Biol Cybern (2014) 108:747–756
DOI 10.1007/s00422-014-0616-4
ORIGINAL PAPER
Bifurcation and oscillation in a time-delay neural mass model
Shujuan Geng · Weidong Zhou · Xiuhe Zhao ·
Qi Yuan · Zhen Ma · Jiwen Wang
Received: 20 May 2013 / Accepted: 17 June 2014 / Published online: 22 July 2014
© Springer-Verlag Berlin Heidelberg 2014
Abstract The neural mass model developed by Lopes da
Silva et al. simulates complex dynamics between cortical
areas and is able to describe a limit cycle behavior for alpha
rhythms in electroencephalography (EEG). In this work, we
propose a modified neural mass model that incorporates a
time delay. This time-delay model can be used to simu-
late several different types of EEG activity including alpha
wave, interictal EEG, and ictal EEG. We present a detailed
description of the model’s behavior with bifurcation dia-
grams. Through simulation and an analysis of the influence
of the time delay on the model’s oscillatory behavior, we
demonstrate that a time delay in neuronal signal transmis-
sion could cause seizure-like activity in the brain. Further
study of the bifurcations in this new neural mass model could
provide a theoretical reference for the understanding of the
neurodynamics in epileptic seizures.
Keywords Neural mass model · Electroencephalography ·
Bifurcation · Spike-like oscillation · Seizure
S. Geng · W. Zhou (B) · Q. Yuan · Z. Ma
School of Information Science and Engineering, Shandong
University, 27 Shanda Road, Jinan 250100,
People’s Republic of China
e-mail: wdzhou@sdu.edu.cn
S. Geng
School of Information and Electric Engineering, Shandong Jianzhu
University, Jinan 250100, People’s Republic of China
X. Zhao · S. Geng · Q. Yuan · W. Zhou · Z. Ma · J. Wang
Suzhou Institute, Shandong University, Suzhou 215123,
People’s Republic of China
X. Zhao · J. Wang
Qilu Hospital, Shandong University, Jinan 250100,
People’s Republic of China
1 Introduction
An electroencephalogram (EEG) is produced by amplify-
ing and recording voltage differences between electrodes,
placed on the scalp or cerebral cortex, which reflect the elec-
trical activity in the brain. EEGs can often be decomposed
into distinct frequency bands (delta, 1–4 Hz; theta, 4–8 Hz;
alpha, 8–12 Hz; beta, 12–30 Hz; gamma, 30–70 Hz). EEGs
are an important tool to study human brain activity in gen-
eral, and epileptic processes in particular, with the appro-
priate time resolution. In neurology, a chief application of
EEGs is used as a diagnostic for epilepsy, since epileptic
brain activity can produce unambiguous abnormalities in a
standard EEG study.
In order to simulate the electrical activity of the brain with
its intricate cortical structures, various mathematical models
have been developed (Deco et al. 2003). One class of such
models is known as neural mass models (NMMs), which
simulate the dynamics of neuronal populations by provid-
ing a balance between mathematical simplicity and biolog-
ical plausibility. They are currently widely used as genera-
tive models to explain noninvasive electrophysiological brain
measurements such as those found in EEGs.
NMMs describe neural function at a mesoscopic level
(Deco et al. 2003; Coombes 2010), in contrast to single neu-
ron ‘integrate-and-fire’ models (Abbott 1999), or the more
elaborate Hodgkin and Huxley models (Hindmarsh and Rose
1984; Hodgkin and Huxley 1952). NMMs quantify the mean
firing rates and mean postsynaptic potentials of distinct neu-
ronal populations, called neural masses (NMs). While single
neurons are considered to be the primary computational units
of the brain’s architecture (Hodgkin and Huxley 1952; Finger
2001), it is also widely accepted that the relevant informa-
tion processing underlying brain function in both healthy and
diseased states is carried out by ensembles of interacting neu-
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rons at the mesoscopic level (Shepherd 1991; Shepherd et al.
1975; Jirsa 2004).
The first NMMs were proposed in the early 1950s (Beurle
1956). Substantial contributions were made by Freeman and
co-workers as part of their study of perceptual processing in
the olfactory system (Freeman 1978; Eeckman and Freeman
1991). Freeman underscored that the simplicity and general-
ity of the elements comprising his model make it applicable
to other neural systems (Freeman 1987). Similar ideas were
developed by Lopes Da Silva et al. and led to the design
of a lumped-parameter model, which was able to generate
an alpha rhythm (Lopes da Silva et al. 1974, 1976). Start-
ing with the lumped-parameter model, Jansen et al. devel-
oped a biologically inspired mathematical framework for
simulating spontaneous electrical activities of neuron assem-
blies as recorded by an EEG, with a particular emphasis on
alpha activity (Jansen et al. 1993; Jansen and Rit 1995). The
framework has been used to explain epilepsy-like brain activ-
ity (Wendling et al. 2000), as well as various narrow-band
EEG oscillations, ranging from the delta to the gamma fre-
