IEEE TRANSACTIONS ON CIRCUITS AND SYSTEMS—II: EXPRESS BRIEFS, VOL. 65, NO.
5, MAY 2018 577
Development and Applications of Biomimetic
Neuronal Networks Toward BrainMorphic
Artificial Intelligence
Timothée Levi , Takuya Nanami, Atsuya Tange, Kazuyuki Aihara, and Takashi Kohno
Abstract—This brief presents the brainmorphic artificial
intelligence (BMAI) project. The main goal is to generate a novel
type of neuromorphic computing systems including novel algo-
rithms and devices, which can achieve very high performance of
artificial intelligence (AI) information processing with low power
consumption and which can be very close to biological systems.
To reach this goal, we developed biomimetic neural networks.
Two systems have been designed, one analog chip and one digi-
tal system into FPGA. We present in this brief two applications of
these biomimetic neural networks, one in AI with a pattern recog-
nition algorithm and one in neuroscience for understanding the
hearing system of Drosophila for designing a new asynchronous
low-power sensor system in the future.
Index Terms—Artificial intelligence, biomimetic neural
network, neuromorphic engineering, silicon neuron.
I. I NTRODUCTION
EUROMORPHIC systems are designed by mimicking
N or being inspired by the nervous system, which real-
izes robust, autonomous, and power-efficient information pro-
cessing by highly parallel architecture. The purpose of the
Brainmorphic artificial intelligence project (BMAI), is to gen-
erate a novel type of neuromorphic computing systems includ-
ing novel algorithms and devices, which can achieve very
high performance of Artificial Intelligence (AI) information
processing with low power consumption and close resem-
blance to biological systems. Using biomimetic neural network
systems, we construct a novel fundamental technology of
the information processing by developing the Brainmorphic
AI system which can execute fast autonomous informa-
tion processing with low energy. Two main objectives are
raised: 1) understanding and simulating biological intelligence;
Manuscript received February 26, 2018; revised April 5, 2018; accepted
April 5, 2018. Date of publication April 9, 2018; date of current version
May 1, 2018. This work was supported in part by NEC Corporation, in part
by the JST PRESTO program, WPI, MEXT Japan, in part by the JST CREST
program, and in part by JSPS KAKENHI under Grant 15H05707 and Grant
17K19450. This brief was recommended by Associate Editor J. M. de la Rosa.
(Corresponding author: Timothée Levi.)
T. Levi, T. Nanami, A. Tange, and T. Kohno are with the
Institute of Industrial Science, University of Tokyo, Tokyo 153-8505,
Japan (e-mail: levi@sat.t.u-tokyo.ac.jp; nanami@sat.t.u-tokyo.ac.jp; tange@
sat.t.u-tokyo.ac.jp; kohno@sat.t.u-tokyo.ac.jp).
K. Aihara is with the Institute of Industrial Science, University of Tokyo,
Tokyo 153-8505, Japan, and also with the WPI-IRCN, UTIAS, University of
Tokyo, Tokyo 153-8505, Japan (e-mail: aihara@sat.t.u-tokyo.ac.jp).
Color versions of one or more of the figures in this paper are available
online at http://ieeexplore.ieee.org.
Digital Object Identifier 10.1109/TCSII.2018.2824827
1549-7747 c 2018 IEEE. Personal use is permitted, but republication/redistribution requires IEEE permission.
See http://www.ieee.org/publications_standards/publications/rights/index.html for more information.
2) designing new low-power neuromimetic systems for AI
applications.
The biomimetic neural network is a neuromorphic system
with a most detailed level of analogy to the nervous system. It
is a network of silicon neurons connected via silicon synapses
and plasticity rules. It can be silicon based [1] or microfluidic
based [2]. To present the different hardware implementations
of these systems [3], we rely on the review of neuromorphic
architectures published in 2010, [4] and we enrich it with other
articles. It will allow us to show the growing interest in neu-
romorphic systems these past/latest years, and their utilities
and their potential. Indeed, their applications extend to high-
energy physics, image processing (object / image / pattern
recognition, image segmentation, video processing), robotics,
acoustic or olfactory recognition and understanding of the ner-
vous system. Hardware implementations are divided into two
major categories: analog implementation (based on dedicated
chips) and digital implementation (based on FPGA, micro-
processors, microcontrollers or neurochips). We focus here on
biomimetic and non-bio-inspired systems. The very first plat-
forms appeared around twenty years ago [5]–[7]. In the case
of analog implementations, some systems implement multi-
compartmental models [8], conductance models [9] or with
threshold models [10], [11]. These platforms start from an
analog computing core, usually an ASIC, which describes the
electrophysiological activity of the neuron. The architecture of
the different platforms results from a compromise between the
computational cost and the complexity of the model (directly
correlated to biological plausibility). The integration of plas-
ticity and synapses is usually done by a digital map that makes
the link between different analog chips. As for the digital
implementation, biomimetic neural network implementations
on FPGAs are generally used for pattern recognition, image
segmentation, video image processing and video analysis [12].
