proved that, in case of bi = 0, the
firing activity of the two interacting neurons obeying to the dynamics (1) can be described
by a couple of Gauss-Diffusion (GD) processes {V1 (t), V2 (t), t [0, +)}. Under suitable
assumptions we identified the probability distribution of the InterSpikeInterval (ISI) random
variable T (i) for the Neuron i with that of the First Passage Time (FPT) random variable
TVi ,Si (v0i , 0) := inf{t 0 : Vi (t) Si , v0i < Si } for i = 1,2.
In particular, denoting by V any of the processess V1 , V2 (so omitting for ease of notation
the subscripts i), it was proved ([9]) that the FPT pdf
gV [S, t|v0 , 0] :=

d
P(TV,S (v0 , 0) t)
dt

is the solution to the second-kind non-singular Volterra integral equation:

Z t
gV [S, t|v0 , 0] = V [S, t|v0 , 0] +
V [S, t|S, z]gV [S, z|v0 , 0] dz,

(4)

where the function V [S, t|v, z] is completely specified by knowing the mean function mV (t)
and the covariance function cV (s, t|v0 , 0) of the process V (t). Indeed, it is [9]
 0
S (t) m0V (t) S(t) mV (t) u0V (t)vV (z) uV (z) vV0 (t)
V [S(t), t|v, z] =

2
2
uV (t)vV (z) uV (z) vV (t)

0
0
y mV (z) uV (t) vV (t) uV (t) vV (t)

fV [S(t), t|y, z],

2
uV (t) vV (z) uV (z) vV (t)
with uV (t), vV (t) being the two covariance factors (i.e. cV (s, t|v0 , 0) = uV (t)vV (t)) and
fV (x, t|y, z) being the transition density of the process V (t), respectively. Then, once determined the mean and covariance functions of both processes, by applying a numerical
procedure for solving (4) we can give an approximation of their FPT pdfs gVi [Si , t|v0i , 0]
and compare them to the estimation of the ISI pdfs obtained by simulating the dynamics
of (1).
2.2. Mean of the two processes. To extend such results in presence of a periodic input
signal, let us consider first the simpler case of one-way interaction (i.e. we assume k1 = 0
in (3)). As proved in [6, Prop. 5], the solution to
p


dV (t) = a(t)V (t) + B(t) dt + 2 (t)dW (t)
(t 0)
with V (0) = v0 is a Gauss-Markov process whose mean and covariance functions are given
by


Z t
m(t|v0 , 0) := mV (t) =eA(t) v0 +
B(s)eA(s) ds
Z s0
cV (s, t|v0 , 0) = uV (s)vV (t) =eA(t) eA(s)
2 ()e2A() d
0

where A(t) =
observing that

Rt
0

a(s) ds. Then, the dynamics of Neuron 1 can be completely specified by

B1,2 (t) = B1 (t) =

1 + 1 1
+ cos(t + ) + i01 et/1
1

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MARIA FRANCESCA CARFORA AND ENRICA PIROZZI

so that
 t/1

h
i
e
et/1
mV1 (t|v01 , 0) =v01 et/1 + (1 + 1 1 ) 1 et/1 + i01
1/1 1/1
o
1 n
t/1
+
cos(t
+
)
+

sin(t
+
)

(cos

sin
)e
1
1
1 + 2 12
whereas for the covariance function we have:
i
h
2 1
cV1 (s, t|v01 , 0) = 1 et/1 es/1 es/1
2

(0 s t).

(5)

Now, referring to the interval [0, (2) ] under the hypothesis 0 < (1) < (2) , the mean
value of the process {V2 (t) : t 0} subject to the dynamics of Neuron 1 is given by

 t/2
h
i
h
i
e
et/2
E V2 (t)| (1) = v02 et/2 + (2 + 2 2 ) 1 et/2 + i02
1/2 1/2
Z th
i
+ k2 et/2
1 es/2 H1 (s)es/2 ds.
0

Since the process {H1 (s) : 0 s t} is measurable, it is possible to apply again the
expectation operator to obtain


Z th
i
E et/2
1 es/2 H1 (s)es/2 ds
0

=e

t/2

Z th

i
1 es/2 es/2 E [H1 (s)] ds

= et/2

Z th
0

i
1 es/2 es/2 PTV1 (s) ds



where we denoted by PTV1 (s) := P (1) s the probability distribution of the first spike
instant (1) of Neuron 1 to occur before s and TV1 := TV1 ,S1 . Then we have

 t/2
h
i
e
et/2
mV2 (t|v02 , 0) =v02 et/2 + (2 + 2 2 ) 1 et/2 + i02
1/2 1/2
(6)
Z th
i
t/2
s/2
s/2
1e
e
PTV1 (s) ds.
+ k2 e
0