quency bands (David and Friston 2003). Nevado-Holgado et
al. (2012) developed a multi-objective genetic algorithm that
can estimate parameters of a neural mass model from clinical
EEG recordings. Estimating the parameters of neural mass
models generally involves the Bayesian inversion of dynamic
causal models using standard variational system identifica-
tion techniques.
Much scientific work has been devoted to the understand-
ing of the behavior of neural mass models. Examples include
the derivations of stability conditions of the synchronized
state in arbitrary networks (Belykh et al. 2005; Hennig and
Schimansky-Geier 2008) as well as the derivations of the
equations for the synchronization manifold (DeMonte et al.
2003; Jirsa 2008) for heterogeneous networks. More gen-
eral, when the system exhibits strong deviations from the
synchronized state, mode decomposition techniques become
more appropriate (Assisi et al. 2005; Stefanescu and Jirsa
2008).
The bifurcation theory of nonlinear systems is a useful
tool for investigating the dynamical behavior in neural mass
models. For example, Grimbert and Faugeras (2006) used
bifurcation analysis to investigate the effect of the input to a
NMM on the dynamics of the model and found that rhythmic
activities such as alpha rhythm and epileptic wave are related
to the structure of a set of periodic orbits and their bifurca-
tion. Touboul et al. (2011) proposed a general framework
for studying the bifurcations of neural mass models defined
by ordinary differential equations. Breakspear et al. (2005)
explained the essential difference between the topology of
the global bifurcation diagram of absence and tonic-clonic
seizures.
NMMs are now used routinely in the dynamic causal mod-
eling of invasive and noninvasive electrophysiological time
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Biol Cybern (2014) 108:747–756
series (David et al. 2006). In this context, NMMs are used
as forward models of hidden neuronal states (that are then
mapped to sensors). This provides a complete generative
model of observed electrophysiological signals. Dynamic
causal modeling (DCM) has been applied to numerous para-
digms in the cognitive neurosciences using both EEG, MEG
(David et al. 2006; Garrido et al. 2007; Kiebel et al. 2008,
2009), and LFP recordings (Moran et al. 2008). Generally,
dynamic causal models use multiple NMMs that are cou-
pled with extrinsic connections. Furthermore, they incorpo-
rate explicit delay parameters accounting for within (intrin-
sic) and between (extrinsic) neural mass connections (Kiebel
et al. 2006). In this paper, we focus on a single neural mass
with multiple populations and provide a quantitative bifur-
cation analysis of intrinsic temporal delays.
Animal studies suggested the existence of multiple thala-
mocortical and corticothalamic pathways, yielding a range
of thalamocortical delays from 0.1 to 5 ms and longer corti-
cothalamic delays from 1 to 30 ms in the mouse (Salami et al.
2003; Liu et al. 2001), rat (Sawyer et al. 1994; Beierlein and
Connors 2002), rabbit (Swadlow and Weyand 1981; Swad-
low 2003), cat (Wilson et al. 1976; Tsumoto et al. 1978;
Tsumoto and Suda 1980; Miller et al. 2001; Sirota et al.
2005), and macaque monkey (Briggs and Usrey 2007). Scal-
ing the above data to human brain size (Robinson et al. 2004),
one can estimate delays of roughly 10 ms for the human thala-
mocortical pathway and a few tens of milliseconds for the
corticothalamic pathway. The work of Roberts and Robin-
son (2008) indicated that seizure waveforms in the cortex and
thalamus depend on the axonal and synaptodendritic delays.
Previous work of models of brain has not explicitly taken
into consideration delays in connections. Although delays
make the analysis more difficult, their effects may be impor-
tant for the applications. Research on Hopfield-type neural
networks with delays first introduced by Marcus and Wester-
velt (1989) has also shown that delay can modify the global
dynamic in interesting ways. Transmission delay seems to
play a significant role in integration of information arriving to
a single neuron in different spatial and temporal windows and
also at the network level in interneuron communication. The
theoretical study of the dynamics of simple units organized
into networks with delayed couplings revealed a rich vari-
ety of possible scenarios of transition to a global oscillatory
behavior induced by the delay (Bungay and Campbell 2007;
Campbell et al. 2005; Guo 2005, 2007; Song et al. 2005; Yuan
and Campbell 2004; Yuan 2007; Wei and Velarde 2004). The
emerging oscillations can exhibit different patterns sensitive
to the delay. Since then, delays have been inserted into various
simple neural networks. Campbell et al. (2004) investigated
the stability and bifurcations in the delayed neural network
of two coupled three-neuron subnetworks.
In this work, we modify the model proposed by Jansen
et al. by adding a time delay in the inhibitory feedback loop
Biol Cybern (2014) 108:747–756 749