The last point of the discussion concerns the size of artifi-
cial networks. Indeed, neurons are organized in networks of
various sizes. Biological plausibility is a constraint on the max-
imum possible size of the network. To obtain large networks
of neurons (population of 1000 neurons or more), it is
necessary to:
• implement a simple neural model and a simple synapse
model. Reference [13] presents an implementation on an ASIC
containing one million LIF (Leak Integrate and Fire) neurons
and 256 million synapses.
• perform accelerated neural network calculations such as
the SpiNNaker [14] platform with a multiprocessor architec-
ture. With over one million cores, and one thousand simulated
578 IEEE TRANSACTIONS ON CIRCUITS AND SYSTEMS—II: EXPRESS BRIEFS, VOL. 65, NO. 5, MAY 2018
neurons per core, the machine will be capable of simulating
one billion neurons. We also have the BrainScaleS system
which is a stack of modules composed of 20 wafers integrating
448 neuromorphic chips and a routing system. Each module
emulates the activity of 512 neurons and 115,000 synapses,
performing calculations 10 000 times faster than biological
time [15]. However, all these platforms are not working in bio-
logical real-time but accelerated time and then are not a good
option to perform bio-hybrid experiments. Another main draw-
back is that the neuron model is bioplausible but these systems
do not allow axonal delay, biomimetic plasticity and synap-
tic noise [16]. All of these different points are mandatory for
reproducing the biological dynamics of living neural networks.
With the emergence of real-time neuromorphic platforms,
significance of bio-hybrid experiments is increasing not only
for the development of neuromorphic biomedical devices [3],
but also for elucidating the mechanisms of the information
processing in the nervous system by the approach of “analysis
by synthesis”. Reference [17] introduces the term “neurobio-
hybrid” for one system formed by at least living neurones
and at least one artificial entity that establish uni or bi-
directional communications between them. The characteristics
of the systems for neurobiohybrid experiments are biolog-
ical real-time, complex neuron models and plasticity that
reproduce temporal neuronal activity and / or action poten-
tial morphology. References [18]–[20] present different works
on closed-loop hybrid experiment [21], which is characterized
by the interconnection between biological neural networks
and their artificial counterparts [22]. Neurobiohybrid systems
are more and more studied [23] and even a geographically
distributed bio-hybrid neural network is now possible [24].
To conclude, there is a trade-off between the bio-plausibility
of the model and simplicity and power-consumption of the
circuit. Power-efficient and simple silicon neurons assume
uniform spikes, but biophysical experimental data [25], [30]
suggest the possibility that variety of spikes given to a synapse
is playing a certain role in the information processing in
the brain. Reference [26] indicates that subthreshold varia-
tion in the presynaptic membrane potential also determines
spike-evoked transmission and that membrane voltage might
modulate neurotransmitter release. Reference [27] discusses
the possible real neural coding used in the brain. We think
that being closer to the biology will lead to better results and
allow neurobiohybrid experiments that bio-inspired systems
cannot perform.
