Input Response of Neural Network Model with Lognormally
Distributed Synaptic Weights
Yoshihiro Nagano
1
, Ryo Karakida
1,2
, Norifumi Watanabe
3
, Atsushi Aoyama
4
, and Masato Okada
1,5+
1
Graduate School of Frontier Sciences, The University of Tokyo, Kashiwa, Chiba 277-8561, Japan
2
Research Fellow of the Japan Society for the Promotion of Science, Chiyoda, Tokyo 102-0083, Japan
3
School of Computer Science, Tokyo University of Technology, Hachioji, Tokyo 192-0914, Japan
4
Faculty of Environment and Information Studies, Keio University, Fujisawa, Kanagawa 252-0882, Japan
5
RIKEN Brain Science Institute, Wako, Saitama 351-0198, Japan
(Received February 19, 2016; accepted May 9, 2016; published online June 6, 2016)
Neural assemblies in the cortical microcircuit can sustain irregular spiking activity without external inputs. On the
other hand, neurons exhibit rich evoked activities driven by sensory stimulus, and both activities are reported to
contribute to cognitive functions. We studied the external input response of the neural network model with lognormally
distributed synaptic weights. We show that the model can achieve irregular spontaneous activity and population
oscillation depending on the presence of external input. The firing rate distribution was maintained for the external input,
and the order of firing rates in evoked activity reflected that in spontaneous activity. Moreover, there were bistable
regions in the inhibitory input parameter space. The bimodal membrane potential distribution, which is a characteristic
feature of the up-down state, was obtained under such conditions. From these results, we can conclude that the model
displays various evoked activities due to the external input and is biologically plausible.
1. Introduction
Neural assemblies in the cortical microcircuit can sustain
irregular low-firing rate spiking activity without any external
inputs. Such firing is referred to as spontaneous activity, and
the spikes of which are reported to be irregular, have low
firing rate, and are non-periodic.
1–4)
Teramae et al. proposed
the strong-sparse and weak-dense (SSWD) model,
5)
which
reproduces such irregular spontaneous activity
1–4,6)
by using
the physiological findings that the distribution of inter-
neuronal synaptic weights follows a lognormal distribu-
tion.
7–9)
Having a few strong and many weak synapses, the
SSWD model can generate noisy spikes internally and
maintain spontaneous firings.
On the other hand, neurons exhibit rich evoked activities
driven by sensory stimulus or top-down signals from the
higher cortical area. For instance, it has been reported that
visual area V4 shows population oscillation in the range of
40–100 Hz caused by sensory visual stimulus.
10)
Such activity
is called gamma oscillation. These spontaneous activity and
population oscillation are general phenomena observed in
various cortical areas. Specifically, both spontaneous activity
6)
and population oscillation
10)
were reported in V4. For these
two phenomena, recent experimental findings suggest that the
firing pattern of spontaneous activity constrains that of evoked
activity,
11–13)
which is known as the sampling hypothesis.
14)
Moreover, the gamma-band population oscillation is believed
to be linked with high-level cognitive functions such attention,
memory, perception, and object-binding problem.
15)
For
figuring out these experimental results and the theoretical
hypothesis, it is important to investigate the neural network
model which achieves both spontaneous and evoked activ-
ities. There are theoretical works
16,17)
investigating the
transition between irregular spontaneous activity and evoked
population oscillation using a randomly connected neural
network model. However, the models proposed in these works
cannot sustain irregular spontaneous activity without relying
on any external inputs. From biological experimental results,
the irregular spontaneous activity is considered to be
generated internally. Therefore, the SSWD model is expected
to be more biologically plausible, but the input response of the
model remains to be uncovered.
In this study, we first revealed that the SSWD model, which
sustains irregular spontaneous firing without external input,
can generate input-driven population oscillation. The oscil-
lation frequency was 70–100 Hz, which corresponds to the
gamma-band oscillation. Next, we found that the firing rate
distribution was maintained for external input, and the order
of firing rates in evoked activity strongly correlated with that
in spontaneous activity, consistent with the physiological
results by Mizuseki et al.
18)
Finally, we revealed that when the
inhibitory external input was injected to the model, there were
bistable regions in the input parameter space. The circuit
settled into a firing state or a no-firing state according to the
initial firing state. Moreover, bimodal membrane potential
distribution was obtained under such conditions, and the
model enables the physiologically reported up-down
state.
19–23)
From these results, we can conclude that the
SSWD model displays various evoked activities caused by
external input and is biologically plausible.
2. Model
2.1 SSWD model
We used the SSWD model proposed by Teramae et al.
5)
It
is known that the model shows irregular spontaneous firing
without externally injected background noise. The dynamics
of neurons in the model are formulated as an extension of the
leaky integrate-and-fire neuron model. The dynamics of the
membrane potential v and excitatory and inhibitory synaptic
conductances g
E
and g
I
normalized by the membrane
capacitance are written as
dv
dt
¼
1
mX
ðv V
L
Þ g
E
ðv V
E
Þ g
I
ðv V
I
Þ; ð1Þ
dg
X
dt
¼
g
X
S
þ
X
j
G
X;j
X
s
j
ðt s
j
d
j
Þ
þ G
X;ext
X
s
ext
ðt s
ext
Þ; ð2Þ
Journal of the Physical Society of Japan 85, 074001 (2016)
http://doi.org/10.7566/JPSJ.85.074001
074001-1
©
2016 The Physical Society of Japan