to simulate signal transmission among neurons, resulting in a density of action potentials, which is represented by a non-
neural mass model with time delay. The new model is able to linear sigmoid function
reproduce several different types of EEG activities including vmax
alpha wave, interictal EEG, and ictal EEG, with all para- Sigm(v) = (3)
1 + er (v0 −v)
meters (excepting extrinsic inputs) being kept constant and
equal to standard values. Through an analysis of the influ- Here vmax is the maximum firing rate of the families of neu-
ence of the time delay on model’s dynamical behaviors, we rons, v0 is the value of the potential for which a 50% firing
succeed in showing that a transmission delay can make the rate is achieved, and r is the slope of the sigmoid at v0 ; v0 can
model to produce seizure-like activity. be regarded either as a firing threshold or as the excitability
of the populations. Interactions between the main cells and
interneurons are summarized in the model via four connec-
2 Model description tivity constants C1-C4, accounting for the average number
of synaptic contacts.
As shown in Fig. 1, the model consists of three subsets of A fast rise time and a slower decay are usually used to
neurons, namely the main cells (i.e., pyramidal cells), the characterize postsynaptic potentials. When we model post-
excitatory interneurons, and the inhibitory interneurons. The synaptic potentials, the model which we most usually use
influence of neighboring areas is represented by an excitatory is the exponential model h(t) = e−αt u(t) where u(t) is the
input p(t) (modeled by band-limited white noise) that glob- Heaviside step function. In Jansen and Rit model (Jansen
ally describes the average density of afferent action poten- and Rit 1995), the rise phase of the postsynaptic potential
tials. The model output y(t) corresponds to the sum of post- is neglected and an incoming spike is considered to have an
synaptic potentials in activated pyramidal cells, which can in instantaneous effect on the membrane potential of the postsy-
turn be used to synthesize EEG activity. naptic cell. This corresponds to neglecting the transmission
In our model, each subset of neurons involves two opera- delays and the fast dynamics of the synapse. This approxima-
tors. The first transforms the average pulse density of action tion is widely applied because it is simpler and could catch
potentials into an average postsynaptic membrane potential, the essential of the phenomenon one wants to simulate. How-
described by the response functions given by ever, it seems that in Jansen and Rit model, the rise phase of
 the postsynaptic potential that creates a delay in the synaptic
Aate−at t ≥ 0 transmission is essential to generate the oscillatory activity
h e (t) = (1)
0 t <0 (Touboul et al. 2011).
To simulate the signal transmission delay among neurons,
for the excitatory case and
 we add a time-delay unit δ(t − τ ) in the inhibitory feedback
Bbte−bt t ≥ 0 loop (see Fig. 1). δ(t − τ ) is the unit impulse function, which
h i (t) = (2) is the response functions of the time-delay unit.
0 t <0
The model is formulated as a set of first-order nonlinear
for the inhibitory case, where A and B determine the delay differential equations as follows:
maximum amplitude of the excitatory and inhibitory post- ⎧
synaptic potentials, respectively. The parameters a and b ⎪
⎪ ẏ0 (t) = y3 (t);
⎪
⎪
lump the characteristic decays in the synaptic transmission ⎪
⎪
⎪ ẏ1 (t) = y4 (t);
⎪
together. The second operator transforms the average mem- ⎪
⎪
⎪
⎪
⎨ ẏ2 (t) = y5 (t);
brane potential of a neuron population into an average pulse
⎪
⎪ ẏ3 (t) = AaSigm[y1 (t) − y2 (t − τ )] − 2ay3 (t) − a 2 y0 (t);
⎪
⎪
⎪
⎪
⎪
⎪ ẏ4 (t) = Aa { p(t) + C2 Sigm[C1 y0 (t)]} − 2ay4 (t) − a 2 y1 (t);
C2 Sigm C1 ⎪
⎪
⎪
⎪
⎩ ẏ5 (t) = Bb {C4 Sigm[C3 y0 (t)]} − 2by5 (t) − b2 y2 (t);