II. B IOMIMETIC N EURAL N ETWORKS
A. Qualitative Silicon Neuronal Modeling
Silicon neuron and synapse models for the Brainmorphic
information processing systems have to be designed care-
fully so that they inherit the features in the neuronal activity
as authentically as possible. In many neuromorphic circuits
with simple circuitry, neuronal spikes are assumed to always
have the same shape and magnitude in the I&F-based mod-
els including the Izhikevich model (IZH) [28] and LIF
model [29], although biophysical experiment results suggest
the possibility that the variation in the spikes can be playing
important roles in the information processing in the nervous
system [30]. Conventional silicon neuron models only focus
Fig. 1. Block diagram of our analog VLSI silicon neuron. The spiking
dynamics is produced by the fast subsystem (v- and n-blocks). The q-block
produces slow dynamics that modulates it. The voltage clamp amplifier (top
block) provides a means to draw the v-, n-, and q-nullclines experimentally.
gx (v) and rx (x) circuits generate a shallower sigmoidal curve. fx (v) circuits
generate a steeper sigmoidal curve.
on the timing of spike generation but variability of spike inten-
sity and phase response curve (PRC) are also important in
brain signal processing. That is one reason for developing
a qualitative silicon neuron model [31]. It is a good trade-off
between biological plausibility and low resource implementa-
tion. It can mimic several classes of neuronal activities that
cannot be realized by LIF and IZH models. Its equations are:
dv
C = fv (v) − gv (v) − rn (n) − rq (q) + Iav + IStim (1)
dt
dn
= fn (v) − gn (v) + Ian − rn (n) (2)
dt
dq
= fq (v) + Iaq − rq (q) (3)
dt
where v is the membrane potential, n the variable for fast
dynamics and q the variable for slow dynamics. Ia represents
a constant leak current. f, g and r functions are monotonic
increasing sigmoidal functions of the idealized V–I charac-
teristic curves of the differential pair and transconductance
amplifier.
B. Analog Silicon Neuron on Chip
We have designed an analog ASIC with TSMC 0.25µm
technology [32], [33] that can realize several classes of
neuronal activities including Fast Spiking (FS) with both
Class I and II in the Hodgkin’s classification [34], Regular
Spiking (RS), Square-Wave Bursting (SWB) and Elliptic
Bursting (EB). Fig. 1 describes the block diagram of this
system.
To design the chip, matured CMOS circuitries are used:
differential pair, transconductance amplifier, etc. Field-effect
transistors (FETs) are operated in their subthreshold domain
for low power consumption. To demonstrate the efficiency of
our circuit, we describe Elliptic bursting mode which is one
of the most complex to implement. Conventional silicon neu-
rons cannot reproduce this rhythmic activity. Elliptic bursting
is a class of bursting activity where a Class II spiking system
has slow negative feedback dynamics. The fast subsystem of
LEVI et al.: DEVELOPMENT AND APPLICATIONS OF BIOMIMETIC NEURONAL NETWORKS TOWARDS BMAI
Fig. 2. Experimental result of the analog chip for the elliptic bursting mode.
The yellow curve is the membrane voltage v and the green curve represents
signal q. Time scale is 200ms by division, and voltage scale is 50mV by
division.
Fig. 3. Experimental results of A) RS neuron and B) LTS neuron. Scope
pictures after 12-bit DAC module using SPI communication. Time scale is
200ms by division for A) and 10ms for B), and voltage scale is 20mV by
division for both pictures.
our silicon neuron can realize Class II and we could realize the
elliptic bursting experimentally as shown in Fig. 2. 16 param-
eter voltages have to be tuned for intended neuronal activity.
Our analog silicon neuron circuit consumes only less than
5 nW. For every neuron mode with typical firing rate (less
than 100Hz), the power consumption did not exceed 5nW. It
is in the same range as [11], [35], and [36] but can repro-
duce more classes of neuronal activities. This ASIC could
be used for neurobiohybrid experiments. As geographically
distributed artificial biomimetic neural networks and living
neurons already exist [23], using this ASIC in combination
of other biomimetic platforms with different neuron mod-
els can demonstrate the importance of the spike variation in
neuromorphic device.
C. Digital Silicon Neuron on FPGA
To verify the algorithms before analog implementation, we
designed a digital spiking silicon neuron (DSSN) model that
can be implemented in FPGA. The DSSN model is a qualita-
tive neuronal model designed for efficient implementation in
a digital arithmetic circuit and can simulate several classes of
neuronal activities: RS, FS, Low Threshold Spiking (LTS),
Intrinsically Bursting (IB), EB and SWB classes [37]. The
DSSN model was implemented in a Kintex-7 FPGA with
few resources (386 LUT and 121 FF for one FS neuron,
and 401 LUT and 123 FF for RS neuron, no DSP are used).