Following the same reasoning it is possible to obtain also the mean of V1 (t) subject to
the dynamics of Neuron 2 (k1 6= 0) as

 t/1
h
i
e
et/1
mV1 (t|v01 , 0) =v01 et/1 + (1 + 1 1 ) 1 et/1 + i01
1/1 1/1
o
1 n
t/1
+
cos(t
+
)
+

sin(t
+
)

(cos

sin
)e
(7)
1
1
1 + 2 12
Z th
i
1 es/1 es/1 PTV2 (s) ds.
+k1 et/1
0

We outline that the expressions given by Eqs (6),(7) for the mean functions of the two
processes are still coupled: while in the simpler case of one way interaction, for instance k1
= 0, we can obtain a numerical approximation for the FPT pdf for Neuron 1 by Eq. (4)
and then for the corresponding distribution PTV1 (s) needed in the evaluation of mV2 , in the
general case of mutual interaction suitable aymptotic approximations are required, that we
describe in the next paragraph.

STOCHASTIC MODELING OF COUPLED NEURONS PERIODICALLY DRIVEN

199

2.3. Asymptotic behavior of the FPT densities. We present here in details the asymptotic result for the more complex dynamics of Neuron 1; the corresponding result for
Neuron 2 easily follows. Let us recall that the process
U (t) = V1 (t) mV1 (t)

(8)

is an OrnsteinUhlenbeck process satisfying the SDE

dU (t) =

1
U (t)dt + 1 dW (t)
1

with U (0)= 0. Now, based on (8) it is possible to turn the FPT problem for the process
V1 (t) through the boundary S1 into the corresponding FPT problem for U (t) through the
transformed boundary SU = S1 mV1 (t). From the results reported in [5, 10, 12] we know
that for the FPT density of U (t), namely gU (t), in presence of an asymptotically periodic
boundary S1 (t) the following asymptotic approximation holds
Z t

hU (s)ds
gU (t) hU (t) e 0
with hU (t) a suitable function; then, following [12] where an analogous asymptotic result is
obtained for a generic Gauss Markov process by spatial transform of both the process and
the boundary, we have that the FPT density for the process V1 (t) through S1 admits a non
homogeneous asymptotic
p approximation under the hypotheses that t  max{1 , 1 } and
[S1 maxt0 (t)] > 12 1 :
Z t

hV1 (s)ds
gV1 (t) hV1 (t) e 0
(9)
where, denoting by Q the period of the signal, it is
:= lim U [S1 mV1 (t + nQ), t + nQ|U (0), 0] =
n




1
[S1 (t)]2
1
0
p
[S

(t)]
+

(t)

exp

1
1 12
1 12 1

hV1 (t)

with the periodic function (t) denoting the asymptotic limit of the mean mV1 :
(t) = lim mV1 (t + nQ|v01 , 0)
n

=1 + 1 1 + k1 1 +

1
[cos(t + ) + 1 sin(t + )] .
1 + 2 12

The FPT density for the process V2 (t) through S2 admits an analogous asymptotic approximation (as already obtained by the authors
in [2]) under the hypotheses that t 
p
2
max{2 , 2 } and S2 (2 + 2 2 + k2 2 ) > 2 2 :
gV2 (t) hV2 ehV2 t
with
hV2



S2 (2 + 2 2 + k2 2 )
[S2 (2 + 2 2 )]2
p
=
exp
.
2 22
2 2 22

From these approximations we also obtain

Z s

hV1 ()d
PTV1 (s) 1 e 0
;

PTV2 (s) 1 ehV2 s

(10)