+ + (4)
⊗
y1
p (t ) he (t )
+
⊗
y
Sigm he (t ) with the output of the system given by y(t) = y1 (t) − y2
−
hi (t )
(t − τ ).
y2 (t − τ ) The standard values of the parameters are determined
D anatomically to be (Jansen and Rit 1995): A = 3.25mV, a =
C4 δ (t − τ ) Sigm C3 100s−1 , B = 22mV, b = 50s−1 , vmax = 5s−1 , r =
0.56mV−1 , v0 = 6mV, C1 = 135, C2 = 0.8C1, C3 =
Fig. 1 The time-delay neural mass model C4 = 0.25C1.

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750 Biol Cybern (2014) 108:747–756

This set of equations is solved using a delay differential p and y being related through Eq. (6).
equations solver (dde23, based on a 2–3’rd order Runge-
Kutta method) in MATLAB. We focus on the output variable 3.2 Stability conditions and bifurcations
y(t) = y1 (t)− y2 (t −τ ) to represent the membrane potential
of the main family of neurons (see Fig. 1). The output of the As we mentioned in the previous section, a steady-state solu-
model y(t) will be used to emulate an EEG signal. tion (equilibrium) of (4) does not depend on the time delay.
But the stability conditions of the steady-state solution (equi-
3 Methods librium) will be affected by the time delay. The stability of a
steady-state solution S(y) of (4) is determined by the roots
We use numerical methods for the bifurcation analysis of of the characteristic equation.
DDEs to analyze bifurcation in our time-delay model. A In order to study the behavior of the model near the equilib-
detailed description of these methods can be found in refer- rium points, we linearize it and calculate its Jacobian matrix.
ences (Luzyanina 1997; Luzyanina and Roose 1996; Engel- We compute the eigenvalues of Jacobian matrix along the
borghs et al. 2000). curve (6) to analyze the stability of the family of equilibrium
points. More detailed information about Jacobian matrix
3.1 Steady-state solutions
and the computing about the eigenvalues can be found in
(Luzyanina 1997). The equilibrium points are asymptotically
A steady-state solution (equilibrium) of Eq. (4) does not
stable provided that all the roots of Jacobian matrix have strict
depend on the time delay. Hence, (4) and the system of ODEs,
negative real part. The stability of the steady state can change
obtained from Eq. (4) by putting the delay to zero, have the
whenever roots of Jacobian matrix cross the imaginary axis.
same steady-state solutions (Engelborghs et al. 2000).
The corresponding bifurcation point is (generically) a saddle-
Let Y = (y0 , . . ., y5 )T , the model (4) can be described as
node bifurcation when a real root crosses through zero and
Ẏ = f (Y, p) a Hopf bifurcation when a complex pair of roots crosses the
imaginary axis. In the former case, a branch of anharmonic
where f is the smooth map from R6 to R6 given by (4) and
oscillation solutions arises from the bifurcation point. In the
p is a parameter when time delay τ = 0.
latter case, a branch of periodic harmonic oscillation solu-
We look for the points Y where Ẏ = f (Y, p) = 0 (called
tions arises from the bifurcation point. The results (when the
equilibrium points). Writing Ẏ = 0 we obtain the system of
time delay τ = 0) are summarized in Fig. 3 (the S-shape curve
equations as follows:
⎧ in the bifurcation diagram). The solid portions of curve cor-
⎪
⎪ y0 = aA Sigm[y1 − y2 ] y3 = 0 respond to stable (all eigenvalues have a negative real part)
⎨
y1 = aA ( p + C2 Sigm[C1 y0 ]) y4 = 0 (5) and the dashed ones to unstable equilibrium points (some
⎪
⎪ eigenvalues have a positive real part). When the value of
⎩
y2 = b C4 Sigm[C3 y0 ]
B
y5 = 0 time delay τ is changed, the location of bifurcation points
which leads to the (implicit) equation of the one-parameter will be different (see Figs. 4, 5, 6).
family of equilibrium points in the ( p, y = y1 − y2 ) plane:
 