Fig. 3 shows hardware implementation of FS and RS neuron.
Our digital system can simulate different classes of neuron
in real-time. The computational cost of the DSSN model is
larger than that of the recent sophisticated Integrate-and-Fire-
based models such as IZH and exponential I&F models, but
smaller than ionic-conductance models. This model is intended
to provide a good trade-off that satisfies the demand for large-
scale neuronal network simulation with biomimetic models.
579
Fig. 4. Architecture of a neuronal network listening incoming spike trains
with hidden patterns. Wji are the synaptic weigh from neuron j (pre-synaptic)
to neuron I (post-synaptic). Inhibitory synapses are represented by white
circles and excitatory ones by black circles.
III. A PPLICATIONS
Here, we present two applications for our biomimetic silicon
neural network. One for AI and one for neuroscience. Both
will be tested first on digital circuits and then implemented in
analog chips.
A. Pattern Recognition
Spike-Timing-Dependent Plasticity (STDP) is a biological
process that adjusts synaptic efficacy between neurons in the
brain. The process adjusts synaptic efficacy based on the rel-
ative timing of a particular neuron’s output and input action
potentials or spikes. Recently, it has been shown how STDP
could play a key role in detecting repeating patterns and in
generating selective response to them [38]. The concept of
STDP has been shown to be an important learning algorithm
for forward-connected artificial neural networks in pattern
recognition.
Particularly in the work presented by Masquelier et al. [38],
it has been shown that repetition of arbitrary spatiotemporal
spike patterns hidden in spike trains can be robustly detected
and learned by multiple neurons equipped with spike-timing-
dependent plasticity (STDP) listening to the incoming spike
trains (Fig. 4). The neurons become selective to successive
coincidences of the patterns.
As used in the work of Masquelier et al. [38], we generated
spikes independently using a Poisson process with a variable
instantaneous firing rate that varies randomly between 0 and
90 Hz. The maximal rate change was chosen so that the neuron
could go from 0 to 90 Hz in 50 ms. Finally, a part of the spike
trains, defined as the ‘pattern’ to be repeated, was replaced for
half input lines into sections of 50ms. We randomly picked
one of these sections and copy the corresponding spikes. As
shown in Fig. 5, four different hidden patterns were gener-
ated (blue, pink, cyan and yellow) with repetition at random
intervals within stochastic Poissonian activity.
The criteria for recognition are the hit rate above 90% and
the false alarm rate below 1 Hz. Using 9 DSSN neurons (LTS
neuron model), 4 patterns and 512 afferent neurons, the suc-
cess rate reaches 88%. Using different family of neurons (FS,
RS or LTS) resulted difference in hit rate (69% for RS for
580 IEEE TRANSACTIONS ON CIRCUITS AND SYSTEMS—II: EXPRESS BRIEFS, VOL. 65, NO. 5, MAY 2018
Fig. 5. Example of 4 patterns detection using 512 afferent neurons and
9 DSSN neurons. On the left side, there is raster plot of the 512 afferent
neurons. On the right side, DSSN neurons are spiking when they detect one
pattern.
512 afferent neurons and 9 output neurons) and demonstrated
that the choice of neuron family is important for such signal
processing.
This brief is expected to be used for pattern recog-
nition directly from the biological neuron recording from
MEA (Micro-Electrode Array) for biomedical applica-
tions [18] and for neurobiohybrid robotic applications [39].
Using this real-time pattern recognition on neuron cul-
ture recordings from MEA with healthy neurons and with
neurological disorder neurons may help neuroscientists to
distinguish the different behaviors on specific disease. As
these patterns are hidden in a noisy environment (sponta-
neous activity), this algorithm will be very efficient for this
case study.
B. Neural Network Mimicking the Hearing System
of Drosophila
The nervous system of Drosophila melanogaster is com-
posed of a relatively small number of neurons, about a hundred
thousand neurons, whose connectivity and physiology are
being addressed by many researchers in experimental neuro-
science. In spite of its simplicity, some experimental studies
revealed its intelligent behavior, for example in classical
conditioning [40] and in courtship behavior using pulse sound
produced by wingbeat [41]. Johnston’s organ is a sensory
organ in the second segment of the antennae, which detects
sound, gravity, and wind [42]. It contains about two hundred
scolopidia, each of is composed of the scolopale cell, the lig-
ament cell, and two neurons (Fig. 6). Axons of the neurons
project to the antennal mechanosensory and motor centers.