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MARIA FRANCESCA CARFORA AND ENRICA PIROZZI

Figure 1. Plots of the numerical FPT pdf for both neurons (blue line),
along with their asymptotic approximations (red line) and corresponding
histograms in the case of no interaction (k1 = k2 = 0.0) for the parameters
values: S = 2.0, v0 = 0, = 0.0, 2 = 1.0, = 0.0, i0 = 0.5, = = 1; on
the left Neuron 1, on the right Neuron 2.
so that the mean of both {V1 (t) : t 0} and {V2 (t) : t 0} can be approximated as
mV1 (t|v01 , 0)
= v01 e

t/1

+ (1 + 1 1 ) 1 e

t/1


+ i01

et/1 et/1
1/1 1/1

o
1 n
cos(t + ) + 1 sin(t + ) (cos + 1 sin )et/1
2
2
1 + 1
Z th
i


t/1
+k1 e
1 es/1 es/1 1 ehV2 s ds,

(11)

mV2 (t|v02 , 0)

 t/2
h
i
et/2
e
t/2
= v02 e
+ (2 + 2 2 ) 1 e
+ i02
1/2 1/2
Z s

Z th
i

hV1 ()d

+k2 et/2
1 es/2 es/2 1 e 0
ds.
t/2

(12)

3. Numerical Experiments. To assess the effectiveness of our approximations, we perform some experiments to compare both the FPT density obtained by numerical integration
of Eq.(4) and its asymptotic approximation as given by Eqs.(9) and (10) with the histogram
of the FPT obtained by the numerical simulation of Eqs.(1).
In the following we specify the periodic signal by setting = 1.0, = /4, = 0.0.
Moreover, for simplicity, we also set 1 = 2 := , 12 = 22 := 2 , 1 = 2 := , i01 = i02 :=
i0 , 1 = 2 := , 1 = 2 := , v01 = v02 := v0 , S1 = S2 := S.
We first consider the dynamics of both neurons, as described by Eqs.(1), in the case of
no interaction (k1 = k2 = 0) to show how the numerical reconstruction of the FPT density
and the related asymptotic approximation fit the histogram of the spike times obtained by
numerical integration of the SDE (1). Indeed, in Fig.1, with the choice of parameters indicated in the corresponding caption, the numerical reconstruction of the probability density
function of FPT (blue line), its asymptotic approximation (red line) and the corresponding
ISIs histograms are shown for both neurons. The agreement is very satisfactory.

STOCHASTIC MODELING OF COUPLED NEURONS PERIODICALLY DRIVEN

201

Then we consider the dynamics of Neuron 2 subject to Neuron 1 firing (one way interaction, k1 = 0 and k2 6= 0). In Fig.2 results are shown for increasing values of the interaction
intensity k2 from 0.1 to 0.7: the retrieved density exhibits damped oscillations that represent
the excitatory effect of the interaction with Neuron 1.

Figure 2. Plots of the FPT pdf for V2 (continuous line) obtained by

Eq.(12) in the case of one-way interaction and corresponding histograms.
Parameters values are: S = 2.0, v0 = 0, = 0.0, 2 = 1.0, = 0.0, i0 =
0.5, = = 1. First row: on the left k2 = 0.1, on the right k2 = 0.3;
second row: on the left k2 = 0.5, on the right k2 = 0.7.
It has to be stressed that the accuracy of our approximation, being based on averaging
the stochastic contributions coming from the spikes of the other Neuron, depends on the
intensity of the interaction. Indeed, the experiments performed and reported in Fig.2 confirm
that the higher the intensity ki of the interaction, the worse is the agreement between the
numerical reconstruction of the FPT pdf and the corresponding histogram of firing densities.
Finally, we present just two examples of mutual interaction: we first consider the case of
excitationinhibition, by setting k1 > 0 and k2 < 0; then the case of inhibitionexcitation
(k1 < 0, k2 > 0). Figure 3 shows the numerical approximations we obtain in both cases
for Neuron 1 and Neuron 2 FPT densities along with the corresponding histograms. Even
if the intensity we chose in all cases for the interaction (k1 = 0.25, k2 = 0.25) is quite
high compared to the value i0 representing the overall contribution of the other surronding
neurons, our approximation is still satisfactory.

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MARIA FRANCESCA CARFORA AND ENRICA PIROZZI

Figure 3. Plots of the numerical approximation of the FPT pdfs for both
neurons (continuous lines) and corresponding histograms in the case of mutual interaction: on the first row the case of excitation-inhibition (k1 =0.25,
k2 =-0.25); on the second row the case of inhibition-excitation (k1 =-0.25,
k2 =0.25). On both rows Neuron 1 on the left, Neuron 2 on the right. Other
parameters are set as in the previous Figures.
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Received September 2014; revised November 2014.

E-mail address: f.carfora@iac.cnr.it
E-mail address: enrica.pirozzi@unina.it