A A A
y = p + C2 Sigm C1 Sigm(y) 4 Results
a a a
 
B A 4.1 Influence of delay on dynamics behavior of the
− C4 Sigm C3 Sigm(y) (6)
b a time-delay model
As mentioned before, y = y1 − y2 can be thought of as
representing the EEG activity of the unit and p is our para- For the band-limited white noise, its mean and variance were
meter of interest. We plot the curve defined by (6) in Fig. 3 adjusted to obtain a rate ranging from 120 to 240 pulses
(the S-shape curve in the bifurcation diagram). per second, for which the time-delay model generates an
The coordinates of the singular points cannot be written output reminiscent of alpha activity when parameters are set
explicitly as functions of p, but every singular point is com- to their standard values and there is no delay (τ = 0), as shown
pletely determined by the quantity y. More precisely, the in Fig. 2a. Spiked-type activity appears for increased values
coordinates of every singular point y have the following form: of the time delay τ . From Fig. 2b, c, we can see that alpha
 activity and spiked-type activity appear alternately when the
A A A time delay is in the range 0.1 ms < τ < 0.5 ms. For larger
S(y) = Sigm(y) ( p + C2 Sigm[C1 Sigm(y)])
a a a time delays, the time-delay model produces sustained spiked
T
B A activity, such as is typically encountered during seizures (see
C4 Sigm[C3 Sigm(y)] 0 0 0 (7) Fig. 2d).
b a

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15 cycles (Kuznetsov 1998; Seydel 2009). Depicting the oscilla-

tory behavior in the output of neural mass models is therefore
10
y(mV)

closely related to studying its bifurcations.

5
The dynamics that result from an input p in a NMM
without time delay is studied in (Grimbert and Faugeras
0 2006). Figure 3 shows a bifurcation diagram from our
0 2 4 6 8 10
t(s) model whenτ = 0, while Fig. 4 shows the conditions for
p = 50, 100, 125, 150.
(a)
Figures 5 and 6 show bifurcation diagrams of the time-
15 delay model when τ = 0.1 ms and τ = 5 ms. From
Fig. 5, we can see that the bifurcation diagram of the model
10 is similar to that of the non-delay case (see Fig. 3), where
y(mV)

the differences are restricted to the location of bifurcation

5
points. Hopf bifurcation happens in the time-delay model
for p = 67.24 and p = 340.32 when τ = 0.1 ms, and
0
0 2 4 6 8 10 in the non-delay model for p = 89.93 and p = 315.7. A
t(s) saddle-node bifurcation appears in the time-delay model for
(b) p = 113.58 and p = 140.43 when τ = 0.1 ms, and in the
non-delay model for p = 113.58 and p = 137.39. Further-
15
more, the p value of the second saddle-node bifurcation is
10 larger with increases in the time delay τ , p = 143.62 when
y(mV)