One of the neurons selectively responds to oscillatory stim-
ulation (sound) and the other neuron responds to deflection
(wind and gravity). And, it is thought that there is mutual inhi-
bition between the two neurons, because they do not fire at the
same time. In collaboration with Kamikouchi laboratory [42],
we proposed three possible models of Johnston’s organ that
describe the selective response of neurons and the mutual
inhibition.
They are composed of two pairs of a neuron and a cilium
model. We assumed that one of the neurons responding to
oscillatory input has the electrical tuning in analogy with hair
cells found in several species [43]. The other neuron respond-
ing to deflection is a general spiking neuron. Each of the
two cilia has mechanosensitive ionic channels and other ionic
Fig. 6. Schematic of Scolopidia and ionic channels.
Fig. 7. Simulation results of the first model. (a) corresponds to GMET
variation, (b) EX shows variation of ion concentration, (c) and (d) describes
membrane potential VnA and VnB of neuron A and neuron B, respectively.
All variables do not have units as it is from a qualitative model.
channels (assumed ionic channels in Fig. 6). It is not elu-
cidated which types of ionic channels are expressed in the
cilium. When the mechanosensitive ionic channels are open,
the ionic current flows into the cilium and depolarizes it, then
the neuron is also depolarized because the neuron and the cil-
ium are electrically connected. We assumed that the mutual
inhibition of two neurons is realized by the change of ionic
composition in the scolopale space, and considered possible
combinations of ionic channels that can change the ionic com-
position in the scolopale space depending on the activation of
the neurons.
Our simplest model incorporates a single type of ion and
a voltage-gated ionic channel. The ionic composition in the
scolopale space is not elucidated, thus we call it ion X. The
ion X is assumed to be filled in the scolopale space at high
concentration and in the cilia and neurons at low concentration.
As shown in the simulation results in Fig. 7, this model could
produce selectivity between oscillatory and deflective stimuli.
Here GMET is a gating variable of the mechanosensitive ionic
channel and EX is a reversal potential of the voltage-gated
ionic channel. VnA and VnB are membrane potentials of neuron
A and B. While t is from 0s to 2s, an oscillatory stimulus is
applied and neuron A showed resonant spikes and neuron B
did not fire. The deflection is added while t is from 2s to
3s, and neuron B fired repetitively and reversal potential EX
decreased by a massive reduction of the concentration of ion
X in the scolopale space. As the ionic current flowed into the
cilium, neuron A is inhibited.
In the two other models, we investigated the ionic concen-
tration variation in scolopale space and the one-way inhibition
from neuron B to neuron A. In our future works, we will con-
duct biological experiments on the basis of our model, and
improve models toward elucidating information processing of
Johnston’s organ. We will implement our model first in FPGA
and then in analog chip. We expect to design an innovative
sensor system that responds to different kind of input with low
latency and low power consumption.
LEVI et al.: DEVELOPMENT AND APPLICATIONS OF BIOMIMETIC NEURONAL NETWORKS TOWARDS BMAI
IV. C ONCLUSION
The main features of this brief can be summarized in five
points. 1) The creation of a new neuronal model is a good
trade-off between biological plausibility and low resource
implementation. Compared to other I&F-based models, this
model can replicate several classes of neuronal activities and
also action potential shape which is important in brain sig-
nal processing. 2) Then, we designed silicon neurons in an
analog chip in TSMC 0.25 µm technology. This ASIC pro-
vides very low power consumption (5 nW) and can replicate
many neuronal activities such as elliptic bursting mode. 3) We
also implemented silicon neurons in FPGA. We validated
this implementation by mimicking cortical neurons. Then we
used these two systems for different applications. 4) First in
AI with a new algorithm of pattern recognition using just
9 DSSN neurons with STDP and lateral inhibitory connec-
tions for detecting four different patterns. This system can
be used to characterize biological culture on MEA or in asyn-
chronous sensors. 5) Finally, we developed models for hearing
system of Drosophila, to further understand the biological
intelligence and to design new generation of low-power and
low-resource sensors. All these systems are included in the
BMAI project in collaboration with The University of Tokyo
and NEC Corporation.
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