τ = 0.2 ms and p = 149.45 when τ = 0.4 ms. The range

5 where spiked epileptic-like limit cycles appear is broader,
with spiked activity increasingly prominent with a larger
0
0 2 4 6 8 10 delay τ . For much larger values of time delay, we observe a
t(s) new kind of bifurcation diagram (see Fig. 6). In this regime,
(c) the model has only one stable state for each value of p, and
15

10 12
y(mV)

5
10
0
0 2 4 6 8 10 8
t(s)
(d) 6
y(mV)

Fig. 2 Different types of activities produced by the time-delay model. 4

a τ = 0. b τ = 0.1 ms. c τ = 0.5 ms. d τ = 5 ms

2
The above described phenomena could explain the under-
lying cause of a seizure disorder, wherein a signal trans- 0
mission delay among neurons may cause seizures when the
degree of the time delay of transmission reaches a certain -2
-50 0 50 100 150 200 250 300 350 400
value. p

Fig. 3 Bifurcation diagram of the time-delay model when τ = 0. In

4.2 Time-delay model analysis using bifurcation diagrams
Bifurcation diagrams can describe the asymptotically invari-
ant behavior of a nonlinear system. With smooth changes in
parameters, the dynamic behavior of the system may undergo
sudden and drastic changes known as bifurcations. Often,
this corresponds to the appearance or disappearance of limit
the bifurcation diagram, solid lines represent stable and dashed lines
represent unstable states. Bifurcations are indicated by white circles
for supercritical Andronov-Hopf, stars for saddle-node and diamonds
for subcritical Andronov-Hopf bifurcations. The dark gray oval region
between the white circles is Hopf cycle, alpha-like limit cycles appear
for p ∈[89.83, 315.7]. The light gray region between the stars is spike-
like limit cycles for p ∈[113.58, 137.39]. The dashed vertical lines
correspond to the examples of the dynamics in Fig. 4

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752 Biol Cybern (2014) 108:747–756

(a) (b) 16

20 20 14

10 10
2

2
12
y

y
0 0
20 40 10
0.1 0.2
10 0.05 20 0.1
y1 0 0 y0 y1 0 0 y0 8

y(mV)
6
(c) (d)

20 4
0.12
10 2
2

0.1
y

0 0.08 0
40 22.5
0.2 22 16
20 0.1 21.5
y1 0 0 y0 y 1 21 14y -2
2 0 100 200 300 400 500
p
Fig. 4 Dynamic behaviors of the time-delay model for several values
of input parameter p when τ = 0. a Two equilibrium points coexist for Fig. 6 Bifurcation diagram of the time-delay model when τ = 5ms.
p = 50, shown as black dot and star. b An alpha-like activity (ring) In this case, the time-delay model present a saddle-node (star, for p =
and an equilibrium point (star) coexist when p = 100. c Alpha-like 113.58) bifurcation and a Hopf bifurcation (white cycle, p = 501.26).
activity (smaller ring) and epileptic-like spiked activity (larger ring) This branch of spiked epileptic-like limit cycles (the light gray region)
coexist when p = 125. d There is only an alpha-like activity (ring) when caused by saddle-node bifurcation smoothly connects to a branch of
p = 140. (The values of the parameter p that correspond to subfigures limit cycles (the dark gray region), corresponding to Alpha-like activ-
a–d are indicated by thin vertical lines in Fig. 3) ity when the input p increases, and eventually vanishing on a Hopf
bifurcation (white cycle, p = 501.26). The spiked epileptic-like limit
12
cycles are more prominent and are the only one available in a wide
range (the light gray region). Alpha-like limit cycles appear when the
values of p is larger (the dark gray region), and between the two dashed
10 vertical lines is the transition from spiked epileptic-like limit cycles to
alpha-like limit cycles

is severely truncated. Moreover, spike-like epileptic activity

6
can no longer coexist with alpha-like activity, which is then
y(mV)

the only type of behavior observed, over a broad interval of

4 p values (the light gray region in Fig. 6).
Figures 7 and 8 show the bifurcation diagrams of the model
2 over smooth changes of the time delay τ when the input of
the model is p = 150 and p = 170, respectively. The bifur-
0 cation analysis with regards to the delay reveals that there
are two stable states (i.e., alpha-like limit cycles and the
-2
spiked epileptic-like limit cycles). When the delay τ changes
-50 0 50 100 150 200 250 300 350 400 smoothly, the behavior of the model exhibits a sudden change
p from alpha-like limit cycles to spiked epileptic-like limit
Fig. 5 Bifurcation diagram of the time-delay model when τ = 0.1 ms. cycles when τ = 0.42 ms for p = 150 and τ =1.03 ms for
Alpha-like limit cycles appear for p ∈[67.24, 340.32], while spiked p = 170, respectively. We also studied bifurcations of the
epileptic-like limit cycles appear for p ∈[113.58, 140.43]. Two Hopf model when the value of p ranges from 120 to 240 and find
bifurcations (white cycles) happen in the time-delay model for p = that, as the value of p increases, the value of the time delay
67.24 and p = 340.32. Saddle-node bifurcations (stars) happen for
p = 113.58 and p = 140.43 τ at which the behavior of the model changes from alpha-
like to spiked epileptic-like limit cycles is increased. When
τ = 5 ms, spiked epileptic-like limit cycles appear for all p
the phenomenon that alpha-like activity coexists with spike- values in the range from 120 to 240.
like epileptic activity disappears. The range where spike-like Figure 9 show the three-dimensional bifurcation diagram
epileptic activity can occur is broader (the light gray region (in y, p and τ ) of the time-delay model for p ∈[1, 550]
in Fig. 6), and the parameter space for possible alpha activity and τ ∈ [0.1, 5 ms] which summarizes the various two-

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Biol Cybern (2014) 108:747–756 753

14 14

12 12

10
10

8
8
y(mV)

y(mV)
6
4
4
2
2
0
0
-2
1 2 3 4 5
τ x 10
-3 -2
1 2 3 4 5
(a)
τ x 10
-3

Fig. 8 Bifurcation diagram of the time-delay model when p = 170.

Alpha-like limit cycles appear for τ ∈ [0.1, 1.03 ms] (the dark
25 gray region), while spiked epileptic-like limit cycles appear for τ ∈
[1.04, 5 ms] (the light gray region). Dynamic behaviors of the time-
20 delay model change from alpha-like activity to spike-like activity when
τ = 1.03 ms
15
y2

10

0
30
20 0.2

10 0.1

y1 0 0 y0

(b)
Fig. 7 a Bifurcation diagram of the time-delay model when p = 150.
Alpha-like limit cycles appear for τ ∈ [0.1, 0.42 ms] (the dark
gray region), while spiked epileptic-like limit cycles appear for τ ∈
[0.43, 5 ms] (the light gray region). Dynamic behaviors of the time-
delay model change from alpha-like activity to spiked epileptic-like Fig. 9 A three-dimensional bifurcation diagram (in y, p and τ ) of the
activity when τ = 0.42 ms. b Dynamic behaviors of the time-delay time-delay model for p ∈[1, 550] and τ ∈ [0.1, 5 ms]
model for τ = 0.2 ms and τ = 4 ms when p = 150. Alpha-like activ-
ity (smaller ring) and spike-like epileptic activity (larger ring) is for
τ = 0.2 ms and τ = 4 ms, respectively
Jansen et al. A time delay in the inhibitory feedback loop
is used to simulate signal transmission among neurons. A
dimensional bifurcation. From this figure we can see the
detailed analysis of the dynamic properties of our time-delay
dynamical behavior in our time-delay model clearly.
model has been performed by means of bifurcation diagrams.
These diagrams are a function of two key parameters, namely
the input of the model p and the time delay τ .
5 Discussion One aim of this work was to investigate the effect of a
time delay on the dynamical behavior of the model, which
We have presented a neural mass model incorporating a time produced several findings: When we consider p as a bifur-
delay that is based on the neural mass model as proposed by cation parameter of the model with τ = constant, we find

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that there are three possible stable states, i.e., stable equilib-
rium points, spiked oscillations, and harmonic oscillations
(see Figs. 3, 4, 5, 6). If the value of τ is relatively small, there
is more than one possible system state for the same p value
(see Figs. 3, 4, 5). If we increase the value of the delay τ ,
we find that there is only one possible stable state for each p
value. The time delay can change the location of bifurcation
points, and higher values of τ lead to a broader range where
spiked-type activity can occur and spiked oscillations feature
more prominently (see Fig. 6).
When we consider τ as a bifurcation parameter in the
model with p = constant, we find that there are two possible
stable states, i.e., alpha-like activity and spiked oscillations
(see Figs. 7, 8). The alpha-like activity appears for low values
of the time delay τ , while the spiked-type activity appears for
higher values of τ . The model exhibits a sudden change in
behavior from alpha-like limit cycles to spiked epileptic-like
limit cycles for certain values of τ . A relatively high value of
the input p requires a large time delay τ to produce a change
from alpha-like limit cycles to the spiked epileptic-like limit
cycles (Figs. 7, 8).
We can examine the model’s output in Fig. 2 from a math-
ematical perspective. Band-limited white noise varying from
120 to 240 Hz was used as the input of the model. With no
time delay (τ = 0), alpha-like limit cycles predominate in
the domain of our chosen input p values (Fig. 3). There-
fore, at every instant, the output trajectories will tend to coil
around an alpha-like limit cycle corresponding to p = p(t).
We therefore observe oscillations of a constant frequency
and varying amplitude leading to the alpha-like wave in
Fig. 2a. As the time delay τ is increased, the range where
epileptic-like limit cycles appear is broadened, and gradu-
ally the spiked-type activities prevail. We see in Fig. 2b, c that
alpha-like activity and spiked activity appear alternately. As
τ is increased continuously, spiked epileptic-like limit cycles
appear for all input values p to the model. Consequently, we
see sustained spiked-type activity in Fig. 2d, which is of the
sort that may be encountered in EEGs at the onset or during
the occurrence of seizures.
Wendling et al. used Jansen’s model with altered parame-
ters to produce epileptiform signals (Wendling et al. 2000).
Their experiments show that a certain ratio that is related
to the balance between excitatory and inhibitory process-
ing directly influences the type of signal dynamics gener-
ated by the model. In the present work, a time delay in the
inhibitory feedback loop can also make the model produce
epileptiform signals, with all parameters (excepting extrinsic
inputs) being kept constant and equal to standard values. As
τ increases, spiked output activity first appears sporadically
(for τ ≥ 0.1 ms), then frequently (for τ ≥ 0.5 ms), and
finally rhythmically (for τ =5 ms). Our findings might shed
light on the root cause for seizure disorders.
123
Biol Cybern (2014) 108:747–756
6 Conclusions
Neural mass models are widely used to simulate highly com-
plex EEG activity. The bifurcation diagram is a useful tool
to describe the behavior of these models. In this work, in
view of the time delay that occurs in real signal transmission
between neurons, we propose a novel neural mass model that
incorporates a time-delay feedback loop. An analysis of the
influence of a delay on the dynamical behavior of the model
shows that transmission delays could make the model pro-
duce epileptiform signals. We have provided a description of
the new model’s behavior via bifurcation diagrams. In our
time-delay model, we find that there are three possible stable
states, i.e., stable equilibrium points, spiked-type activity,
and alpha-like activity. The alpha-like activity appears for
low values of delay, while the spiked-type activity appears
for higher values of delay when the input parameter p is kept
constant. High values of p require longer delays to cause a
change from alpha-like limit cycles to spiked epileptic-like
limit cycles. These findings indicate that a signal transmis-
sion delay among neurons may cause seizure-like activity in
the brain when the degree of the delay reaches a certain value.
Further investigations into the bifurcations of this time-delay
neural mass model might provide a theoretical foundation for
the neurodynamics of epileptic seizures and the brain’s non-
linear electrical activities.
Acknowledgments This work was supported by the Key Pro-
gram of Natural Science Foundation of Shandong Province (No.
ZR2013FZ002), the Program of Science and Technology of Suzhou
under Grant ZXY2013030, and the Independent Innovation Founda-
tion of Shandong University under Grant 2012DX008.
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